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J. Phycol.

34, 757–763 (1998)

MINIREVIEW

WASTEWATER TREATMENT WITH SUSPENDED AND NONSUSPENDED ALGAE1

James P. Hoffmann2
Department of Botany and Agricultural Biochemistry, University of Vermont, Burlington, Vermont 05405

Mass culture of algae in wastewater can signifi- Chemical- and physical-based technologies are avail-
cantly contribute to the management of freshwater able to remove nutrients and metals from wastewa-
ecosystems by providing a more environmentally ter; however, they consume significant amounts of
sound approach to reducing the eutrophication po- energy and chemicals and therefore are costly
tential of point sources of human wastes than is (Tchobanoglous and Burton 1991). Oswald (1988b)
achieved by current treatment practices. Incorpo- estimates that the relative cost doubles with each ad-
rating algal systems into conventional wastewater ditional stage of treatment. Furthermore, chemical-
treatment has the potential to improve the water based treatments often lead to the contamination of
quality of the effluent by reducing the nutrient and the sludge by-product of conventional treatment
metal loads into freshwater ecosystems. The use of plants. For example, a common tertiary treatment
algae to treat wastewater has been investigated for for phosphorus removal can cause increased levels
over 40 years, with one of the first descriptions of of aluminum in the sludge and create problems of
this application being reported by Oswald and Go- safe disposal.
taas (1957). For a historical survey of outdoor algal
mass culture efforts, including wastewater treatment, ROLE OF ALGAE IN SOLVING THE PROBLEM
see Goldman (1979a) and Soeder (1980). Most re- Algal treatment of wastewater, mediated through
search has focused on suspended microalgae grow- a combination of nutrient uptake, elevated pH, and
ing in shallow, artificial ponds containing sewage. high dissolved oxygen concentration, can offer an
However, in recent years there has been an in- ecologically safe, less expensive, and more efficient
creased research emphasis on the use of nonsus- means to remove nutrients and metals than conven-
pended algae, either as unialgal cultures immobi- tional tertiary treatment (Oswald 1988a, b, c, Hunt-
lized in a polymeric matrix or as attached algal com- ley et al. 1989, Redalje et al. 1989, Lincoln and Earle
munities (biofilm/periphyton) growing in shallow, 1990, de la Noüe et al. 1992). These benefits can be
artificial streams or on the surfaces of rotating bio- achieved with little or no use of chemical additives
logical contactors (RBC/biodiscs). and, furthermore, may offer the benefit of resource
In this minireview, I focus on the use of algae in recovery and recycling (see Table 1 for a compari-
advanced treatment of wastewater, comment on son between algal-based treatment systems and con-
some of the advantages and disadvantages of this ventional treatment for the removal of phosphorus).
biotechnology, and suggest the likely direction of To achieve the desired level of treatment with algal
future research in this area. First, I briefly survey the systems, maximizing autotrophic production is of
extensive work on suspended algal systems, with em- primary importance (Goldman 1979b), and basic
phasis on more recent research. Then I follow this principles of algal mass culture (Huntley et al. 1989,
with a more complete summary of the research on Richmond 1992) must be applied, particularly the
nonsuspended algal systems. need to effectively harvest the algal biomass in order
to remove the sequestered nutrients. The largest
NATURE OF THE PROBLEM
body of information on how to accomplish accept-
Declining water quality, associated with human ac- able levels of wastewater treatment with algae is
tivities, has created environmental and public health available for suspended algal systems.
problems. For example, one cause of the toxic algae High-Rate Algal Ponds (HRAP) are shallow oxi-
fish kills recently experienced on the east coast of dation ponds that encourage the growth of sus-
the United States is thought to be nutrient loading pended microalgae. These systems, which are some-
by wastewater discharge into the rivers that empty times constructed as raceways (circular channels
into the estuaries (Glasgow et al. 1995). This nutri- with provisions for mixing the microalgae) have
ent loading can be substantial since many conven- been used throughout the world for wastewater
tional treatment plants discharge .106 L of waste- treatment for many years. Oswald (1988b, c) provid-
water per day, and nutrients in wastewater can be ed detailed reviews of these systems. It has been re-
three orders of magnitude more concentrated than peatedly shown that HRAPs can achieve a high level
in the receiving water (de la Noüe et al. 1992). of treatment of both domestic and agricultural
wastewater, as measured by reductions in BOD, TSS,
1 Received 25 November 1997. Accepted 8 June 1998. nitrogen, phosphorus, and metals (Shelef et al.
2 Author for reprint requests; e-mail jphoffma@zoo.uvm.edu. 1980, Fallowfield and Garrett 1985, Picot et al. 1991,
757
758 JAMES P. HOFFMANN

TABLE 1. Comparison of tertiary treatment technologies for the removal of phosphorus from wastewaters. The treatment type Chemical refers to the
conventional method of concentrating phosphate in sewage sludge by precipitation with aluminum or iron compounds added to the wastewater. The
treatment types HRAP, Immobilized, and Periphyton refer to the algal-based technologies described in the text. Values listed as ranges encompass the reported
data.

Phosphorus concentration
Algal (mg·L21) Highest reported Range of
Treatment productiona percentage residence Selected sources
type (g·m22·day21) Influent Effluent removed times (days) (see text for others)

Chemical — 3–15 0.2–1.0 .95% 0.3–0.5 Tchobanoglous & Burton 1991


Laliberté et al. 1994
HRAP 10–35 7–15 0.5–1.0 94–97% 2–6 Oswald 1988a, b
Shelef et al. 1980
Immobilized NRb 7–10 ,1–4 .90% 0.3–0.8 Travieso et al. 1992
Yan et al. 1996
Periphyton 10–35 3–5 0.2–1.7 .95% 0.014–7 Craggs et al. 1996a, b
Hoffmann (unpubl.)
a Dry weight.
b Not reported.

Muttamara et al. 1995). Furthermore, processing of vestigated. A two or more unit increase in pH, due
the harvested algae may result in significant re- to intense algal photosynthesis, typically occurs in
source recovery. For example, the feasibility of using these ponds (Azov and Shelef 1987). At high pH,
microalgae to recycle manure nitrogen in a swine polyvalent cations, such as calcium and magnesium,
production facility has been demonstrated (Lincoln interact with phosphates to precipitate as an algal–
1985, Lincoln and Earle 1990). Our understanding mineral complex (Nurdogan et al. 1993). There-
of HRAPs is the most advanced of all the algal treat- fore, this mechanism, which is referred to as auto-
ment systems. The specific details of optimal design flocculation, contributes not only to the lowering of
criteria (size, depth, hydraulic loading, flow rates, the phosphorus concentration, but also aids in the
etc.) have been thoroughly researched, reviewed, removal of the suspended algae from the effluent.
and updated at regular intervals (see Oswald However, wastewater often is deficient in calcium
[1988a] for the most recent comprehensive treat- and magnesium. Nurdogan et al. (1993) demon-
ment of the engineering aspects of these systems). strated that adding lime to the wastewater increased
Algal diversity over an annual cycle in HRAPs tends phosphorus removal efficiency to .90%. Moutin et
to be low (generally #12 taxa) with the genera Chlo- al. (1992) examined, both empirically and theoret-
rella, which has a short generation time, and Scene- ically, the chemical mechanisms involved in the re-
desmus, which is more resistant to predation, often duction of phosphate and concluded that ortho-
dominating the community at different times of the phosphate concentration was being controlled by
year (Canovas et al. 1995). the solubility of a calcium phosphate mineral. How-
There has been considerable effort directed to- ever, subsequent modeling and validation by Mesplé
ward modeling HRAPs. The specific objectives of et al. (1995, 1996) suggested that uptake by sus-
these efforts have included predicting algal biomass pended algae was more important to orthophospha-
concentration, productivity, and oxygen production te removal than chemical precipitation.
(Kroon et al. 1989, Martin and Fallowfield 1989); The principal disadvantage of HRAPs is the diffi-
analyzing the economics of design parameters on culty and associated cost of harvesting the small
treatment costs (Oron and Shelef 1980); optimizing (,20 mm), suspended microalgae (Huntley et al.
algal biomass production (Sukenik et al. 1991); and 1989). Many harvesting methods (filtration, flota-
exploring the mechanisms responsible for soluble tion, flocculation, sedimentation, centrifugation, mi-
phosphorus removal (Mesplé 1996). Dynamic com- crostraining) have been investigated (see Laliberté
puter models have been developed that include spe- et al. [1994] for an overview and Mohn [1988], Os-
cific details of algal nutrient uptake kinetics and me- wald [1988a], and Huntley et al. [1989] for specific
tabolism and that incorporate first principles of the details of these techniques). Although it is techni-
physicochemical mechanisms of nutrient removal cally possible to remove these particles, none of the
that operate in these systems. These models are ca- approaches has proven to be simple, inexpensive,
pable of accurately predicting the observed algal and suitable to large-scale outdoor cultures. Accept-
productivity and treatment efficiency of the systems able treatment in terms of low effluent BOD, TSS,
(Buhr and Miller 1983, Moreno-Grau et al. 1996). and nutrient concentrations cannot be achieved
One of the earliest efforts to remove phosphorus without adequate harvest of the algal crop (Cromar
from sewage with suspended algae was described by et al. 1992). This difficulty has stimulated different
Bogan et al. (1961). More recently, the specific role research directions, one of which is the attempt to
of algal-mediated pH increase in the interaction be- select dominant species that are easy to harvest.
tween calcium and phosphate in HRAPs, with the Talbot and de la Noüe (1993) cultured an epilith-
subsequent precipitation of phosphate, has been in- ic, filamentous cyanobacterium, Phormidium bohneri,
WASTEWATER TREATMENT WITH ALGAE 759

on secondary effluent in the laboratory and found species also have different tolerances to ammonia.
nutrient removal rates comparable to suspended mi- An isolate of Chlorella from a waste pond was able to
croalgae. The tendency for this alga to self-aggregate grow at 10 mM NH3 and was more tolerant than a
and sink to the sediments facilitates its harvesting. Euglena isolate (Konig et al. 1987). Grazing of the
Hashimoto and Furukawa (1989) also found a high algae by zooplankton in HRAPs can also be signifi-
nutrient removal rate and easy harvestability of Os- cant. Canovas et al. (1995) present evidence that
cillatoria when it was grown on activated sludge ef- suggests algal species shifts may be partly due to
fluent. However, due to contamination with small, grazing, and Oswald (1988c) has observed periodic
rapidly growing microalgae, species control in large- grazing of Chlorella that was sufficient to deplete the
scale, outdoor open systems is a major problem algae and cause the pond to become anaerobic. In
(Chaumont 1993), and efforts to selectively favor general, though, when these ponds are properly
and sustain the more easily harvested but slower- managed in terms of organic loading, they are quite
growing filamentous forms of algae have had mixed stable in their performance despite changes in algal
results. Benemann et al. (1980) used microscreen- community structure.
ing of Oscillatoria filaments and the colonial green The use of nonsuspended algae to treat wastewa-
alga Micractinium, with subsequent reinoculation ter is a logical way to obviate the harvesting prob-
into the algal pond, in an attempt to establish dom- lem. Immobilizing microalgae in a polymeric matrix
inance of these easily harvested taxa. They were un- is one approach that has been investigated. The bio-
able to sustain dominance and concluded that bio- technology of immobilizing cells is an extension of
mass recycle was not a satisfactory means of species the techniques developed for immobilizing enzymes
control. However, more recent work in South Africa and organelles in closed bioreactors for producing
(Pretorius and Hensman 1985, Wood 1987) has marketable metabolites. Robinson et al. (1986),
been more promising. These workers used a com- Huntley et al. (1989), de la Noüe et al. (1990), and
bination of short hydraulic retention times to wash Becker (1994) have reviewed this technology, as ap-
out the smaller suspended microalgae and crossflow plied to algae, and they provide specific details of
microscreening to retain larger algae and success- the technique. The potential advantages are many;
fully sustained dominance by easily harvested Stigeo- those particularly relevant to wastewater treatment
clonium. Biological methods of harvesting the sus- are better species control, faster removal rates of nu-
pended algae have also been investigated. A com- trients and therefore higher loading rates, avoid-
mon approach that has been successful in the trop- ance of washout, and cell-free effluent. Work to date
ics has been to integrate the production of algae has all been at the laboratory bench scale.
growing on wastewater with aquaculture (see Pan- Studies have consistently indicated efficient and
tastico [1987] for a review of this topic). An algal– rapid removal of nitrogen and phosphorus from
fish system model was developed by McDonald wastewater by immobilized algae over a range of
(1987), and model output suggested phosphorus re- temperatures, pH, and light levels (Chevalier and de
moval of $88%. Meiring et al. (1993) achieved la Noüe 1985, de la Noüe and Proulx 1988, Travieso
some success by integrating a trickling filter into a et al. 1992, Canizares et al. 1993, 1994, Kaya et al.
HRAP system. The algae became entrapped in the 1994, Vilchez and Vega 1994, Yan et al. 1996). Ni-
biofilm of the trickling filter and were easily har- trogen and phosphorus removal efficiencies of
vested. .90% over periods of ,24 h have regularly been
Some of the other concerns with HRAPs, al- measured. Both Cyanophyceae and Chlorophyceae
though not as vexing as the difficulty of harvesting taxa have been used in these studies and include
the algae, are related to costs and operational sta- Anabaena, Phormidium, Spirulina, Chlamydomonas,
bility. Although the construction and operation Chlorella, and Scenedesmus. Carrageenan, chitosan,
costs of HRAPs are very favorable compared to con- and alginate are the polymers often used in these
ventional treatment systems (Oswald 1988b, c), the algal systems, with alginate beads being used most
availability and cost of land required for these pond frequently. A comparison among these polymers
systems could be prohibitive in urban environments. suggests that chitosan enhanced the removal of an-
Another constraint is climate; these systems function ions while carrageenan improved cation removal
best in warmer regions not subjected to freezing (Mallick and Rai 1994). Kaya et al. (1994) recently
winters. The issue of ammonia toxicity to algae has showed that Scenedesmus immobilized on alginate
been investigated and found significant at short hy- sheets achieved higher nutrient uptake rates than
draulic retention times (48 h) when concentrations when immobilized on alginate beads. It has also
above 2 mM NH3 and pH values above 8.0 occurred been shown that a starvation pretreatment of 24 h
(Abeliovich and Azov 1976). However, at longer re- increased phosphate uptake rates by 33% (Mallick
tention times (several days), higher pH values (be- and Rai 1994). Heavy metal removal also has been
tween 9 and 10) were observed which volatilized am- investigated with immobilized algal systems. Da Cos-
monia and allowed for continued algal growth (Abe- ta and Leite (1991) reported nearly 100% removal
liovich and Azov 1976, Azov and Shelef 1987, Picot of cadmium and zinc and Wilkinson et al. (1989)
et al. 1991, Nurdogan et al. 1993). Different algal reported .99% removal of mercury by immobilized
760 JAMES P. HOFFMANN

algae; however, it was also observed that subsequent plankton communities, when normalized per unit
mercury volatilization was extensive. weight and time, consistently showed periphyton
Given these high removal rates and efficiencies had higher average uptake rates. Furthermore, the
and the ease of algal removal, immobilized algal sys- tanks with periphyton and plankton had a maxi-
tems appear to be a good choice for wastewater mum soluble phosphorus reduction of 98% at the
treatment. However, when scaled to the size needed end of the experiment compared to 17% for the
to effectively treat a community’s wastewater, the tanks with only plankton. More recently, a novel ap-
cost of the polymeric matrix becomes prohibitive proach of exposing wastewater to algae grown on a
(Laliberté et al. 1994). Nevertheless, research on im- rotating disk followed by a denitrification bed was
mobilized algae for wastewater treatment is in a very shown to remove 90% of the nitrogen from the
early stage. It seems likely that the search for inex- wastewater (Przytocka-Jusiak et al. 1984). In this two-
pensive polymers will ultimately be successful. With step process, the algae provided a replacement for
future research on the sustainability of the cultures methanol as the carbon source for the denitrifying
and the frequency of harvesting needed to avoid sat- bacteria.
uration and effectively remove the sequestered nu- Sládečková et al. (1983) and Vymazal (1988) dem-
trients, the potential of this technique for practical onstrated the feasibility of using artificial streams
wastewater treatment may be realized. (fitted with nylon screens to support extensive pe-
Another approach that obviates the harvesting riphyton communities) to remove nutrients from
problem associated with HRAPs is the use of algae polluted waters. Cook et al. (1986) and Morris et al.
attached to surfaces as periphyton biofilms. The di- (1988) established the feasibility of using a periphy-
versity and seasonal dynamics of the algal commu- tic algal system to remove nutrients from wastewater
nity that naturally develop on temperate outdoor- under light and temperature conditions comparable
submersed surfaces in conventional wastewater to winter in a northern climate. More recently, Adey
treatment facilities have been described by Davis et and coworkers have used an attached algal system,
al. (1990a). Sládečková (1994) also provided a list known as an algal turf scrubber (ATSy), for the
of both algal and nonalgal periphyton taxa that treatment of agricultural run-off and domestic
grow in wastewater. The algal genera most common- wastewater (Adey et al. 1993, Craggs et al. 1996a, b).
ly reported in such communities are Oscillatoria, The ATSy was developed for maintaining the water
Phormidium, Lyngbya, Navicula, Nitzschia, Oedogonium, quality of aquaria and is described in detail in Adey
Scenedesmus, and Stigeoclonium. Davis et al. (1990b) and Loveland (1991). These studies have consis-
also determined that seasonal production and nu- tently shown peak periphyton production in the
trient removal potential of these periphyton com- range of 25 to 35 g dry weight·m22·day21, which is
munities was comparable to suspended algal sys- comparable to peak production typically reported
tems. for HRAPs. However, unlike in HRAPs, the algae
One of the first reports on the use of attached can be harvested by simple mechanical means.
algae for removing nutrients from sewage was by Diurnal shifts in pH of two or more units have
Bush et al. (1963). They reported maximum remov- been observed in wastewater streams containing al-
al of 76% for phosphorus and nearly 100% for ni- gal periphyton (Bush et al. 1963, Hemens and Ma-
trogen in the effluent from an elongated raceway son 1968, Morris et al. 1988, Craggs et al. 1996a, b).
pond in which the algae were attached to the lining. This is comparable to that reported above for
Hemens and Mason (1968) evaluated wastewater HRAPs. The pH-dependent, calcium-phosphate pre-
tertiary treatment using an outdoor shallow stream. cipitation that can occur in HRAPs also seems to
Their system included a 3 km long by 50 cm wide occur in these wastewater streams. Craggs et
slow- flowing channel in which microalgae had set- al.(1996b) suggested that the high mean phospho-
tled to the bottom. They reported .90% nitrogen rus concentration of the periphyton harvest (2.1%
and phosphate removal during the warmer months, of the dry weight) was a result of the incorporation
brought about by volatilization and precipitation, re- of a phosphate precipitate into the biofilm. Work by
spectively, with lower removal efficiencies during the House et al. (1989) showed that coprecipitation of
colder months. The effectiveness of their system was phosphate with calcium occurs in natural streams
directly dependent on the elevated pH of the waste- due to elevated pH brought about by algal photo-
water that is mediated by algal photosynthesis. Tor- synthesis. Elevated pH within algal biofilms may also
pey et al. (1971) and Jackson and Jackson (1972) contribute to precipitation of metals (Bender et al.
described the use of periphyton on illuminated ro- 1994, Liehr et al. 1994).
tating discs partially submersed in wastewater tanks. The complex interactions among carbon, light,
A complex community of unicellular and filamen- and pH in algal biofilms has been extensively inves-
tous algae, bacteria, protozoa, and metazoans devel- tigated and modeled (Liehr et al. 1988, 1989, 1990,
oped on the disks. Jackson and Jackson (1972) con- Flora et al. 1995). The modeling results have made
ducted a 29-day experiment with an initial waste- clear the importance of the steep concentration gra-
water phosphorus concentration of 12 mg·L21. A dient and boundary layer in driving diurnal pH
comparison of 32P-PO4 activity in the periphyton and swings in these biphasic systems. Kuenen et al.
WASTEWATER TREATMENT WITH ALGAE 761

(1986) used microelectrodes to measure the O2 and systems to close the gap in our understanding of
pH isopleths of an algal biofilm on a trickling filter nonsuspended versus suspended algal systems. For
at a sewage treatment plant. Their empirical work, both systems, it is likely that a more integrated ap-
which is consistent with the modeling efforts men- proach in the context of ecological engineering at
tioned above, demonstrated a 100–500 mm thick dif- the ecosystem level will be emphasized. The work by
fusive boundary layer in the water above the biofilm Drenner et al. (1997) on a periphyton–fish treat-
and also revealed the rapid dynamics that occurred ment system is a recent example of this approach.
during the transition from dark to light when pH The fundamental principles of the ecological design
was observed to increase from 8.1 to 9.7 over a 25- of these living technologies for wastewater treatment
min period. Furthermore, their results, along with have recently been summarized by Todd and Jo-
the results of Kugaprasatham et al. (1992), empha- sephson (1996) and underlie the applications de-
sized the need for sufficient current velocity and tur- scribed by Guterstam (1990) and Teal and Peterson
bulence to ensure adequate nutrient flux into the (1991).
biofilms of wastewater systems. The practical goal of species control in these hy-
Given the comparable performance of attached pereutrophic culture systems also may present a
algal systems to HRAPs and the obvious ease of har- unique opportunity to community ecologists who
vesting, it would seem that periphytic systems would study assembly rules. The low algal diversity in these
be superior for algal-based wastewater treatment. systems would seem to imply fewer interactions and
However, most investigations have been at the lab- since the investigator has a greater ability to control
oratory scale and only two wastewater studies have and manipulate these cultures than natural systems,
been done at a pilot scale over an annual cycle (He- the mechanisms leading to dominance may be more
mens and Mason 1968, Craggs et al. 1996a, b). Re- tractable.
searchers have much less experience with periphytic
systems than with HRAPs. The long-term sustaina- Abeliovich, A. & Azov, Y. 1976. Toxicity of ammonia to algae in
bility of treatment efficiency of periphytic systems sewage oxidation ponds. Appl. Environ. Microbiol. 31:801–6.
has not been established. In particular, the potential Adey, W., Luckett, C. & Jensen, K. 1993. Phosphorus removal
from natural waters using controlled algal production. Restor.
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toux, J., Mara, D. D., Pearson, H. W. & Silva, S. A. 1995.
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