Vous êtes sur la page 1sur 17

Modeling microbial processes in porous media

Ellyn M. Murphy 7 Timothy R. Ginn

Abstract The incorporation of microbial processes Résumé L’introduction des processus microbiologi-
into reactive transport models has generally proceeded ques dans des modèles de transport réactif a générale-
along two separate lines of investigation: (1) transport ment suivi deux voies différentes de recherches: (1) le
of bacteria as inert colloids in porous media, and (2) transport de bactéries sous forme de colloïdes inertes
the biodegradation of dissolved contaminants by a en milieu poreux, et (2) la biodégradation de polluants
stationary phase of bacteria. Research over the last dissous par une phase stationnaire de bactéries. Les
decade has indicated that these processes are closely recherches conduites au cours des dix dernières années
linked. This linkage may occur when a change in meta- indiquent que ces processus sont intimement liés. Cette
bolic activity alters the attachment/detachment rates of liaison peut intervenir lorsqu’un changement dans
bacteria to surfaces, either promoting or retarding l’activité métabolique modifie les taux de fixation/libé-
bacterial transport in a groundwater-contaminant ration de bactéries des surfaces, soit en facilitant, soit
plume. Changes in metabolic activity, in turn, are en retardant le transport bactérien dans le panache de
controlled by the time of exposure of the microbes to polluant de l’eau souterraine. Des changements de
electron acceptors/donor and other components l’activité métabolique peuvent en retour être contrôlés
affecting activity. Similarly, metabolic activity can affect par le temps d’exposition des microbes à des donneurs
the reversibility of attachment, depending on the resi- ou à des accepteurs d’électrons et à d’autres composés
dence time of active microbes. Thus, improvements in affectant cette activité. De façon similaire, l’activité
quantitative analysis of active subsurface biota necessi- métabolique peut affecter la réversibilité de la fixation,
tate direct linkages between substrate availability, en fonction du temps de séjour des microbes actifs.
metabolic activity, growth, and attachment/detachment Ainsi, les améliorations de l’analyse quantitative des
rates. This linkage requires both a detailed under- organismes souterrains nécessitent d’établir des liens
standing of the biological processes and robust quanti- directs entre les possibilités du substrat, l’activité méta-
tative representations of these processes that can be bolique, la croissance et les taux de fixation/libération.
tested experimentally. This paper presents an overview Cette liaison nécessite à la fois une compréhension
of current approaches used to represent physicochem- détaillée des processus biologiques et des représenta-
ical and biological processes in porous media, along tions quantitatives robustes de ces processus qui puis-
with new conceptual approaches that link metabolic sent être testées expérimentalement. Cet article
activity with partitioning of the microorganism between présente une revue des approches courantes utilisées
the aqueous and solid phases. pour représenter les processus physio-chimiques et
biologiques en milieu poreux, en même temps que de
nouvelles approches conceptuelles qui associent l’acti-
vité métabolique à la répartition des micro-organismes
entre les phases aqueuse et solide.

Received, January 1999 Resumen La incorporación de los procesos microbianos


Revised, June 1999, July 1999 en los modelos de transporte reactivos ha procedido
Accepted, October 1999 tradicionalmente a lo largo de dos líneas de investiga-
Ellyn M. Murphy (Y) ción independientes: (1) el transporte de bacterias
Interfacial Geochemistry Group, Pacific Northwest National como coloides inertes en el medio poroso, y (2) la bio-
Laboratory, MSIN K3–61, P.O. Box 999 degradación de los contaminantes disueltos por una fase
Richland, Washington 99352, USA estacionaria de bacterias. En los últimos años se ha
e-mail: ellyn.murphy6pnl.gov
Fax: c1-509-3756954 comprobado que estos dos procesos están muy interre-
lacionados. En concreto, un cambio en la actividad
Timothy R. Ginn
172 Everson Hall, Department of Civil and Environmental
metabólica puede alterar la relación de adsorción/
Engineering, University of California Davis desorción de las bacterias, favoreciendo o retardando
Davis, California 95616–5294, USA el transporte bacteriano en un penacho de contamina-

Hydrogeology Journal (2000) 8 : 142–158 Q Springer-Verlag


143

ción. A su vez, los cambios en la actividad metabólica 1994), growth is often eliminated in column or field
están controlados, entre otros factores, por el tiempo experiments of biocolloid transport (Champ and
de exposición de los microbios a los receptores/ Schroeter 1988; Harvey et al. 1989, 1993; Bales et al.
donantes de electrones. Además, la actividad metaból- 1995).
ica puede afectar la reversibilidad de la adsorción, en Quantitative representations of microbial processes
función del tiempo de residencia de los microbios in saturated porous media are numerous; however, the
activos. Así, el análisis cuantitativo de la actividad coupling of these processes in dynamic contaminant
subsuperficial biótica necesita de un estudio detallado systems is not well understood. Under oligotrophic
de las conexiones entre disponibilidad del substrato, (carbon-limiting) conditions in aquifers, microbial
actividad metabólica, crecimiento y relación de adsor- growth is limited and most of the biomass is associated
ción/desorción, lo que requiere tanto un conocimiento with the solid phase (Harvey et al. 1984; Hirsch and
de los procesos biológicos, como una representación Rades-Rohkohl 1988; Kölbel-Boelke et al. 1988; Godsy
cuantitativa robusta de dichos procesos, comprobable et al. 1992; Albrechtsen 1994). In these growth-limited
experimentalmente. Este artículo presenta una revisión environments, physical processes likely dominate trans-
de los métodos actuales para representar los procesos port of that portion of the biomass in the aqueous
fisioquímicos y biológicos en el medio poroso, además phase. In contrast, in nutrient-rich environments, such
de nuevas metodologías para relacionar la actividad as contaminated aquifers, field observations consis-
metabólica con el fraccionamiento de los microorgan- tently indicate a higher level of biomass in the aqueous
ismos entre las fases sólida y acuosa. phase. In a contaminated portion of the Cape Cod
aquifer in Massachusetts, USA, Harvey et al. (1984)
Key words contamination 7 bacterial transport 7 report that the aqueous biomass increased by an order
numerical modeling 7 microbial processes of magnitude, whereas the concentration on the sedi-
ments remained approximately the same. Harvey and
Barber (1992) observed 1 30% of total biomass free-
Introduction living in a sewage-contaminated plume; Godsy et al.
Progress in modeling microbial processes in porous (1992) note that 90% of total biomass in a creosote-
media is essential to improving our understanding of contaminated aquifer was attached, but 49% of
how physical, chemical, and biological processes are (creosote-degrading) methanogens were in the aqueous
coupled in groundwater and their effect on ground- phase. Likewise, at an in-situ bioremediation study at
water-chemistry evolution, bioremediation, and the the Savannah River Site in Georgia, USA, the propor-
reactive transport of contaminants and bacteria. Much tion of methanotrophs, which were stimulated to
of the emphasis to date has been on quantitative repre- degrade chlorinated hydrocarbons, increased by as
sentations of either the kinetics of contaminant degra- much as five orders of magnitude in the aqueous phase
dation or the physical (or physicochemical) processes (USDOE 1993). These observations are consistent with
that affect the transport of bacteria in porous media, specific recognition of growth-induced partitioning to
primarily because these issues are more tractable to the the aqueous phase (Jenneman et al. 1985, 1986;
microbiological and hydrologic transport fields. Reynolds et al. 1989; Sharma et al. 1993). Such condi-
Whether the modeling objective is to understand the tions indicate a greater propensity for transport of
biodegradation of contaminants or the movement of native microbes under natural hydraulic gradients or
bacteria, the processes that must be considered are the under pumping as part of an accelerated bioremedia-
same. These processes are generally divided into physi- tion strategy when growth is a factor.
cochemical and biological. The physicochemical pro- This article first briefly reviews physicochemical and
cesses include advection, diffusion, dispersion, exclu- biological microbial processes of relevance to subsur-
sion, straining, and physical filtration. The physico- face phenomena on short time scales (e.g., bioremedia-
chemical processes are primarily based on the structure tion) and the quantitative representations that have
and properties of the groundwater flow system and been developed for these processes. Then, experiments
porous media. Consequently, most reactive transport are discussed that link the physicochemical and biolog-
models incorporate some of the major physical pro- ical processes (specifically, growth and attachment of
cesses, and these processes have been the focus of bacteria) and new approaches for quantitatively
numerous experimental and numerical modeling describing these coupled processes in reactive transport
studies on colloid and biocolloid research. In contrast, models.
the biological processes of growth/decay, chemotaxis,
predation, physiological adaptation (survival), and
adhesion or active detachment are characteristics of the Background on Reactive Transport Modeling
bacterial population and by comparison have received of Coupled Processes
little attention in field-scale hydrogeologic transport The terminology used in interdisciplinary studies is
models. Although many researchers readily acknowl- sometimes more confusing than the actual processes
edge the importance of growth processes in transport involved. Chemical reactions that involve different
(Harvey et al. 1984; Hornberger et al. 1992; Tan et al. phases (e.g., aqueous and solid) are termed heteroge-

Hydrogeology Journal (2000) 8 : 142–158 Q Springer-Verlag


144

neous, and reactions that involve a single phase are face biotic activity are discussed in some detail. The
termed homogeneous. Unfortunately, aquifer proper- equally important issue of simulating a complex set of
ties that vary spatially are also termed heterogeneous, these processes within the framework of a conventional
whereas properties that are constant in space are flow and transport model is not the focus of this review
termed homogeneous. Adhesion in this paper refers to but is relevant and therefore is briefly mentioned
physiologically driven attachment of a microorganism here.
to a surface, an active process initiated by the microor- One of the aspects of a reaction system that is most
ganism. In this regard, this definition of adhesion is important for modeling fate and transport in porous
much narrower than that of others who may include all media is the range of the reaction rates. Reacting
intermolecular and surface forces in the definition of mixtures can involve a variety of individual reactions,
adhesion (for this more generic classification, the term each with a particular rate, and the set of rates can
attachment is used). Partitioning refers to the phase range from the very slow to the very fast to the instan-
separation of a microbial community and is equivalent taneous. Instantaneous reactions (that is, transforma-
to attachment/detachment. Partitioning is a general term tions that occur relatively instantaneously when viewed
that does not denote a specific process or mechanism on the time scale of transport processes) involve equi-
that controls the distribution of bacteria between the librium relations between interacting chemicals and are
mineral and aqueous phases in a flowing system. termed equilibrium reactions. Reactions that involve a
Kinetic attachment/detachment rates may arise from rate that is on the same time scale as transport (that is,
growth or metabolic activity, but they do not vary transformations that have a relatively finite rate) are
between resting and active cells. Dynamic partitioning termed non-equilibrium, or kinetic, reactions. In
refers to a temporal change in the attachment/detach- general, the majority of subsurface biotic transforma-
ment kinetics as a function of growth activity. Substrate tions are non-equilibrium and have similar time scales
denotes the energy source/electron donor for biode- (e.g., rates within 1–2 orders of magnitude). Because
gradation and does not refer to the solid-phase aquifer these rates are similar, these problems are easily
materials. handled with conventional reactive-transport numer-
Reactive transport models are no more than a ical-solution schemes such as operator splitting (e.g.,
collection of process representations (physical, chem- Chilakapati et al. 1998).
ical, and biological) of varying accuracy and sophistica- However, some biotic and chemical transformations,
tion that are used to describe a coupled dynamic such as solute adsorption, occur in much shorter time
system. The relative importance of individual processes scales. When this occurs, the reaction rates of the
can only be assessed through experimentation and data coupled system may span many orders of magnitude
collection. More often than not, key processes are (e.g., contain both kinetic and equilibrium transforma-
either poorly understood or lumped into a single tions), and the system must be solved using increasingly
expression of mass-transfer rate in reactive transport smaller time steps over a longer time frame to capture
models. Consequently, parameter fitting is often the effects of the fast reactions upon the slower kinetic
invoked to fit, sometimes non-uniquely, a set of simpli- and transport transformations. Such systems are diffi-
fied process representations to describe a particular cult to simulate because the short time step required to
system. Because isolation of the effects of individual accurately capture the fast reactions can render the
processes on the overall system dynamics typically computational costs prohibitively expensive. One
requires sequential data analyses and experimental approach to such systems is to treat the “fast” reactions
design, an iterative theoretical modeling and experi- as occurring instantaneously, i.e., as equilibrium trans-
mental approach that includes both laboratory and formations. The resulting model description contains a
field studies is expected to yield the greatest advances combination of differential and algebraic equations,
in our understanding of these complex, coupled proc- i.e., a “DAE system.” Specialized approaches for
esses. numerically solving reactive transport systems under
This section summarizes some of the important both fully kinetic formulations (using operator split-
issues in modeling the coupled processes involved in ting) and mixed kinetic-equilibrium formulations (using
subsurface microbial activity, ranging from model specialized DAE solvers such as DASSL; Petzold 1983)
construction to model solution. These are treated in are available in the public codes HYDROGEOCHEM
reverse order, beginning with the challenges in solving (Yeh and Tripathi 1989) and RAFT (Chilakapati 1995).
fate and transport models involving multiple rates of The reader is referred to a more thorough review of the
reactions, and concluding with broad summaries of the issue of reaction systems in Steefel and MacQuarrie
constitutive theories used to develop mechanistic (1996).
expressions for particular processes.

Structure of Subsurface Biomass


Multiple Rates of Reactions The constitutive theory used to upscale the processes
In the subsequent sections, individual reaction-rate occurring at the cell scale (to the degree that they are
expressions for various processes involved in subsur- understood) to the bulk-phase scale depends on the

Hydrogeology Journal (2000) 8 : 142–158 Q Springer-Verlag


145

nature of the various reactions involved in subsurface focus of numerous experimental and numerical
biotic processes, including their speeds and reversi- modeling studies. These important processes provide
bility. The description of these cell-scale reactions is the framework for bacterial transport and reaction in
highly dependent on the structure of the biological porous media. Indeed, the impact of biological proc-
phase. The basic representation of the structure of a esses in a flowing groundwater system can only be eval-
biological phase in porous media, however, is a matter uated within this physicochemical framework. There-
without consensus, as noted in the exchanges of Baveye fore, the physicochemical processes are defined and
and Valocchi (1991), Widdowson (1991), Baveye et al. briefly reviewed in this section, and descriptions are
(1992), and Jaffe and Taylor (1992). Typically, in struc- summarized in Table 1. Readers are referred to reviews
tured biomass models, the biophase is represented as by McDowell-Boyer et al. (1986) and Harvey (1991) for
either a (1) continuous biofilm on the solid surface more thorough discussions of physicochemical proc-
(Taylor and Jaffe 1990; Taylor et al. 1990), or (2) esses.
discontinuous patchy film (Widdowson et al. 1988; Microbes undergo convective transport as a particu-
Vandevivere and Baveye 1992; Rittman 1993). Mathe- late or a dissolved species moving with the porewater
matically, such structured biofilm models are often whose velocity is governed by the hydraulic pressure
associated with a diffusion limitation on the transport gradient, porosity, and permeability distribution
of solutes from aqueous phase to biomass phase, where [Table 1, Eqs. (1) and (2)]. The occurrence of nutrient
they can be degraded (Wood et al. 1994). and/or electron acceptor as a solute undergoing trans-
In the so-called unstructured biomass models, no port may be coupled to the transport process through
assumptions are made on the biophase structure the effects of these constituents on the fluid properties
(MacQuarrie et al. 1990; Sudicky et al. 1990; Zysset et of density and viscosity. Convective transport in porous
al. 1994), and the biomass is treated as a suspended but media is also associated with hydrodynamic dispersion,
kinetically sorbing/desorbing species (MacQuarrie et al. an enhanced mixing process arising from the tortuosity
1990; Zysset et al. 1994). Therefore, in unstructured of the convective paths compounded by molecular-
models the biomass is a fully penetrable volumeless scale (diffusional) mixing. The resulting convective-
component that assumes that a linear relation exists dispersive transport terms are shown in Eq. (3) of
between mass of substrate consumed and mass of Table 1.
biomass produced and that no diffusion limitations Straining and physical filtration represent the
affect the transfer of substrate mass from solution into removal of microbes from solution by physical
the biomass. This approach has been taken in past (geometric and intermolecular/surface) forces.
column studies that focus on bacterial transport Straining is the trapping of microbes in pore throats
(Lindqvist et al. 1994; Tan et al. 1994) and in studies of that are too small to allow passage and is exclusively a
intermediate-scale flow cells that focus on active result of pore geometry (Corapcioglu and Haridas
degradation and growth and coupled transport 1984). Prediction of mass removal by straining, based
(Murphy et al. 1997b). on purely geometric relations between the effective
The degree to which the particular structural diameter of biocolloids and the diameter and packing
assumption impacts the resulting expressions for reac- (coordination number) of grains, is not significant
tion transformation is incompletely understood. For where the colloid diameter is less than 5% of the
example, the process of metabolic lag (Wood et al. porous-medium grain diameter (Sakthivadivel 1966,
1995), discussed below, may be experimentally indistin- 1969; Herzig et al. 1970; Corapcioglu and Haridas 1984;
guishable from a substrate diffusion limitation through McDowell-Boyer et al. 1986; Harvey and Garabedian
a biofilm. Both processes result in a delay in the onset 1991).
of degradation, and the correct labeling of the process Physical filtration is the removal of particle mass
may or may not have an effect on the ultimate amount from solution via collision with and deposition on the
of contaminant degraded. Recently, several studies porous medium; here, the term includes both sedimen-
have used volume averaging to formally upscale the tation [Table 1, Eq. (4)] and attachment [Table 1,
processes of mass transport and reactions in biofilms Eqs. (5) and (6)]. Sedimentation is filtration due to
(Wood and Whitaker 1998, 1999, in press). Continuing gravity (Corapcioglu and Haridas 1984; McDowell-
investigations such as these may help to refine our Boyer et al. 1986) and depends on particle buoyancy
understanding of the role of biofilm structure in the (Wan et al. 1995). Many natural bacteria and viruses
subsurface (Characklis and Marshall 1990). are neutrally buoyant, in which case sedimentation is
negligible. However, cultured microorganisms are typi-
cally larger and sometimes denser than their native
Physicochemical Processes counterparts (Harvey et al. 1997) and may involve size-
Most reactive transport models that consider microbial able buoyancy-driven filtration.
processes incorporate physicochemical processes, such Physical forces resulting in attachment (Brownian,
as advection, dispersion, straining, and physical filtra- electrostatic, van der Waals, and pore-water hydrody-
tion. Unlike the biological processes, physicochemical namic) are the dominant mechanisms for partitioning
processes affecting microbial transport have been the of biocolloids to solid media and have received

Hydrogeology Journal (2000) 8 : 142–158 Q Springer-Verlag


146

Table 1 Quantitative representations of physicochemical processes

Description of process Quantitative representation Limitations

Flow: groundwater velocity V(x) is 1. uV(x)pPK=h(x) Unknown multiscale variability of


related to pressure gradient through permeability incurs unknown
Darcy’s law (1) and is governed by 2. =7(uV(x))pq(x) non-uniformities in convections.
water mass conservation law (2), with
water source q(x). Fluid density r and
viscosity m are assumed constant.

Transport: solutes and microbes iCi Unknown non-uniformities in


undergo convective and dispersive mass
fluxes, expressed in partial mass-balance
3.
it )
transport
pP=7(Ci(Vcvsẑ)c=7[D7=(Ci)] convective water flux complicate
tracking of solution substrates,
terms (3) for concentration C of arbi- (rsPr)gds electron acceptors, and microbes.
trary (subscript i) species. 4. vs p
Convective transport at groundwater 18m Fails to capture pore-scale insta-
velocity V may be augmented by micro- bilities arising from density/
organism density-induced sedimentation viscosity, which can greatly
velocity, ns (for cultured microbes; increase mixing and thus biode-
Harvey et al. 1997), approximated here gradation.
by Stokes’ law for descent of a sphere
of density rs and diameter ds, and
viscosity m (4).

Physical microbial attachment/detach- iCmm Non-mechanistic, essentially


ment processes: physical partitioning of
microbes between aqueuos (5) and
5.
it ) phys. part.
pPKf CmmcKrCim empirical model fails to capture
potentially important cause-effect
attached (6) phases is quasi-empirically iCim relations for microorganisms
given by various first- or second-order
6.
it )
phys. part.
pKf CmmPKrCim
actively involved in biodegrada-
models (first-order shown here). Cmm tion.
and Cim equal concentration of mobile iCim
microbes and immobile microbes,
7.
it )
phys. part.
pKf vCmm
respectively. When physical processes See clarification of h, which
are dominated by passive colloid filtra- 3 (1Pu) appears here in Eq. (8), in Logan
8. Kf p ah
tion (7) (Rajagopalan and Tien 1976), 2 dc et al. (1995).
Kf in (8) includes sticking (a) and colli-
iCmm (C max
im PCim)
sion (h) factors that depend on v and
particle properties, and Krp0. In (9),
9.
it )
phys. part. in
pPKf
C max
im
CmmcKrCim
saturable sites.
site saturation limits attachment of
bacteria; where C im
max is maximum reten-
tion capacity of saturable sites.

substantial attention, partly as a result of their quantita- 1990; Mills et al. 1994). The major mineral component
tive tractability (cf. review by McDowell-Boyer et al. of most aquifers, quartz, is predominantly negatively
1986). A typical model is shown in Table 1, Eqs. (5) and charged, as are most bacteria; thus, the hydrodynamic
(6). The microbe is treated as a spherical particle and attractive forces must overcome the repulsive elec-
moving through a uniformly packed homogeneous bed trostatic force for bacterial immobilization to occur.
of spherical grains (Herzig et al. 1970; Shaw 1970; Tien Sand grains coated with iron hydroxide have positive
et al. 1979). The microbial mass removal from the surface charges, thus reversing the electrostatic force
aqueous phase has also been cast in terms of pore- from repulsive to attractive and increasing the likeli-
water velocity, viscosity, and density; media grain size; hood of microbial attachment. Hydrophobic interac-
and media porosity [Table 1, Eq. (7)]. This approach of tions can also result in sorption of microorganisms
colloid-filtration theory incorporates a sticking coeffi- (Fletcher and Loeb 1979; van Loosdrecht et al. 1987;
cient (a) and collision factor (h) in the forward attach- Fletcher 1991; McCaulou et al. 1994). The reversibility
ment rate [Kf; Table 1, Eqs. (7) and (8)]. The resulting of physical filtration, via reduction in solute ionic
relations are well known (de Marsily 1986) and have strength (Scholl et al. 1990; McDowell-Boyer 1992;
been widely applied to microbial transport (Harvey et Bales et al. 1995), is not inherent in models based on
al. 1989; Harvey and Garabedian 1991). filtration theory, because the filtration models repre-
Previous research has demonstrated that attachment sent irreversible deposition only under conditions of
is influenced by (1) solution ionic strength through the uniform flow direction and fixed solution chemistry.
effect on electrostatic interactions (Sharma et al. 1985; Thus, treatment of detachment is entirely absent in
van Loosdrecht et al. 1989; Scholl et al. 1990; several filtration-theory analyses of microbial transport
McDowell-Boyer 1992; Shonnard et al. 1994; Tan et al. (e.g., Jewett et al. 1995). The evidential significance of
1994); (2) pH (McEldowney and Fletcher 1988); and detachment processes in experimental studies,
(3) mineralogy (Fletcher and Loeb 1979; Scholl et al. however, has led to incorporation of a more-or-less

Hydrogeology Journal (2000) 8 : 142–158 Q Springer-Verlag


147

empirical detachment term. The resulting models use kinetic equations are used for modeling different types
some combination of sites undergoing equilibrium of microbial metabolisms (Molz et al. 1986; Widdowson
attachment; sites undergoing irreversible kinetic attach- et al. 1988; Kindred and Celia 1989; Taylor and Jaffe
ment, in accordance with filtration theory; and sites 1990; Kinzelbach et al. 1991; Wood et al. 1994; Zysset et
undergoing kinetic-reversible attachment (Bales et al. al. 1994; Ginn et al. 1995; Corapcioglu and Kim 1996;
1991; Harvey and Garabedian 1991; Lindqvist and Koch 1998).
Bengtsson 1991; Mills et al. 1991; Hornberger et al. For example, Table 2 shows the evolution equations
1992; Kinoshita et al. 1993; McCaulou et al. 1994). for a solute [Eq. (1)] undergoing aerobic degradation
Some researchers suggest augmenting the first-order with consumption of electron acceptor [oxygen;
kinetic attachment model with a non-linear governing Eq. (2)]. The concurrent growth of aqueous and
factor intended to represent the attachment-limiting attached biomass is shown in Eqs. (3) and (4) of Table 2
effect of site saturation at saturable sites [Table 1, (Murphy et al. 1997b). Such studies account for
Eq. (9)], while maintaining a linear attachment rate at biomass growth through a simple linear conversion of
other sites and a linear detachment rate overall (Lind- mass of nutrient degraded to biomass increase [see the
qvist et al. 1994; Tan et al. 1994; McCaulou et al. 1995; factors F and Y in Eqs. (1) and (2), where F is the mass
Saiers and Hornberger 1996), or a residence-time ratio of electron acceptor per substrate consumed, and
controlled detachment rate (Johnson et al. 1995). Y is the yield coefficient or biomass per mass
In addition to physical filtration, size exclusion substrate]. Monod kinetics generally work well for
results in differential bacterial and ion-tracer break- bacterial populations having low saturation constants
through times in column (Hornberger et al. 1992; for organic substrates, as is normally the case in subsur-
Mayotte et al. 1996) and field experiments (Wood and face environments (Harvey and Widdowson 1992). The
Ehrlich 1978; Pyle and Thorpe 1981; Harvey et al. Monod formulation was originally based on Michaelis-
1989). Size exclusion is the phenomenon of transported Menten enzyme kinetics, and the Monod coefficients
particles moving faster than the pore water, or at least and formulation itself are quasi-empirical (Button
faster than the average pore-water velocity, as indi- 1993).
cated by the breakthrough of an inert molecular-scale Several enhancements have been incorporated into
tracer. Pore-water velocity within a capillary or pore Monod kinetics to address limitations in the original
throat is generally parabolically distributed, in which formulation. For example, the Monod formulation
the maximum velocity occurs at the centerline and represents growth rate as depending only on the instan-
velocity at the pore walls is equal to zero (de Marsily taneous concentration of substrate and electron-
1986). Conventional transport theory assumes that acceptor and does not account for a lag in the response
molecular-scale solutes thoroughly sample the full of growth rate to changes in substrate concentration,
distribution of velocities. Microbes and large colloids, nor does it account for the historical variations in
by virtue of their size, preferentially experience the substrate concentration (Powell 1967). Metabolic lag is
higher velocities near pore centerlines, yielding an essentially the delay in biodegradation of a contami-
average velocity that is higher than that of a dissolved nant between the time that the contaminant is first
tracer. Thus, microbes can precede the tracers down- encountered and when it is utilized. This delay gener-
gradient. The occurrence of exclusion typically requires ally results from the time it takes to synthesize enzymes
the bacterial diameter to be ~1% of the porous necessary to take up or metabolize the contaminant.
medium-grain diameter, which is common for transport Degradation rates in natural media may reflect
in sandy aquifers (Dodds 1982; de Marsily 1986). When different levels of microbial metabolic activity, which
the electrostatic forces between the media and colloid depend on the history of nutrient availability to the
are repulsive, as is the case with negatively charged microorganism and on the history of the growth of the
microbes in negatively charged quartzitic media, the microorganism (e.g., Wood et al. 1995). Different
force field tends to channel the microbes closer to the approaches to accounting for the resulting lag in micro-
pore-throat centerlines and away from the walls (anion bial degradation under a change from nutrient-limiting
exclusion; de Marsily 1986). Thus, the effect may be to nutrient-rich conditions are described in Wood et al.
drastically more pronounced at larger observation (1995) and in Ginn (1999). The Wood et al. (1995)
scales in natural media, as has been reported in some formulation [Table 2, Eq. (5)] is based on the threshold
experiments (Pyle 1979; Enfield and Bengtsson 1988; concentrations of substrate and electron acceptor,
Harvey et al. 1989, 1993; Shonnard et al. 1994). which can be experimentally determined. This formula-
tion works quite well for attached microbial popula-
tions; however, when the microbes partition between
Biological Processes phases, their metabolic potential arises as a distributed
Growth and decay processes are generally linked to quantity, which is accounted for by using the approach
spatial and temporal variations in nutrient flux through of Ginn (1999), described below.
Monod (substrate-limited) or dual-Monod (substrate Endogenous respiration is the process by which
and electron-acceptor limited) microbial reaction kine- microorganisms consume cell reserves in the absence of
tics (Monod 1949). Several forms of Monod-based substrate and thereby continue to use a terminal elec-

Hydrogeology Journal (2000) 8 : 142–158 Q Springer-Verlag


148

Table 2 Quantitative representations of biological processes

Description of process Quantitative representation Limitations

Biodegradation: solution substrates iCc lmM C0 Cc Difficult to distinguish kinetic


(Cc) and electron acceptors (C0)
undergo transformations by both
1. )
it bio deg’n
pP
Y
(CmmcCim)7 5
(K0cC0) (KccCc) 6 rates for attached and unat-
tached microorganisms.
aqueous microbes (Cmm) and iC lmM C0 Cc
it ) 5 6
0
2. pPF (CmmcCim)7
attached microbes (Cim). In simplest bio deg’n Y (K0cC0) (KccCc)
case, transformations of substrate (1)
and electron acceptor (2) are limited
by nutrient availability expressed by
Monod {bracketed} factors. Ypyield
coefficient (biomass/mass substrate)
and Fpelectron acceptor/mass
substrate.

Microbial growth: substrate and elec- iCmm C0 Cc No mechanistic connection


tron acceptor degradation induces
changes in biomass of both aqueous
3.
it )
bio deg’n
pPlmMCmm7 5 (K cC )(K cC ) 6
0 0 c c
between growth and microbial
detachment.
(Cmm) and attached (Cim) microbes; iCim C C During growth-mediated
mMpspecific growth rate.
4.
it )
bio deg’n
pPlmMCim 75
(K cC ) (K cC ) 6
0
0

0 c
c

c
transport, microorganisms
enter aqueous stream as a
result of cell division.
t
Metabolic lag (l) is the delay Interaction with diffusive
between time when a microbe first 5. l(t)p # K(t)CS(tPt) dt processes unknown, i.e., what
0
encounters an electron donor and terms described in Wood et al. (1995) is threshold level of substrate
when it is able to build the enzyme required for induction?
systems required to use the electron Unable to incorporate with
donor. partitioning microbes.

Endogenous respiration (b0) is the iC0 C0 This representation lumps


process where microbes consume cell
reserves in absence of donor and
6.
it )
endo. resp.
pPb0(CmmcCim)7 5 (K cC ) 6
0 0
both (static) baseline mainte-
nance with endogenous respi-
continue to use an electron acceptor. ration.
Endogenous respiration is
dynamic and likely depends
on concentration of storage
reserves.

Random motility and chemotaxis are iCmm Chemotactic motility models


microbial transport fluxes driven by
both diffusion-like random motions
7.
it )
motility
p=7(dm=CmmPCmmvx) are quasi-empirical and
mainly fitted to monoclonal
and automobility (vx) directed cultured populations – results
toward increasing substrate concen- for natural environment
trations (upgradient; e.g., Barton and strains are few.
Ford 1995). dm is the random
motility coefficient.

Competitive inhibition occurs in iCc lmM Cc C0 Invariance of inhibition


mixed populations that use the same
nutrients (Bailey and Ollis 1986;
Semprini et al. 1991), where CI is
8.
it
pP
Y
(CmmcCim)
3 KccCc c
CI
KI
4 3K cC 4
0 0
constant requires steady-state
assumption for competitive
population.
inhibitor concentration and KI is
inhibition constant.

Cometabolism is the transformation iC2 k2 C2


of a compound that does not yield
energy or growth. C2 is concentra-
9.
it
p P(CmmcCim)
K2 1 21 C cK 2
2 2

tion of non-growth contaminant; k2/


K2 is a ratio of constants equivalent
to second-order rate constant.

tron acceptor (TEA). The term maintenance respiration between endogenous respiration and maintenance
usually refers to a baseline respiration rate in the pres- energy is not universally accepted (Herbert 1958; Pirt
ence of substrate that provides cell energetic require- 1975; Smith et al. 1986; Smith 1989; Hess et al. 1996).
ments for survival or preservation of a particular cell Although maintenance energy is important and highly
state, which is not associated with growth (Bailey and relevant to questions regarding the long-term survival
Ollis 1986; Beeftink et al. 1990). This distinction of microorganisms in oligotrophic environments, it is

Hydrogeology Journal (2000) 8 : 142–158 Q Springer-Verlag


149

probably less important than endogenous respiration in was twice the rate of attached bacteria and that the
the description of biodegradation and microbial trans- rates were further halved in a flowing system. Further
port in a dynamically evolving contaminant plume. modeling studies supported by experimental evidence
Subsurface microorganisms may have highly vari- are needed before general conclusions can be made about
able endogenous respiration rates (Novitsky and phase-dependent microbial reactions in porous media.
Morita 1977) that depend directly on nutrient exposure Additional biological processes affecting microbial
history and hence the level of cell reserves. The cell transport are expressed through the growth/decay
reserves are highest after a sustained growth phase, and process and include active adhesion/detachment,
even in the absence of contaminant degradation, the survival, and chemotaxis. Active adhesion/detachment
terminal electron acceptor continues to be depleted. is treated here as a biological-driven process. Several
Therefore, endogenous respiration affects the redox studies report that microorganisms exhibit active adhe-
conditions of the groundwater long after the substrate sion/detachment processes that may be a response to
has disappeared (Murphy et al. 1997b). Experimental local nutrient availability (Dawson et al. 1981; Kjelle-
evidence suggests that the initial period of starvation, berg and Hermansson 1984; van Loosdrecht et al.
after substrate disappearance, is characterized by an 1990), survival mechanisms (Dawson et al. 1981;
increase in endogenous respiration (Kjelleberg et al. Wrangstadh et al. 1990; Gilbert and Brown 1995), and/
1987), possibly due to production of starvation proteins or growth (Jenneman et al. 1985, 1986; Reynolds et al.
(Smigielski et al. 1989; Matin 1990; Oliver et al. 1991). 1989; Sharma et al. 1993). No generally accepted quan-
An increase in cell division has also been noted at the titative treatment of active adhesion/detachment pro-
onset of starvation (Novitsky and Morita 1976) and cesses exists. The distinctions between a microor-
may be a survival response to increase the surface-to- ganism’s response to nutrient availability, survival
volume ratio of the cell. Sometime after the onset of stress, and growth are not necessarily separable nor are
starvation, endogenous respiration sharply decreases they independent processes.
and these minimal rates may be associated with a Microorganisms that have the capability to move in
dormancy phase (Novitsky and Morita 1977; Kapre- response to a chemical gradient are termed chemo-
lyants et al. 1993). Under these conditions, respiration tactic. Both taxis (possessing motility genes) and
may only be used to maintain basic cell structures and chemotaxis have been cited as potential means of trans-
repair DNA. The rate of endogenous respiration can be port for subsurface organisms (Corapcioglu and
highly variable, yet in biodegradation models endoge- Haridas 1984; Jenneman et al. 1985; Reynolds et al.
nous respiration is often combined with maintenance 1989; Mercer et al. 1993; Barton and Ford 1995). Quan-
respiration and usually treated as a constant parameter titatively, taxis is an effective diffusive flux for microor-
rather than a dynamic process linked to cell reserves ganisms that depends on the local spatial gradient in
and physiological state. A typical quantitative formula- aqueous microorganism concentration, and chemotaxis
tion is shown in Table 2, Eq. (6). Mechanistic formula- is a flux of microorganisms associated with the gradient
tions of dynamic endogenous respiration based on both in nutrient supply. These two terms are shown in order
nutrient history (e.g., cell reserves) and threshold elec- in Table 2, Eq. (7). Chemotaxis requires energy and
tron donor/acceptor concentrations would require an therefore is closely linked to growth processes in
accounting of the time a microorganism has been porous media. In oligotrophic environments, nutrient
exposed to nutrients, a capability lacking in current gradients are quite small and are likely to be associated
modeling approaches. with either preferential flow paths (if the nutrients arise
Several modeling studies have ignored the explicit from recharge) or solid-phase chemical heterogeneity.
presence of bacteria in both aqueous and attached Chemotaxis may be a very important transport mecha-
phases and their dual role in contaminant removal nism in these low-nutrient environments. Mercer et al.
(Molz et al. 1986; MacQuarrie et al. 1990; Chen et al. (1993) observed that bacteria subjected to oligotrophic
1992). A few studies have considered the presence of conditions displayed enhanced chemotactic response.
cells at various phases, but they have also assumed A contaminant plume results in large chemical
microbial reaction kinetics to be independent of the gradients that may also contribute to microbial trans-
phase in which cells reside (Taylor and Jaffe 1990; port via chemotaxis. Like virtually all microbial charac-
Zysset et al. 1994; Corapcioglu and Kim 1996; Murphy teristics, tactic capability varies widely among organ-
et al. 1997b). This assumption may not be adequate, isms. Therefore, these organism-specific transport char-
because cells attached to the solid phase may behave acteristics have not been incorporated into predictive
differently from the cells suspended in the aqueous models of microbial transport applicable to field-scale
phase. Harms and Zehnder (1994) provide data indi- hydrogeological applications. However, much work has
cating that attached microbes degrade substrate more been done on developing basic models of chemotactic
slowly than their aqueous-phase counterparts, and they transport of cell populations in response to gradients in
attribute the difference to limitations on substrate aqueous-phase nutrients. These efforts and the
transport by diffusion to the cell surface due to the resulting models are beyond the current scope of this
presence of the solid phase. Eisenmann et al. (1998) paper; the interested reader is referred to the review of
report that the rate of predation of aqueous bacteria Ford and Cummings (1998).

Hydrogeology Journal (2000) 8 : 142–158 Q Springer-Verlag


150

Several other processes become important when


analyzing multiple interacting microbial populations.
Population interactions that have received the most
attention are competition, predation, and come-
tabolism (Bailey and Ollis 1986; Semprini et al. 1991;
Mohn and Tiedje 1992; Semprini and McCarty 1992;
Harvey et al. 1995; Lang et al. 1997; Smith and McCarty
1997; Smith et al. 1997). Although competition has a
much broader definition in population dynamics, in
terms of representing this process in Monod kinetics,
competition is simply when two or more microbial
species compete for the same nutrients. A Monod
formulation for competitive inhibition is shown in
Table 2, Eq. (8). Predation, primarily by protozoa,
affects a microorganism’s ability to survive and may Figure 1 Breakthrough curve of biomass in response to a pulse
also be a crucial process controlling aqueous-phase of substrate in an intermediate flow cell. Flow cell was packed
biomass concentrations in groundwater (Harvey et al. with sand equilibrated with P. cepacia sp. 866A. AODC
1995). Cometabolism is the transformation of a Acridine orange direct counts. (After Murphy et al. 1997b)
compound by a microorganism that is incapable of
using the compound as a source of energy or growth
[Table 2, Eq. (9)]. Generally, cometabolism occurs in The aqueous-phase partitioning of bacteria in
the presence of a growth substrate or other transform- response to cell division was investigated in sand-
able compound, but it also may include transformations column experiments where cell division was blocked in
by resting cells if no growth occurs (Chang et al. 1993; one column by nalidixic acid, an antibiotic that
Criddle 1993; Smith and McCarty 1997). In one of the prevents DNA replication. Results are shown in
most common examples of cometabolism, aerobic Figure 2. When cell division was blocked, no increase
bacteria employ oxygenases, such as methane mono- occurred in the aqueous-phase bacteria (Pseudomonas
oxygenase in methanotrophic bacteria, to oxidize chlo- cepacia sp.), whereas a characteristic increase was
rinated solvents (Little et al. 1988; Mohn and Tiedje observed in the control column that did not contain
1992; Ely et al. 1997; Smith and McCarty 1997; Smith et nalidixic acid (Murphy et al. 1997a). Collectively, this
al. 1997). experimental information suggests that a strong
coupling exists between metabolic processes and
aqueous partitioning or transport of the microbial
community.
Metabolic Effects on Microbial Transport As discussed above, many investigators note that
and Contaminant Degradation starvation or nutrient availability can stimulate a
change in the partitioning of a microbial community
Modeling studies often simplify the explicit presence of
bacteria in both aqueous and attached phases, instead
treating the biomass as a fixed, often uniform phase. In
reality, bacteria are distributed both in the aqueous and
on the solid phases, and this distribution is dynamic in
the presence of a contaminant plume. In an experiment
conducted in an intermediate-scale flow cell
(100!20!10 cm dimensions), a substrate pulse
resulted in an increase in aqueous-phase bacteria, as
shown in Figure 1 (Murphy et al. 1997b), similar to
observations in field bioremediation efforts (USDOE
1993). Subsequent column experiments suggest that
this response may be cell-division-mediated transport, a
mechanism long recognized in the microbiology litera-
ture (Kjelleberg et al. 1982; Jenneman et al. 1985, 1986;
Reynolds et al. 1989; Sharma et al. 1993). Cell-division-
mediated transport has also been referred to as
mother–daughter or shedding cells and occurs when the
“mother” cell, attached perpendicular to the mineral Figure 2 Breakthrough of biomass in columns packed with sand
equilibrated with P. cepacia sp. 866A in response to a substrate
surface, grows and divides. The “daughter” cell is pulse. In one column, cell division was inhibited by maintaining
released into the aqueous phase (Marshall 1996) and a constant level of nalidixic acid. AODC Acridine orange direct
the mother cell remains attached. counts

Hydrogeology Journal (2000) 8 : 142–158 Q Springer-Verlag


151

between the solid and aqueous phases. A contaminant attachment/detachment rates were formulated as
plume creates a dynamic nutrient environment, but it is shown in Eqs. (5) and (6) in Table 1. Dynamic parti-
not clear whether the corresponding response in parti- tioning rates were formulated by allowing the forward
tioning of the microbial community has any effect at all attachment rate to decrease with increasing metabolic
on the actual contaminant degradation. Therefore, activity, shown here for the case of aqueous microor-
Ginn et al. (1998) investigated the relative importance ganisms:
of dynamic partitioning of the bacterial phase on
contaminant degradation by modeling the response of a iCmm
c =7(CmmV)p=7[D=Cmm]
consortium of anaerobic bacteria involved in the it
degradation of chlorinated hydrocarbons. This consor- Cc Cc n

tium consisted of two organisms, a propionate degrader cmMCmm 3


KscCs 4
PKf Cmm 1 P 1 3
KccCc 42 cK C r im

that produces formate and displays dynamic parti- (1)


tioning, and Desulfomonile tiedjei that uses formate and
reductively dechlorinates the chlorinated hydrocar- where Cmmpconcentration of aqueous “mobile
bons. D. tiedjei displays only kinetic partitioning and is, microbes” (mass per unit pore volume), Ccpconcentra-
in general, irreversibly attached. This example concerns tion of substrate (mass per unit pore volume),
the stimulation of a natural subsurface microbial Cimpconcentration of attached “immobile microbes”
community that would be, under initial conditions, (mass per unit pore volume), Dpdispersion tensor
dominantly associated with the mineral phase. (L 2T –1), Vppore-water velocity (LT –1), Kf,
However, when substrate is present, as in a contami- Krpforward and reverse attachment/detachment rates
nant plume, the propionate degrader displays dynamic (T –1), mMpMonod specific growth rate (T –1), and
partitioning, e.g., the forward attachment rate, Kf, KcpMonod half-saturation constant (T –1).
changes with the level of metabolic activity. Two exam- In this modeling exercise, a pulse (or plume) of chlo-
ples were compared to determine the effect of the rinated hydrocarbon was injected into the left-hand
dynamic attachment/detachment of the propionate side of the flow cell, shown in Figure 3. The sediments
degrader: (1) both bacteria controlled by kinetic attach- in the flow cell consisted of a darker, high-permeability
ment/detachment rates, i.e., no change in the attach- region, and a lighter, low-permeability region. The
ment/detachment rates with metabolic activity; and (2) contaminant showed an early breakthrough in the high-
the propionate degrader displays dynamic attachment/ permeability portion of the sediment, followed by a
detachment, whereas D. tiedjei continues to display secondary peak of the contaminant moving through the
only kinetic attachment/detachment rates. Kinetic lower permeability zone (Figure 3a) when both bacteria

Figure 3 Movement and


degradation of a hypothetical
chlorinated hydrocarbon
plume represented by light
area moving from left to right.
Reductive dehalogenation
occurs with a consortium of
bacteria, a propionate
degrader and Desulfomonile
tiedjei. a Bacteria display
kinetic attachment/detach-
ment, or b propionate-
degrader displays dynamic
attachment/detachment while
D. tiedjei displays kinetic
attachment/detachment

Hydrogeology Journal (2000) 8 : 142–158 Q Springer-Verlag


152

were only displaying kinetic attachment/detachment. aqueous microbes, Cmm, and attached microbes, Cim,
However, when the propionate-degrader undergoes respectively:
dynamic partitioning (Figure 3b), only contaminant
iCmm
traveling through the high-permeability zone reaches c =7(CmmV)p=7[D=Cmm]PKf CmmcKr Cim (2a)
the end of the flow cell; contaminant moving through it
the low-permeability region is completely degraded, as iCim
shown in the 40-h simulation. The enhanced degrada- p Kf CmmPKrCim (2b)
it
tion under dynamic conditions is due to the aqueous
partitioning of the propionate-degrader that results in where Cim is in units of biomass per aqueous volume
an increasing population moving with the plume, and (pCim[biomass/solid mass]rb /u), and D, V, and the K’s
hence increasing concentrations of formate, as the are as introduced above. This model distributes
contaminant plume moves along the flow path. In this biomass over space x and time t, so that Cmm is Cmm
example, the rate of formate production by the (x, t). With this conventional fate-and-transport mass
propionate-degrader was limiting the metabolic activity balance, it is impossible to incorporate any dependence
of D. tiedjei that promotes the dechlorination reaction. of partitioning kinetics upon residence time, because
This simulation illustrates the importance of under- residence time is not in the model. In Ginn (1999), a
standing the partitioning of bacteria under dynamic reformulation of the conventional fate-and-transport
growth conditions and of being able to track the tran- mass balance is developed that allows distributions of
sient movement of bacteria under changing chemical solutes such as biomass over space x and time t, and
conditions. generalized exposure-time (here, residence time) v on
surfaces, so that Cmm is the function Cmm(x, t, v). The
result is a mass-balance equation system just as the
Exposure Time Model for Tracking a Dynamic above, but with the addition of a convection term
Bacterial Population dictating the evolution of the biomass over space, time,
and the residence time coordinate v. Thus:
One instance of dynamic partitioning occurs when the
iCmm i(CmmV mm
v )
propensity for a microorganism to become irreversibly c =7(CmmV) c
attached to a solid phase depends on the residence time it iv
of the microorganism near the mineral surface. Resi- p =7[D=Cmm]PKf CmmcKr(v)Cim (3a)
dence time is defined here as the amount of time a iCim i(CimV im
v )
microorganism is reversibly associated with a surface c p Kf CmmPKr(v)Cim (3b)
it iv
through a specific interaction, such as electrostatic, van
der Waals, or hydrophobic interactions. Irreversible where now V mm v is the rate of displacement of aqueous
attachment is usually associated with active adhesion biomass in the residence-time dimension, just as
processes on the part of the microbe (Rijnaarts et al. VpV mm x is the rate of displacement in the x dimension;
1993; Fletcher 1996). For instance, a microbe may and V im
v is the rate of displacement of attached biomass
exhibit slow (relative to transport) cell-surface changes, in the residence-time dimension. Also, the rate of
such as exopolysaccharide production (Williams and detachment, Kr, is now expressed as a function of resi-
Fletcher 1996; Jucker et al. 1997) associated with dence time, v, that is, KrpKr (v). If indicated, one may
biofilm formation that effectively increases the proba- also specify a dependence of attachment rate, Kf, on
bility of irreversible attachment over a population of residence time, v.
microbes. Conventional descriptions of partitioning A subtle but important distinction exists between
kinetics at the bulk-phase scale are incapable of the exposure-time formulation (Ginn 1999) and the
capturing this behavior, because such models cannot formulation presented here for residence time on
track the distribution of biomass over the contiguous surfaces. In the original formulation, the exposure time
residence time. This limitation is noted in Johnson et al. increases for a component whether it is in a mobile or
(1995), who provide a heuristic accounting of the an immobile phase. Here, the phase association deter-
effects of residence time on reversibility by zeroing the mines the residence time, with residence time
detachment rate for microbes whose residence time increasing only when the bacteria are on a surface
exceeds a particular threshold. A new theoretical (immobile phase). Usually, the only thing known about
approach allows the tracking of residence-time effects the attachment process is from observations at the
on arbitrary reaction terms (Ginn 1999). This numerical bulk-continuum scale, such as the effective rates of
approach supports both variable methods of accounting kinetic first-order attachment and detachment.
of residence time (e.g., cumulative vs. contiguous) and Different attachment-detachment mechanisms may
arbitrary specification of the effect of residence time on operate and give rise to the same “bulk-scale” kinetic
the overall partitioning kinetics. first-order rate coefficients, yet these different attach-
The conventional model for dilute suspended ment-detachment mechanisms involve very different
bacteria undergoing convective-dispersive transport residence times on surfaces. For a simple illustration,
and first-order kinetic reversible partitioning is, for consider a detachment kinetic described by first-order

Hydrogeology Journal (2000) 8 : 142–158 Q Springer-Verlag


153

theory with a coefficient Krp0.1 per time unit. This microorganism on time scales that may be kinetically
means that, per time unit, 10% of the biomass is controlled. For example, a newly attached microbe may
detached and 90% of the biomass is attached at the end start to produce proteins and/or exopolysaccharides in
of the time unit. the process of biofilm formation, and if this microbe
If the detached biomass all underwent exactly one detaches, these structures may not instantaneously
detachment event during that time unit, then one may disappear. This notion is congruent with the under-
define some bulk-scale residence time of the attached standing of the time scale of metabolic lag, which has
biomass. However, the newly detached bacteria do not been observed on the same order as that of transport,
necessarily all undergo exactly one detachment event; requiring its treatment as a kinetically controlled
in fact, any number of bacteria may have undergone process (e.g., Wood et al. 1995; Murphy et al. 1997b),
multiple partitioning events within the time unit, as and it has recently been treated with an exposure-time
long as the local attached and detached cell numbers approach (Ginn 1999).
obey the postulated first-order kinetics. This non- Thus it may be useful to generalize the foregoing in
uniqueness in basic mechanisms means that the order to accommodate memory or adhesion processes
accounting of residence time is also non-unique and for continuous residence time, v. In a general sense, the
impossible without further assumptions regarding the role of memory in the attachment/detachment kinetic
underlying mechanism of attachment–detachment. The rates depends on the ratio of the time scale of physio-
most powerful assumption is constructed by simply logic changes associated with active adhesion processes
requiring the attachment-detachment process to to the time scale of detachment intervals, e.g., the mean
involve exactly one partitioning event during the time time between attachments. For illustration, consider
unit specified. This assumption is basically the same the two cases where kinetics of detachment depend on
mechanistic assumption that is used to calculate the (1) cumulative and (2) contiguous residence time, as
rates of reactions with statistical thermodynamics using shown in Figure 4. In the cumulative memory model,
transition-state theory (e.g., Kreevoy and Truhlar 1986) the physiological state of the microorganism depends
and is referred to as the “no-recrossing rule.” Thus, only on the total cumulative time that the microbe has
during one unit time, exactly Kf of the local aqueous spent in the attached state, regardless of how that time
cells attach and exactly Kr of the local attached cells is distributed over attachment events or how much time
detach, and no other partitioning events, such as an the microbe has spent in the aqueous phase
attached cell detaching and then reattaching, occur in (Figure 4b). In the contiguous memory model, the
that same unit time. This assumption sets the character- physiological state of the microorganism depends on
istic time scale of the partitioning event, and, in doing some finite memory of historical attachment, and so
so, links the units of the first-order rate coefficients (Kf, time spent in the aqueous phase after any given attach-
Kr) with the residence time on the surface. ment event may result in a kinetically controlled return
A rational model that is a generalization of the to a pre-attached state (i.e., slow loss of memory of
Johnson et al. (1995) formulation may be written by attachment; Figure 4c). In the cumulative case, physiol-
supposing that a limitation on detachment arises as a ogical changes in the cell surface may stop if a cell
result of active adhesion (e.g., via exopolysaccharide becomes detached, but they never reverse, or they
production, biofilm formation). In this case, one may reverse so slowly that they may be considered irrever-
specify a function Kr(v), where Kr (e.g., detachment sible. In the contiguous state, time spent in the aqueous
rate) decreases with increasing residence time, v. The phase between attachment events can result in reversal
form of this function that is equivalent to that of of the physiological changes in the cell surface.
Johnson et al. (1995) is where Kr(v) is a positive
constant to some critical residence time, vpv*, beyond
which the rate of detachment [Kr(v)] is zero. That is: Cumulative Case
In the case where changes in the cell surface occur so
Kr 0^v^v* slowly that they may be considered irreversible, then
Kr(v) p 50 0^v*^v
(4)
cumulative residence time is what controls detachment
frequency. In this case, residence time needs to be
In the approach of Johnson et al. (1995), an attached tracked during the microbes’ time spent in the solid
cell accumulates residence time at a rate of unity per phase, where the rate of change in residence time, v, is
unit time (in discrete increments), and, upon detaching, unity with time, t, i.e., the increase in residence time, v,
undergoes an instantaneous decrease of residence time per unit time, t, attached is 1 : 1; thus V im
v p1. Further-
to zero. This approximation reflects the notion that more, in this case, time spent in the aqueous phase does
cells maintain zero memory of attachment, i.e., that any nothing to the accounting of residence time, so V mm v p
structural surface changes due to adhesion processes 0. Thus the model becomes:
are reversed upon detachment at a rate that is faster
than one discrete time interval. However, as noted in iCmm
c=7(CmmV)p=7(D7=Cmm)PKfCmmcKr(v)Cim
the studies cited above, active adhesion processes are it
associated with physiologic changes that occur in the (5a)

Hydrogeology Journal (2000) 8 : 142–158 Q Springer-Verlag


154

iCim iCim
c p cKf CmmPKr(v)Cim (5b)
it iv
This case is schematically illustrated in Figure 4,
where the trajectory of a single microbe that undergoes
two attachment events during 1-D transport under a
constant velocity is illustrated first in the characteristic
plane of physical transport (x, t) (Figure 4a), and then
in the characteristic space of the model above, (x, t, v)
(Figure 4b). Physical attachment is shown in Figure 4a
at the times a (with detachment at b) and c (with irrev-
ersible residence time reached at d). The same trajec-
tory, augmented with an explicit accounting of cumula-
tive residence time, is shown in Figure 4b. There,
increase in the v-dimension takes place at dt:dvp1 : 1,
exactly when the microbe is attached; no increase
occurs in v when the microbe is in the aqueous phase.
With cumulative residence time, v, thus accounted, it is
possible to keep track of the time and space coordi-
nates at which the critical cumulative residence time,
v*, is reached, and thus to keep track of the proportion
of microbes that become irreversibly attached.

Contiguous Case
In the case where cells retain some structural memory
of the changes induced by attachment but lose this
memory kinetically while in the unattached phase, it is
necessary to represent the reduction in contiguous resi-
dence time for aqueous-phase microbes (Figure 4c). In
addition to the aging velocities V im introduced in the
previous section, some non-equilibrium rate of expo-
sure-time reduction is required in the aqueous phase
V mm
v 1 0. A simple expression for exponential (acceler-
ated) reduction is obtained with V mmv pPv, in which
case the model takes the form
iCmm i(vCmm)
c =7(CmmV) P
it iv
p =7(D7=Cmm)PKf CmmcKr(v)Cim (6a)
iCim iCim
c p cKf CmmPKr(v)Cim (6b)
it iv
Determination of the appropriate form for the
velocity of reduction in residence time (when it
matters) requires controlled experiments. It may also
be useful to treat this velocity as a random variable,
reflecting variability of rates of bacterial adhesion
Figure 4 a Trajectory of a single microbe undergoing transport in among different individual cells. Given statistical prop-
a constant 1-D velocity field, with two attachment events occur- erties of the distribution of this velocity, one might use
ring at times a and c, and indicated by horizontal portions of the stochastic-analytic techniques (e.g., Gardiner 1990) to
characteristic path in x, t. b Same trajectory in physical-time coor- seek the average behavior of the system.
dinates, now augmented with component of displacement in the
v-dimension corresponding to cumulative residence time. In this
hypothetical simplification, the microbe becomes irreversibly
attached when cumulative residence time exceeds v*. c Same Conclusions
trajectory in physical-time coordinates with additional residence
time. In this contiguous case, time spent in the aqueous phase
between attachment events (b to c) results in reversal of physiol- Advances in modeling microbial processes in the
ogical changes to cell surface that may have occurred during a subsurface require a multidisciplinary approach.
prior attachment period (a to b) Understanding the biological processes and the

Hydrogeology Journal (2000) 8 : 142–158 Q Springer-Verlag


155

coupling of these processes with the physical flow and Champ DR, Schroeter J (1988) Bacterial transport in fractured
transport is critical. Field and laboratory experiments rock: a field-scale tracer test at the Chalk River Nuclear Labo-
ratories. Water Sci Technol 20 : 81–87
demonstrate that the metabolic activity of subsurface Chang M-K, Voice TC, Criddle CS (1993) Kinetics of competitive
microorganisms can create a dynamic distribution of a inhibition and cometabolism in the biodegradation of
microbial population between aqueous and solid benzene, toluene, and p-xylene by two Pseudomonas isolates.
phases in groundwater systems. Enhanced aqueous Biotechnol Bioeng 41 : 1057–1065
Characklis WG, Marshall KC (1990) Biofilms. John Wiley, New
partitioning of the biomass can, in some cases, increase York
the degradation of contaminants as a plume moves Chen Y, Abriola LM, Alvarez PJJ, Anid PJ, Vogel TM (1992)
along a groundwater gradient. In many of the examples Modeling transport and biodegradation of benzene and
presented here, the complexity of the biological pro- toluene in sandy aquifer material: comparison with experi-
cesses requires advances in numerical and theoretical mental measurements. Water Resour Res 28 : 1833–1847
Chilakapati A (1995) A simulator for reactive flow and transport
modeling approaches. One such advancement is the of groundwater contaminants. Pacific Northwest National
development of an exposure-time model that allows Laboratory, Richland, Washington
incorporation of cell-level processes into reactive trans- Chilakapati A, Ginn TR, Szecsody J (1998) An analysis of
port models by tracking biomass in space, time, and the complex reaction networks in groundwater modeling. Water
additional dimension of exposure time. Using this Resour Res 34 : 1767–1780
Corapcioglu MY, Haridas A (1984) Transport and fate of micro-
approach, important, distributed variables, such as resi- organisms in porous media: a theoretical investigation. J
dence time on a surface or the amount of time that a Hydrol 72 : 149–169
microbial population has been exposed to nutrients, Corapcioglu MY, Kim S (1996) Modeling facilitated contaminant
can be incorporated to evaluate both the transport and transport by mobile bacteria. Water Resour Res
31 : 2639–2647
metabolic activity of a microbial population. This capa- Criddle CS (1993) The kinetics of cometabolism. Biotechnol
bility permits simulation of dynamic processes occur- Bioeng 41 : 1048–1056
ring in an evolving contaminant plume and is expected Dawson MP, Humphrey A, Marshall KC (1981) Adhesion: a
ultimately to lead to a better understanding of the tactic in the survival strategy of a marine vibrio during starva-
subsurface behavior of microbial communities. tion. Curr Microbiol 6 : 195–199
de Marsily G (1986) Quantitative hydrogeology. Academic Press,
New York
Acknowledgments The authors acknowledge the support of the Dodds J (1982) La chromatographie hydrodynamique. Analusis
US Department of Energy, Office of Biological and Environ- 10 : 109–119
mental Research, Natural and Accelerated Bioremediation Eisenmann H, Harms H, Meckenstock R, Meyer EI, Zehnder
program. Also thanked are the guest editor, Barbara Bekins, and AJB (1998) Grazing of a Tetrahymena sp. on adhered bacteria
two anonymous reviewers, who greatly improved the clarity of in percolated columns monitored by in situ hybridization with
this manuscript. fluorescent oligonucleotide probes. Appl Environ Microbiol
64 : 1264–1269
Ely RL, Williamson KJ, Hyman MR, Arp DJ (1997) Come-
tabolism of chlorinated solvents by nitrifying bacteria: kine-
References tics, substrate interactions, toxicity effects, and bacterial
response. Biotechnol Bioeng 54 : 520–534
Albrechtsen H-J (1994) Distribution of bacteria, estimated by a Enfield CG, Bengtsson G (1988) Macromolecular transport of
viable count method, and heterotrophic activity in different hydrophobic contaminants in aqueous environments. Ground
size fractions of aquifer sediment. Geomicrobiol J Water 26 : 64–70
12 : 253–264 Fletcher M (1991) Bacterial colonization of solid surfaces in
Bailey JE, Ollis DF (1986) Biochemical engineering fundamen- subsurface environments. In: Fliermans CB, Hazen TC (eds)
tals, 2nd edn. McGraw-Hill, New York Proc 1st Int Symp on Microbiology of the Deep Subsurface,
Bales RC, Hinkle SR, Kroeger TW, Stocking K (1991) Bacterio- Orlando, Florida, 1990
phage adsorption during transport through porous media: Fletcher M (1996) Bacterial adhesion: molecular and ecological
chemical perturbations and reversibility. Environ Sci Technol diversity. In: Mitchell R (ed) Ecological and applied microbi-
25 : 2088–2095 ology. Wiley-Liss, New York, 361 pp
Bales RC, Li S, Maguire KM, Yahya MT, Gerba CP, Harvey RW Fletcher M, Loeb GI (1979) Influence of substratum characteris-
(1995) Virus and bacteria transport in a sandy aquifer, Cape tics on the attachment of a marine pseudomonad to solid
Cod, Massachusetts. Ground Water 33 : 653–661 surfaces. Appl Environ Microbiol 37 : 67–72
Barton JW, Ford RM (1995) Determination of effective transport Ford RM, Cummings PT (1998) Mathematical models of bacterial
coefficients for bacterial migration in sand columns. Appl chemotaxis. In: Koch AL, Robinson JA, Milliken GA (eds)
Environ Microbiol 61 : 3329–3335 Mathematical modeling in microbial ecology. Microbiology
Baveye P, Valocchi A (1991) Reply. Water Resour Res Series. Chapman & Hall, New York, 273 pp
27 : 1379–1380 Gardiner CW (1990) Handbook of stochastic methods for
Baveye P, Vandevivere P, Lozada DD (1992) Comment on physics, chemistry, and the natural sciences. Springer, Berlin
“Biofilm growth and the related changes in the physical prop- Heidelberg New York
erties of a porous medium, 1; experimental investigation,” by Gilbert P, Brown MRW (1995) Mechanisms of the protection of
SW Taylor and PR Jaffe. Water Resour Res 28 : 1481–1482 bacterial biofilms from antimicrobial agents. In: Lappin-Scott
Beeftink HH, Heijden RTJMvd, Heijnen JJ (1990) Maintenance HM, Costerton JW (eds) Microbial biofilms. Cambridge
requirements: energy supply from simultaneous endogenous University Press, Cambridge, pp 118–130
respiration and substrate consumption. FEMS Microbiol Ecol Ginn TR (1999) On the distribution of multi-component mixtures
73 : 203–210 over generalized exposure-time in subsurface flow and reac-
Button DK (1993) Nutrient-limited microbial growth kinetics: tive transport: foundations, and formulations for groundwater
overview and recent advances. Antonie van Leeuwenhoek; J age, chemical heterogeneity, and biodegradation. Water
Microbiol Serol 63 : 225–235 Resour Res 35 : 1395–1408

Hydrogeology Journal (2000) 8 : 142–158 Q Springer-Verlag


156

Ginn TR, Simmons CS, Wood BD (1995) Stochastic-convective Jenneman GE, McInerney MJ, Crocker MF, Knapp RM (1986)
transport with nonlinear reaction: biodegradation with micro- Effect of sterilization by dry heat or autoclaving on bacterial
bial growth. Water Resour Res 31 : 2689–2700 penetration through Berea sandstone. Appl Environ Micro-
Ginn TR, Scheibe TD, Murphy EM, DeFlaun MF, Onstott TC biol 51 : 39–43
(1998) Effects of chemical heterogeneity on subsurface fate Jewett DG, Hilbert TA, Logan BE, Arnold RG, Bales RC (1995)
and transport involving biotic reaction systems: two examples. Bacterial transport in laboratory columns and filters: influence
In: American Geophysical Union Fall Meeting, San Francisco, of ionic strength and pH on collision efficiency. Water Res
December 1998. Eos Trans 79(45):F294 29 : 1673–1680
Godsy EM, Goerlitz DF, Grbic-Galic D (1992) Methanogenic Johnson WP, Blue KA, Logan BE, Arnold RG (1995) Modeling
biodegradation of creosote contaminants in natural and simu- bacterial detachment during transport through porous media
lated ground-water ecosystems. Ground Water 30 : 232–242 as a residence-time-dependent process. Water Resour Res
Harms H, Zehnder AJB (1994) Influence of substrate diffusion 31 : 2649–2658
on degradation of dibenzofuran and 3-chlorodibenzofuram by Jucker BA, Harms H, Hug SJ, Zehnder AJB (1997) Adsorption
attached and suspended bacteria. Appl Environ Microbiol of bacterial surface polysaccharides on mineral oxides is
60 : 2736–2745 mediated by hydrogen bonds. Series B: Biointerfaces. Colloids
Harvey RW (1991) Parameters involved in modeling movement Surfaces 9 : 331–343
of bacteria in groundwater. In: Hurst CJ (ed) Modeling the Kaprelyants AS, Gottschal JC, Kell DB (1993) Dormancy in non-
environmental fate of microorganisms. American Society for sporulating bacteria. FEMS Microbiol Rev 104 : 271–286
Microbiology, Washington, DC, pp 89–114 Kindred JS, Celia MA (1989) Contaminant transport and bio-
Harvey RW, Barber LB (1992) Associations of free-living degradation, 2. Conceptual model and test simulations. Water
bacteria and dissolved organic compounds in a plume of Resour Res 1989 : 1149–1159
contaminated groundwater. J Contam Hydrol 9 : 91–103 Kinoshita T, Bales RC, Yahya MT, Gerba CP (1993) Bacteria
Harvey RW, Garabedian SP (1991) Use of colloid filtration transport in a porous medium: retention of bacillus and pseu-
theory in modeling movement of bacteria through a contami- domonas on silica surfaces. Water Res 27 : 1295–1301
nated sandy aquifer. Environ Sci Technol 25 : 178–185 Kinzelbach W, Schafer W, Herzer J (1991) Numerical modeling
Harvey RW, Widdowson MA (1992) Microbial distributions, of natural and enhanced denitrification processes in aquifers.
activities, and movement in the terrestrial subsurface: experi- Water Resour Res 27 : 1123–1135
mental and theoretical studies. In: Wagenet RJ, Baveye P, Kjelleberg S, Hermansson M (1984) Starvation-induced effects on
Stewart BA (eds) Advances in soil science. Lewis Publishers, bacterial surface characteristics. Appl Environ Microbiol
Boca Raton, pp 185–225 48 : 497–503
Harvey RW, Smith RL, George L (1984) Effect of organic Kjelleberg S, Humphrey BA, Marshall KC (1982) The effect of
contamination upon microbial distributions and heterotrophic interfaces on small starved marine bacteria. Appl Environ
uptake in a Cape Cod, Mass., aquifer. Appl Environ Microbiol Microbiol 43 : 1166–1172
48 : 1197–1202 Kjelleberg S, Hermansson M, Marden P (1987) The transient
Harvey RW, George LH, Smith RL, LeBlanc DR (1989) Trans- phase between growth and nongrowth of heterotrophic
port of microspheres and indigenous bacteria through a sandy bacteria, with emphasis on the marine environment. Annu
aquifer: results of natural- and forced-gradient tracer experi- Rev Microbiol 41 : 25–49
ments. Environ Sci Technol 23 : 51–56 Koch AL (1998) The Monod model and its alternatives. In: Koch
Harvey RW, Kinner NE, MacDonald D, Metge DW, Bunn A AL, Robinson JA, Milliken GA (eds) Mathematical modeling
(1993) Role of physical heterogeneity in the interpretation of in microbial ecology. Microbiology Series. Chapman & Hall,
small-scale laboratory and field observations of bacteria, New York, pp 62–93
microbial-sized microsphere, and bromide transport through Kölbel-Boelke J, Anders E, Nehrkorn A (1988) Microbial
aquifer sediments. Water Resour Res 29 : 2713–2721 communities in the saturated groundwater environment II:
Harvey RW, Kinner NE, Bunn A, MacDonald D, Metge D diversity of bacterial communities in a Pleistocene sand
(1995) Transport behavior of groundwater protozoa and aquifer and their in vitro activities. Microb Ecol 16 : 31–48
protozoan-sized microspheres in sandy aquifer sediments. Kreevoy MM, Truhlar DG (1986) Transition state theory. In:
Appl Environ Microbiol 61 : 209–217 Bernasconi CF (ed) Investigations of rates and mechanisms of
Harvey RW, Metge DW, Kinner N, Mayberry N (1997) Physiol- reactions, Part 1. General considerations and reactions at
ogical considerations in applying laboratory-determined conventional rates, 4th edn. Wiley, New York, pp 13–97
buoyant densities to predictions of bacterial and protozoan Lang MM, Roberts PV, Semprini L (1997) Model simulations in
transport in groundwater: results of in-situ and laboratory support of field scale design and operation of bioremediation
tests. Environ Sci Technol 31 : 289–295 based on cometabolic degradation. Ground Water
Herbert D (1958) Some principles of continuous culture. In: 35 : 565–573
Tunevall G (ed) Recent progress in microbiology. Blackwell Lindqvist R, Bengtsson G (1991) Dispersal dynamics of ground-
Scientific, Oxford, pp 381–396 water bacteria. Microb Ecol 21 : 49–72
Herzig JP, Leclerc DM, LeGoff P (1970) Flow of suspension Lindqvist R, Cho JS, Enfield CG (1994) A kinetic model for cell
through porous media; application to deep filtration. Ind Eng density dependent bacterial transport in porous media. Water
Chem 62 : 129–157 Resour Res 30 : 3291–3299
Hess TF, Schmidt SK, Colores GM (1996) Maintenance energy Little CD, Palumbo AV, Herbes SE, Lidstrom ME, Tyndall RL,
model for microbial degradation on toxic chemicals in soil. Gilmer PJ (1988) Trichloroethylene biodegradation by a
Soil Biol Biochem 28 : 907–915 methane-oxidizing bacterium. Appl Environ Microbiol
Hirsch P, Rades-Rohkohl E (1988) Die Vielfalt mikrobieller 54 : 951–956
Mosrphotypen im Grundwasservereich des Segeberger Logan BE, Jewett DG, Arnold RG, Bouwer EJ, O’Melia CR
Forstes. Z Dtsch Geol Ges 139 : 343–353 (1995) Clarification of clean-bed filtration models. J Environ
Hornberger GM, Mills AL, Herman JS (1992) Bacterial transport Eng December:869–873.
in porous media: evaluation of a model using laboratory MacQuarrie KTB, Sudicky EA, Frind EO (1990) Simulation of
observations. Water Resour Res 28 : 915–938 biodegradable organic contaminants in groundwater. 1.
Jaffe PR, Taylor SW (1992) Reply. Water Resour Res Numerical formulation in principal directions. Water Resour
28 : 1483–1484 Res 26 : 207–222
Jenneman GE, McInerney MJ, Knapp RM (1985) Microbial Marshall KC (1996) Adhesion as a strategy for access to
penetration through nutrient-saturated Berea sandstone. Appl nutrients. In: Fletcher M (ed) Bacterial adhesion, molecular
Environ Microbiol 50 : 383–391 and ecological diversity. John Wiley, New York, pp 59–87

Hydrogeology Journal (2000) 8 : 142–158 Q Springer-Verlag


157

Matin A (1990) Molecular analysis of the starvation stress in E. Rajagopalan R, Tien C (1976) Trajectory analysis of deep-bed
coli. FEMS Microbiol Ecol 74 : 185–196 filtration with the sphere-in-a-cell porous media model. Am
Mayotte TJ, Dybas MJ, Criddle CS (1996) Bench-scale evaluation Inst Chem Eng 22 : 523–533
of bioaugmentation to remediate carbon tetrachloride Reynolds PJ, Sharma P, Jenneman GE, McInerney MJ (1989)
contaminated aquifer materials. Ground Water 34 : 358–367 Mechanisms of microbial movement in subsurface materials.
McCaulou DR, Bales RC, McCarthy JF (1994) Use of short-pulse Appl Environ Microbiol 55 : 2280–2286
experiments to study bacteria transport through porous Rijnaarts HHM, Norde W, Bouwer EJ, Lyklema J, Zehnder AJB
media. J Contam Hydrol 15 : 1–14 (1993) Bacterial adhesion under static and dynamic condi-
McCaulou DR, Bales RC, Arnold RG (1995) Effect of tempera- tions. Appl Environ Microbiol 59 : 3255–3265
ture-controlled motility on transport of bacteria and micro- Rittman BE (1993) The significance of biofilms in porous media.
spheres through saturated sediment. Water Resour Res Water Resour Res 29 : 2195–2202
31 : 271–280 Saiers JE, Hornberger GM (1996) The role of colloidal kaolinite
McDowell-Boyer LM (1992) Chemical mobilization of micron- in the transport of cesium through laboratory sand columns.
sized particles in saturated porous media under steady flow Water Resour Res 32 : 33–41
conditions. Environ Sci Technol 26 : 586–593 Sakthivadivel R (1966) Theory and mechanism of filtration of
McDowell-Boyer LM, Hunt JR, Sitar N (1986) Particle transport non-colloidal fines through a porous medium. Report HEL
through porous media. Water Resour Res 22 : 1901–1921 15-5. Hydraulic Engineering Laboratory, University of Cali-
McEldowney S, Fletcher M (1988) Effect of pH, temperature, and fornia, Berkeley, 110 pp
growth conditions on the adhesion of a gliding bacterium and Sakthivadivel R (1969) Clogging of a granular porous medium by
three nongliding bacteria to polystyrene. Microb Ecol sediment. Report HEL 15-7. Hydraulic Engineering Labora-
16 : 183–195 tory, University of California, Berkeley, 106 pp
Mercer JR, Ford RM, Stitz JL, Bradbeer C (1993) Growth rate Scholl MA, Mills AL, Herman JS, Hornberger GM (1990) The
effects on fundamental transport properties of bacterial popu- influence of mineralogy and solution chemistry on the attach-
lations. Biotechnol Bioeng 42 : 1277–1286 ment of bacteria to representative aquifer materials. J Contam
Mills WB, Liu S, Fong FK (1991) Literature review and model Hydrol 6 : 321–336
(comet) for colloid/metals transport in porous media. Ground Semprini L, McCarty PL (1992) Comparison between model
Water 29 : 199–208 simulations and field results for in-situ biorestoration of chlo-
Mills AL, Herman JS, Hornberger GM, de Jesus TH (1994) rinated aliphatics: Part 2. Cometabolic transformations.
Effect of ionic strength and iron coatings on mineral grains on Ground Water 30 : 37–44
sorption of bacterial cells to quartz sand. Appl Environ Micro- Semprini L, Hopkins GD, Roberts PV, Grbic-Galic D, McCarty
biol 60 : 3300–3306 PL (1991) A field evaluation of in-situ biodegradation of chlo-
Mohn WW, Tiedje JM (1992) Microbial reductive dehalogena- rinated ethenes: Part 3. Studies of competitive inhibition.
tion. Microbiol Rev 56 : 482–507 Ground Water 29 : 239–250
Molz FJ, Widdowson MA, Benefield LD (1986) Simulation of Sharma MM, Chang YI, Yen TF (1985) Reversible and irrever-
microbial growth dynamics coupled to nutrient and oxygen sible surface charge modifications of bacteria for facilitating
transport in porous media. Water Resour Res 22 : 1207–1216 transport through porous media. Colloids Surfaces
Monod J (1949) The growth of bacterial cultures. Annu Rev 16 : 193–206
Microbiol 3 : 371–393 Sharma PK, McInerney MJ, Knapp RM (1993) In situ growth and
Murphy EM, Ginn TR, Brockman FJ, Boone DR (1997a) Growth activity and modes of penetration of Escherichia coli in uncon-
effects on the partitioning and transport of bacteria. In: Amer- solidated porous materials. Appl Environ Microbiol
ican Geophysical Union Fall Meeting, San Francisco, 59 : 3686–3694
December 1997. Eos Trans 78(46) : F231 Shaw DJ (1970) Introduction to colloid and surface chemistry,
Murphy EM, Ginn TR, Chilakapati A, Resch CT, Phillips JL, 2nd edn. Butterworth-Heinemann, Woburn, Massachusetts,
Wietsma TW, Spadoni CM (1997b) The influence of physical pp 168–177
heterogeneity on microbial degradation and distribution in Shonnard DR, Taylor RT, Hanna ML, Boro CO, Duba AG
porous media. Water Resour Res 33 : 1087–1103 (1994) Injection-attachment of Methylosinus trichosporium
Novitsky JA, Morita RY (1976) Morphological characterization OB3b in a two-dimensional miniature sand-filled aquifer
of small cells resulting from nutrient starvation in a psychro- simulator. Water Resour Res 30 : 25–36
philic marine vibrio. Appl Environ Microbiol 32 : 619–622 Smigielski A, Wallace B, Marshall K (1989) Changes in
Novitsky JA, Morita RY (1977) Survival of a psychrophilic membrane functions during short-term starvation of Vibrio
marine vibrio under long-term nutrient starvation. Appl fluvialis strain NCTC 11328. Arch Microbiol 151 : 336–341
Environ Microbiol 33 : 635–641 Smith JL (1989) Sensitivity analysis of critical parameters in
Oliver J, Nilsson L, Kjelleberg S (1991) Formation of noncultur- microbial maintenance-energy models. Biol Fert Soils 8 : 7–12
able Vibrio vulnificus cells and its relationship to the starva-
Smith LH, McCarty PL (1997) Laboratory evaluation of a two-
tion state. Appl Environ Microbiol 57 : 2640–2644
stage treatment system for TCE cometabolism by a methane-
Petzold L (1983) A description of DASSL: a differential/algebraic
oxidizing mixed culture. Biotechnol Bioeng 55 : 650–659
system solver. In: Stepelman RS (ed) Scientific computing:
Smith JL, McNeal BL, Cheng HH, Campbell GS (1986) Calcula-
applications of mathematics and computing to the physical
tion of microbial maintenance rates and net nitrogen mineral-
sciences. North Holland, New York, pp 65–68
ization in soil at steady-state. Soil Sci Soc Am J 50 : 332–338
Pirt SJ (1975) Principles of microbe and cell cultivation. John
Wiley, New York Smith LH, Kitanidis PK, McCarty PL (1997) Numerical modeling
Powell EO (1967) The growth rate of microorganisms as a func- and uncertainties in rate coefficients for methane utilization
tion of the substrate concentration. In: Powell EO, Evans GT, and TCE cometabolism by a methane-oxidizing mixed culture.
Strange RE, Tempest DW (eds) Microbial physiology and Biotechnol Bioeng 53 : 320–331
continuous culture. HMSO, London, pp 34–56 Steefel CI, MacQuarrie KTB (1996) Approaches to modeling of
Pyle BH (1979) Technical publication no 2. Lincoln College reactive transport in porous media. In: Lichtner PC, Steefel
Department of Agriculture Microbiology, Canterbury, New CI, Oelkers EH (eds) Reactive transport in porous media.
Zealand Mineral Soc Am Rev Mineral 34 : 83–130
Pyle BH, Thorpe HR (1981) Evaluation of the potential for Sudicky EA, Schellenberg SL, MacQuarrie KTB (1990) Assess-
microbiological contamination of an aquifer using a bacterial ment of the behaviour of conservative and biodegradable
tracer. In: Proc Conf on Ground-Water Pollution, Sydney. solutes in heterogeneous porous media. In: Cushman JH (ed)
Australian Water Resources Council Conference Series Dynamics of fluids in hierarchical porous media. Academic
1 : 213–224 Press, San Diego, pp 429–462

Hydrogeology Journal (2000) 8 : 142–158 Q Springer-Verlag


158

Tan Y, Gannon JT, Baveye P, Alexander M (1994) Transport of Widdowson MA, Molz FJ, Benefield LD (1988) A numerical
bacteria in an aquifer sand: experiments and model simula- transport model for oxygen- and nitrate-based respiration
tions. Water Resour Res 30 : 3243–3252 linked to substrate and nutrient availability in porous media.
Taylor SW, Jaffe PR (1990) Substrate and biomass transport in a Water Resour Res 24 : 1553–1565
porous medium. Water Resour Res 26 : 2181–2194 Williams V, Fletcher M (1996) Adhesion and transport through
Taylor SW, Milly PCD, Jaffe PR (1990) Biofilm growth and porous media of Pseudomonas fluorescens is affected by lipo-
related changes in the physical properties of a porous medium polysaccharide composition. Appl Environ Microbiol
2. Permeability. Water Resour Res 26 : 2161–2170 62 : 100–104
Tien C, Turian RM, Pandse H (1979) Simulation of the dynamics Wood WW, Ehrlich GG (1978) Use of baker’s yeast to trace
of deep bed filters. Am Inst Chem Eng 25 : 385–395 microbial movement in ground water. Ground Water
USDOE (U.S. Department of Energy) (1993) Cleanup of VOCs 16 : 398–403
in non-arid soils – the Savannah River integrated demonstra- Wood BD, Whitaker S (1998) Diffusion and reaction in biofilms.
tion. US Department of Energy, Environmental Restoration Chem Eng Sci 53 : 397–425
and Waste Management Office of Technology Development, Wood BD, Whitaker S (1999) Cellular growth in biofilms.
Washington, DC Biotechnol Bioeng 64 : 656–670
Vandevivere P, Baveye P (1992) Saturated hydraulic conductivity Wood BD, Whitaker S (in press) Multispecies diffusion and reac-
reduction caused by aerobic bacteria in sand columns. J Soil tion in biofilms. Chem Eng Sci
Sci Soc Am 56 : 1–13 Wood BD, Dawson CN, Szecsody JE, Streile GP (1994) Modeling
van Loosdrecht MCM, Lyklema J, Norde W, Schraa G, Zehnder contaminant transport and biodegradation in a layered porous
AJB (1987) Electrophoretic mobility and hydrophobicity as a media system. Water Resour Res 30 : 1833–1845
measure to predict the initial steps of bacterial adhesion. Appl Wood BD, Ginn TR, Dawson CN (1995) Effects of microbial
Environ Microbiol 53 : 1898–1901 metabolic lag in contaminant transport and biodegradation
van Loosdrecht MCM, Lyklema J, Norde W, Zehnder AJB modeling. Water Resour Res 31 : 553–563
(1989) Bacterial adhesion: a physiochemical approach. Microb Wrangstadh M, Szewzyk U, Oestling J, Kjelleberg S (1990) Star-
Ecol 17 : 1–15 vation-specific formation of a peripheral exopolysaccharide by
van Loosdrecht MCM, Lyklema J, Norde W, Zehnder AJB a marine Pseudomonas sp., strain S9. Appl Environ Microbiol
(1990) Influence of interfaces on microbial activity. Microbiol 56 : 2065–2072
Rev 54 : 75–87 Yeh G, Tripathi V (1989) A critical evaluation of recent develop-
Wan J, Tokunaga TK, Tsang CF (1995) Bacterial sedimentation ments in hydrogeochemical transport models of reactive
through a porous medium. Water Resour Res 31 : 1627–1636 multichemical components. Water Resour Res 25 : 93–108
Widdowson MA (1991) Comment on “An evaulation of mathe- Zysset A, Stauffer F, Dracos T (1994) Modeling of reactive
matical models of the transport of biologically reacting solutes groundwater transport governed by biodegradation. Water
in saturated soils and aquifers.” Water Resour Res Resour Res 30 : 2423–2434
27 : 1375–1378

Hydrogeology Journal (2000) 8 : 142–158 Q Springer-Verlag