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Fungal Communities in Terrestrial Ecosystems

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Geoactive Fungal Roles in the Biosphere

Geoffrey Michael Gadd

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9.1 Introduction .................................................................................................................................................................121

9.2 Metal–Fungal Interactions and Transformations ....................................................................................................... 122
9.2.1 Metal Mobilization ......................................................................................................................................... 122
9.2.2 Metal Immobilization ..................................................................................................................................... 122
9.3 Bioweathering of Rocks and Minerals: Mineral Transformations ............................................................................. 123
9.3.1 Mineral Formation .......................................................................................................................................... 123
9.3.2 Mineral Biodeterioration ................................................................................................................................ 123
9.4 Common Mineral and Biomineral Transformations by Fungi ................................................................................... 124
9.4.1 Carbonates ...................................................................................................................................................... 124
9.4.2 Oxalates .......................................................................................................................................................... 124
9.4.3 Oxides ............................................................................................................................................................. 125
9.4.4 Phosphates ...................................................................................................................................................... 125
9.4.5 Silicates ........................................................................................................................................................... 126
9.4.6 Reduction or Oxidation of Metals and Metalloids ......................................................................................... 126
9.4.7 Other Mycogenic Minerals ............................................................................................................................. 126
9.5 Fungal Symbioses in Geomycology ........................................................................................................................... 126
9.5.1 Lichens ............................................................................................................................................................ 127
9.5.2 Mycorrhizas .................................................................................................................................................... 127
9.6 Environmental and Applied Significance of Geomycology ....................................................................................... 127
9.7 Conclusions ................................................................................................................................................................. 129
9.8 Acknowledgments....................................................................................................................................................... 129
References ............................................................................................................................................................................ 130

9.1 INTRODUCTION the biosphere, with the chemo-organotrophic metabolism of

fungi determining all fungal activities and interactions with
Geomycology can be defined as “the scientific study of the environment. A variety of inorganic or organic fungal
the roles of fungi in processes of fundamental importance metabolites can serve as chemical reactants in processes
to geology” in past, current, and future contexts (Gadd such as metal immobilization or solubilization and rock and
2007a, 2011; Gadd et al. 2012). Important topics under this mineral bioweathering, while biomechanical effects on solid
heading include bioweathering of rocks and minerals, soil substrates result from the fungal branching filamentous
formation, the transformation and accumulation of metals, growth form (Burford et  al. 2003a; Gadd 2007a, 2008a).
and the cycling of elements and nutrients. Organic matter “Geomycology” can be considered a subset of “geomicro-
decomposition and degradation can also be included, since biology,” namely the role of microorganisms and microbial
these result in major biogeochemical cycling of elements in processes in geological and geochemical processes (Ehrlich


and Newman 2009; Gadd 2010). Although appreciation of et al. 2001; Fomina et al. 2003; Gadd et al. 2012). Many met-
fungi as agents of biogeochemical change is growing, they als, for example, Na, K, Cu, Zn, Co, Ca, Mg, Mn, and Fe,
are frequently neglected within broader geomicrobiological are essential for life, but all metals can be potentially toxic
contexts (Gadd 2008b). Undoubtedly, the main reason for when present above certain threshold concentrations. Other
this is the vast metabolic diversity found in archaea and bac- metals, for example, Cs, Al, Cd, Hg, and Pb, have no known
teria, including their widespread abilities in using a variety metabolic function in fungi but can still be accumulated.
of terminal electron acceptors in respiration and affecting Metal toxicity is affected by physico-chemical conditions
many different redox transformations of metal species (Gadd and the chemical behavior of the particular metal species
2008b; Kim and Gadd 2008). However, in aerobic terres- (Gadd 1993a; Howlett and Avery 1997; Fomina et al. 2005c).
trial environments, fungi are of great importance, especially However, fungi are ubiquitous in metal-polluted locations,
when considering rock surfaces, soil, and the plant root–soil and a variety of direct and indirect mechanisms contribute to
interface. Free-living fungi have a major role in the decom- their survival. Such mechanisms include reduction of metal
position of plant and other organic materials, including uptake and/or increased efflux; metal immobilization by,
xenobiotics, and, therefore, in the biogeochemical cycling for example, biosorption to cell walls and exopolymers and
of all the elements associated with such substances (e.g., bioprecipitation; intracellular sequestration by, for example,
C, N, P, S, and metals) (Gadd 2004a, 2007a, 2008a). Fungi metallothioneins and phytochelatins; and localization in
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are also important components of rock-inhabiting micro- vacuoles (Gadd et  al. 1987; Gadd 1993a; Joho et  al. 1995;
bial communities, participating in mineral dissolution and Blaudez et  al. 2000; Perotto and Martino 2001; Baldrian
secondary mineral formation (Burford et al. 2003a,b, 2006; 2003; Meharg 2003). The mechanisms by which fungi (and
Fomina et al. 2005a,b; Gadd et al. 2005, 2007; Gadd 2007a). other microorganisms) change metal speciation and mobil-
As a result of these properties, fungi can be major biodete- ity not only influence survival but are also components of
riorative agents of stone, wood, plaster, cement, and other biogeochemical cycles for metals and other elements that
building materials (Gadd et al. 2014). Mycorrhizal fungi are may be associated with organic and inorganic substrates,
associated with most plant species and are involved in major including carbon, nitrogen, sulfur, and phosphorus (Gadd
redistributions of inorganic nutrients (Fomina et al. 2006; 2004a, 2006, 2007a,b, 2008a). These may be considered in
Finlay et  al. 2009), while lichens, a fungal growth form, terms of metal mobilization or immobilization.
play important role in rock colonization and early stages of
mineral soil formation (Haas and Purvis 2006). Free-living 9.2.1 Metal Mobilization
fungi may also have a role in the maintenance of soil struc-
ture, owing to their filamentous branching growth habit Metal mobilization from rocks, minerals, soil, and
and exopolymer production (Ritz and Young 2004). In the other substrates can be a consequence of protonolysis; car-
aquatic environment, fungi are also important decomposers bonic acid formation from respiratory CO2; complexation by
(Reitner et al. 2006; Edgcomb et al. 2011). Fe(III)-binding siderophores and other excreted metabolites,
This chapter emphasizes the importance of fungi as for example, amino acids, phenolic compounds, and organic
agents of geochemical change, particularly regarding roles in acids; and methylation, which can result in volatilization.
rock, mineral, metal, and soil transformations. It also high- Fungal-excreted carboxylic acids can attack mineral surfaces
lights the applied significance of geomycological processes in (see later), providing protons as well as a metal-chelating
such areas as bioremediation, revegetation, metal and mineral anion, for example, citrate (Burgstaller and Schinner 1993).
biorecovery, and production of novel biomineral products. Oxalic acid can leach metals that form soluble oxalate
complexes, for example, Al and Fe (Strasser et  al. 1994).
Solubilization mechanisms can result in metal mobilization
9.2 METAL–FUNGAL INTERACTIONS from toxic-metal-containing minerals, for example, pyromor-
AND TRANSFORMATIONS phite [Pb5(PO4)3Cl]; contaminated soil; and other solid wastes
(Sayer et al. 1999; Fomina et al. 2004, 2005b,c). Fungi may
Metals are central to almost all geomicrobial processes, also mobilize metals and attack mineral surfaces by redox
and their transformations and alterations in mobility are transformations: Fe(III) and Mn(IV) solubility is increased
important in bioweathering, mineral formation and disso- by reduction to Fe(II) and Mn(II), respectively. Fungal
lution, and soil formation. Metals, metalloids, metal radio- reduction of Hg(II) to volatile elemental Hg(0) has also been
nuclides, organometals, and organometalloids, and their recorded (Gadd 1993b). Metals may also be mobilized from
compounds, interact with fungi in various ways, depending organic substrates during decomposition (Gadd 2008b).
on chemical speciation, organism, and environment, with
the fungi also able to influence metal speciation and mobil- 9.2.2 Metal Immobilization
ity (Gadd and Griffiths 1978, 1980; Gadd 1984, 1992, 1993a,
2004a,b, 2005, 2007a,b, 2008c, 2009a,b; Newby and Gadd Fungal biomass can be an effective accumulator of met-
1987; Dutton and Evans 1996; Ramsay et  al. 1999; Gadd als and related substances. Important mechanisms include

biosorption to cell walls, pigments, and exopolymers; metal speciation and mobility, especially when metals are
intracellular transport; accumulation and sequestration; a component of the interacting mineral or are present in the
or bioprecipitation on and/or around hyphae (Gadd 1993a, cellular microenvironment.
2000a,b, 2001a,b,c, 2007a, 2009a; Baldrian 2003; Fomina
et al. 2007b,c; Fomina and Gadd 2014). Living or dead fun- 9.3.1 Mineral Formation
gal biomass can be an effective biosorbent for a variety of
metals, including Ni, Zn, Ag, Cu, Cd, and Pb, as well as Biomineralization refers to the processes by which
actinides, for example, U and Th, with a variety of func- organisms form minerals. Biologically induced mineraliza-
tional groups being involved (Gadd 1990, 1993a; Sterflinger tion (BIM) is where an organism modifies the local micro-
2000; Fomina and Gadd 2014). The presence of chitin and environment, creating conditions that favor extracellular
pigments such as melanin enhances the ability of fungal bio- chemical precipitation of mineral phases. The organism
mass to act as a biosorbent. Fungal biomineralization pro- does not appear to control the biomineralization process in
cesses also lead to metal immobilization as biominerals or BIM, while a great degree of control over biomineraliza-
elemental forms, as described later (Gadd 2007a). tion is exerted in biologically controlled biomineralization
(BCM), for example, complex cellular biomineral struc-
tures in certain eukaryotes (Gadd and Raven 2010). Fungal
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9.3 BIOWEATHERING OF ROCKS AND biomineralization, therefore, usually refers to biologically

MINERALS: MINERAL TRANSFORMATIONS induced mineralization. This can result from redox transfor-
mations of a metal species and from metabolite excretion,
Weathering is a process in which rock is broken down for example, CO2 and oxalate (Gadd et  al. 2012, 2014). It
into smaller particles and finally to constituent minerals, can also result from organic matter decomposition, where
ultimately leading to mineral soil formation (Tazaki 2006; released substances reprecipitate with metals in the micro-
Ehrlich and Newman 2009). Physical, chemical, and biolog- environment, and vice versa, with fungal surfaces providing
ical processes are involved: bioweathering can be defined reactive sites for sorption (≡ biosorption), which can also
as the erosion and decay of rocks and minerals, mediated lead to formation of mineral precipitates (Lloyd et al. 2008;
by living organisms. Many fungi are effective biologi- Gadd 2009a, 2010).
cal weathering agents (Gorbushina et  al. 1993; Sterflinger
2000; Verrecchia 2000; Burford et al. 2003a,b; Gadd 2007a; 9.3.2 Mineral Biodeterioration
Gorbushina and Broughton 2009; Sverdrup 2009). Fungi are
probably associated with all rocks and minerals, building Direct and indirect biomechanical and biochemical
stone, and concrete (Burford et  al. 2003a,b; Gleeson et  al. mechanisms are involved in mineral biodeterioration (Sand
2005, 2006, 2007, 2010; Gorbushina 2007; Gorbushina and 1997; Edwards et al. 2005; Lian et al. 2008; Bonneville et al.
Broughton 2009). Lichens are also highly significant bio- 2009, 2011; McMaster 2012). These are also thought to be
weathering agents (Adamo and Violante 2000; Adamo et al. significant mechanisms in bioweathering. Biomechanical
2002). Lithobiotic biofilm communities can interact with deterioration of rocks and minerals occurs through penetra-
mineral substrates, and deterioration of this can also result tion, boring, and burrowing into porous or decaying mate-
in the formation of patinas, films, varnishes, crusts, and rial and along crystal planes in, for example, calcitic and
stromatolites (Gadd 2007a; Gorbushina 2007; Fomina et al. dolomitic rocks (Sterflinger 2000; Golubic et al. 2005; Smits
2010). Mycorrhizal fungi are also very important in mineral 2006; Gadd 2007a; Cockell and Herrera 2008). Biochemical
weathering and dissolution of insoluble metal compounds weathering of rocks and minerals occurs through excre-
in the soil. Acidification is an important fungal bioweath- tion of, for example, H+, CO2, organic acids, siderophores,
ering mechanism, with low–molecular-weight organic acid and other metabolites, and is thought to be more impor-
anions being especially significant (Gadd 1999; Hoffland tant than mechanical degradation. This can result in pitting
et al. 2004). Because production of these substances has a and etching to complete dissolution (Drever and Stillings
carbon cost, symbiotic mycorrhizal fungi that are provided 1997; Ehrlich 1998; Gharieb et al. 1998; Kumar and Kumar
with organic carbon compounds by the plant host may have 1999; Adamo and Violante 2000; Adeyemi and Gadd 2005;
an advantage over free-living saprotrophs (Hoffland et  al. Edwards et al. 2005; Wei et al. 2012b). Oxalate is particu-
2004). It should be stressed that the activities of all groups larly important in biodeterioration of uranium oxides and
of microbes and interactions between them should be con- depleted uranium (Fomina et al. 2007a,b, 2008; Gadd and
sidered in bioweathering. Fungal–bacterial interactions are Fomina 2011). Mineral dissolution may result in release
likely to be significant in mineral weathering in the root of toxic (Sayer et  al. 1999) or essential metals such as K
environment, as well as in many rock and mineral substrates (Lian et  al. 2008). Fungi acidify their microenvironment
(Balogh-Brunstad et al. 2008; Koele et al. 2009). Fungi are via a number of mechanisms, which include the excretion
involved in the formation and deterioration of minerals, of protons and carboxylic acids, while respiratory CO2  can
most such interactions being accompanied by changes in result in carbonic acid formation. In addition, fungi excrete a

variety of other metal-complexing metabolites (e.g., sidero- play an important role in the environmental fate, bioremedi-
phores, amino acids, and phenolic compounds) (Burgstaller ation, or biorecovery of Sr or other metals and radionuclides
and Schinner 1993). Fungal tunnels within soil minerals that form insoluble carbonates (Li et al. 2015). Paecilomyces
have been explained as a result of dissolution and “bur- javanicus was found to mediate formation of an unknown
rowing” within the mineral matrix (Jongmans et  al. 1997; lead–mineral phase after incubation in liquid media with
Landeweert et  al. 2001; Golubic et  al. 2005; Cockell and lead shot. After 2-weeks incubation, precipitated min-
Herrera 2008). Fungi may also explore pre-existing cracks, eral phase particles were found to contain plumbonacrite
fissures, pores, and weak points in weatherable minerals and [Pb10(CO3)6O(OH)6]. However, after 4-weeks incubation,
build a matrix of secondary minerals of the same or dif- the lead particles that accumulated inside the fungal pel-
ferent chemical composition as the substrate, for example, lets were transformed into a white mineral phase composed
secondary CaCO3  precipitation in calcareous soil and rock of lead oxalate (PbC2O4), hydrocerussite [Pb3(CO3)2(OH)2],
(Verrecchia 2000) or oxalate formation (Fomina et al. 2010; and a new species of lead hydroxycarbonate, thus revealing
Gadd et  al. 2014). This can result in fissures and cracks novel steps in lead carbonation by fungi (Rhee et al. 2016).
becoming cemented with mycogenic minerals, and after Insoluble carbonates may be broken down by fungal
death and degradation of fungal hyphae, tunnels may be left attack, usually the result of acid formation, but may also
within the minerals (Fomina et al. 2010). involve biophysical processes (Lian et al. 2008), and various
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fungi and lichens have this property (Adamo and Violante

2000; Cockell and Herrera 2008; Lian et  al. 2008). Such
9.4 COMMON MINERAL AND BIOMINERAL activity is particularly evident on limestones and marble
TRANSFORMATIONS BY FUNGI used in building construction but can also occur in natu-
ral limestone (Golubic et  al. 2005; Cockell and Herrera
Fungi may be involved in many nonspecific mineral trans- 2008). Fungal attack on carbonate substrates (dolomites and
formations in the environment at differing scales (Hutchens limestones) can result in diagenesis of these substrates to
2009; Rosling et al. 2009; Smits 2009), especially when con- dolomite [CaMg(CO3)2], glushinskite (MgC2O4.2H2O), wed-
sidering their ubiquity and capacity for production of mineral- dellite (CaC2O4.2H2O), whewellite (CaC2O4.H2O), and pos-
transforming metabolites, their symbiotic associations, and sibly struvite (NH4MgPO4·6H2O) (Kolo et al. 2007).
the consequences of their significant environmental proper-
ties such as organic matter decomposition (Gadd 2008a,b). 9.4.2 Oxalates

9.4.1 Carbonates Calcium oxalate is the most common form of oxalate in

the environment, occurring as the dihydrate (CaC2O4.3H2O,
Certain fungi can deposit calcium carbonate extra- weddellite) or the more stable monohydrate (CaC2O4.H2O,
cellularly (Verrecchia et  al. 1990; Burford et  al. 2006; Li whewellite) (Gadd 1999; Gadd et al. 2014). The initial pre-
et  al. 2014, 2015). A mixture of calcite (CaCO3) and cal- cipitation phase is the trihydrate (CaC2O4.3H2O), which
cium oxalate monohydrate (whewellite; CaC2O4.H2O) was loses water of crystallization to form either the dihydrate
precipitated on hyphae of Serpula himantioides when or the monohydrate. Calcium oxalate can be associated
grown in simulated limestone microcosms (Burford et  al. with free-living, pathogenic, and plant-symbiotic fungi and
2006). Urease-positive fungi can be used for the precipi- lichens and is formed by precipitation of soluble calcium as
tation of metal-containing carbonates, which provides the oxalate (Gharieb et  al. 1998; Gadd 1999; Gharieb and
a means of metal biorecovery and purification (Li et  al. Gadd 1999; Adamo and Violante 2000; Adamo et al. 2002;
2014). Incubation of Neurospora crassa in urea-containing Pinzari et  al. 2010). Fungal calcium oxalate can exhibit a
media  provided a system for the formation of calcite, variety of crystalline forms (tetragonal, bipyramidal, plate-
as well as carbonates containing other metals. When a like, rhombohedral, or needles) (Arnott 1995). Calcium
carbonate-laden N. crassa culture supernatant was mixed oxalate has an important influence on soil biogeochemis-
with CdCl2, the Cd was precipitated in the form of otavite try, acting as a calcium reservoir, and can also influence
(CdCO3), thus immobilizing the cadmium. The otavite was phosphate availability. The natural dihydrate form of cal-
of high purity, and a small proportion exhibited nanoscale cium sulfate (CaSO4.2H2O) (gypsum) found in gypsifer-
dimensions, which may provide further advantages for ous soils and certain building construction materials, was
industrial application than larger-size biominerals (Li et al. solubilized by Aspergillus niger and Serpula himantioides,
2014). After incubation in media amended with urea and with the production of oxalic acid, resulting in precipitation
CaCl2  and/or SrCl2, Pestalotiopsis sp. and Myrothecium of calcium oxalate (Gharieb et al. 1998; Gharieb and Gadd
gramineum, isolated from calcareous soil, could precipitate 1999). Fungi can produce many metal oxalates on interact-
calcite (CaCO3), strontianite (SrCO3), vaterite in different ing with a variety of different metals and metal-bearing
forms, [CaCO3, (CaxSr1−x)CO3] and olekminskite [Sr(Sr, Ca) minerals, for example, Ca, Cd, Co, Cu, Mg, Mn, Sr, Zn,
(CO3)2], again suggesting that urease-positive fungi could Ni, and Pb (Sayer and Gadd 1997; Gadd 1999, 2007a; Sayer

et al. 1999; Jarosz-Wilkołazka and Gadd 2003; Gadd et al. 9.4.4 Phosphates
2014). Aspergillus niger and S. himantioides can transform
insoluble manganese oxide minerals, including those pro- Phosphorus occurs primarily as organic phosphate esters
duced biogenically, into manganese oxalates. In some cases, and inorganic forms, for example, calcium, aluminum, and
manganese oxalate trihydrate resulted, followed by conver- iron phosphates. Organic phosphates are hydrolyzed by
sion to manganese oxalate dihydrate (Wei et al. 2012a). The phosphatases, which liberate orthophosphate during the
formation of toxic metal oxalates may contribute to fungal microbial degradation of organic material. Fungi also mobi-
metal tolerance (Gadd 1993a; Jarosz-Wilkolazka and Gadd lize orthophosphate from insoluble inorganic phosphates by
2003). In many arid and semiarid regions, calcareous soils producing acids or chelators, for example, gluconate, citrate,
and near-surface limestones (calcretes) are secondarily oxalate, and lactate, which complex the metal, resulting in
cemented with calcite (CaCO3) and whewellite (calcium dissociation. Phosphate solubilization is very important in
oxalate monohydrate, CaC2O4.H2O), and the presence of the plant mycorrhizosphere (Whitelaw et al. 1999). Microbes
fungal filaments biomineralized with these substances can also play a role in the formation of phosphate minerals
has been reported (Verrecchia 2000). Calcium oxalate can such as vivianite [Fe3(PO4)2.8H2O], strengite (FePO4.2H2O),
also be degraded to calcium carbonate, and this may again and variscite (AlPO4.2H2O). Here, the orthophosphate may
cement pre-existing limestones (Verrecchia et  al. 2006). arise from organic phosphate degradation, while Fe or Al
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Other experimental work has demonstrated fungal pre- may arise from microbial solubilization of other minerals.
cipitation of secondary calcite, whewellite, and glushkin- Such formation of phosphate minerals is probably most
skite (MgC2O4.2H2O) (Burford et al. 2003a,b, 2006; Gadd common in soil (Ehrlich and Newman 2009). Fungal bio-
2007a). Fungal attack on a dolomitic and seawater substrate deterioration of metallic lead can result in pyromorphite
resulted in the formation of calcium oxalates (weddellite, (Pb5[PO4]3X [X = F, Cl, or OH]) formation (Rhee et  al.
CaC2O4.2H2O; whewellite, CaC2O4.H2O) and glushinskite 2012, 2014a,b). Many fungi can solubilize uranium oxides
(MgC2O4.2H2O) (Kolo and Claeys 2005). and depleted uranium and reprecipitate secondary uranium
phosphate minerals of the meta-autunite group, uramphite,
9.4.3 Oxides and/or chernikovite, which can encrust fungal hyphae to
high accumulation values of 300–400  mg U g dry wt−1
Several fungi can oxidize Mn(II) to Mn(IV)O2, includ- (Fomina et al. 2007a,b, 2008). Such minerals appear capa-
ing Acremonium spp. (Miyata et al. 2004, 2007; Saratovsky ble of long-term U retention (Fomina et al. 2007a,b, 2008;
et al. 2009). Fungal oxidation is probably nonenzymatic in Gadd and Fomina 2011). Aspergillus niger and Paecilomyces
many cases and mediated by a metabolic product (e.g., a javanicus precipitated U-containing phosphate biominer-
hydroxycarboxylic acid) or a cellular component (Ehrlich als when grown with an organic P source, with the hyphal
and Newman 2009), although involvement of laccase and/ matrix acting to localize the resultant uranium minerals.
or multicopper oxidases has been shown in ascomyce- The uranyl phosphate species identified included potas-
tes (Miyata et  al. 2004, 2007). The MnOx produced by sium uranyl phosphate hydrate (KPUO6.3H2O), meta-
Acremonium KR21-2 has a todorokite-like tunnel struc- ankoleite [(K1.7Ba0.2)(UO2)2(PO4)2.6H2O], uranyl phosphate
ture, which is different than previously reported micro- hydrate [(UO2)3(PO4)2.4H2O], meta-ankoleite [K(UO2)
bial MnOx materials, which adopt layered birnessite-type (PO4).3H2O], uramphite (NH4UO2PO4.3H2O), and cherniko-
structures (Saratovsky et al. 2009). Nonenzymatic micro- vite [(H3O)2(UO2)2(PO4)2.6H2O] (Liang et  al. 2015). These
bial Mn2+ oxidation may be affected through production organisms could also mediate lead bioprecipitation during
of organic acids such as citrate, lactate, malate, gluconate, growth on organic P substrates, which resulted in almost
and tartrate. Some fungi can oxidize Mn(II) and Fe(II) complete removal of Pb from solution and extensive precipi-
in metal-bearing minerals such as siderite (FeCO3) and tation of lead-containing minerals around biomass (Liang
rhodochrosite (MnCO3), resulting in their precipitation as et al. 2016a). These minerals were identified as pyromorphite
oxides (Grote and Krumbein 1992). Manganese and iron [Pb5(PO4)3Cl], which was only be produced by P. javanicus,
oxides are major components (20%–30%), along with clay and lead oxalate (PbC2O4), which can be produced by
(~60%) and various trace elements in the brown-to-black A. niger and P. javanicus. Two main lead biomineralization
veneers known as desert varnish or rock varnish (Grote mechanisms were therefore distinguished: pyromorphite
and Krumbein 1992; Gorbushina 2007). Conversely, man- formation, depending on organic phosphate hydrolysis, and
ganese-reducing microbes may mobilize oxidized man- lead oxalate formation, depending on oxalate excretion. This
ganese, releasing it into the aqueous phase. Most of those also indicated some species specificity in biomineralization
fungi that reduce Mn(IV) oxides reduce them indirectly (Liang et al. 2016a). Several yeast species could also medi-
(nonenzymatically), with the likely mechanism being the ate lead bioprecipitation when utilizing an organic phos-
production of metabolic products that can act as reductants phorus-containing substrate (glycerol 2-phosphate, phytic
for Mn(IV) oxides such as oxalate (Ehrlich and Newman acid) as sole phosphorus source. The minerals precipitated
2009; Wei et al. 2012a). here included lead phosphate [Pb3(PO4)2], pyromorphite

[Pb5(PO4)3Cl], anglesite (PbSO4), and the lead oxides massi- mineral interactions also play an important role in soil devel-
cot and litharge (PbO). All yeasts examined produced pyro- opment, aggregation, and stabilization (Burford et al. 2003a;
morphite, and most of them produced anglesite (Liang et al. Ritz and Young 2004). Such interactions between clay min-
2016b). Such processes may be relevant to metal immobili- erals and fungal biomass can alter the sorptive properties
zation biotechnologies for bioremediation, metal and P bio- of both clay minerals and fungal hyphae (Morley and Gadd
recovery, as well as utilization of waste organic phosphates. 1995; Fomina and Gadd 2002a). Clay minerals (e.g., ben-
tonite, palygorskite, and kaolinite) can also affect the size,
9.4.5 Silicates shape, and structure of fungal mycelial pellets (Fomina and
Gadd 2002b).
Silicates comprise 30% of all minerals and about 90% of
the Earth’s crust (Ehrlich 1998; Brehm et al. 2005; Ehrlich 9.4.6 Reduction or Oxidation of
and Newman 2009). Many species of fungi play important Metals and Metalloids
roles in the dissolution of silicates, and therefore in the genesis
of clay minerals, and in soil and sediment formation (Barker Many fungi can precipitate reduced forms of metals and
and Banfield 1996, 1998; Arocena et al. 1999, 2003; Banfield metalloids, for example, reduction of Ag(I) to elemental
et al. 1999; Adamo and Violante 2000; Tazaki 2006; Theng silver Ag(0), selenate [Se(VI)] and selenite [Se(IV)] to ele-
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and Yuan 2008). The presence of clay minerals can be a typ- mental selenium [Se(0)], and tellurite [Te(IV)] to elemental
ical symptom of biogeochemically weathered rocks, and this tellurium [Te(0)] (Kierans et al. 1991; Gharieb et al. 1995,
has been observed for lichens and ectomycorrhizas (Barker 1999). Reduction of Hg(II) to volatile Hg(0) can also be
and Banfield 1998; Arocena et  al. 1999). Bioweathering mediated by fungi (Gadd 1993b, 2000a). An Aspergillus sp.
is mainly indirect, through the production of metabolites, was able to grow at arsenate concentrations of 0.2 M, and it
together with biomechanical effects, as already discussed was suggested that increased arsenate reduction contributed
(Cromack et al. 1979; De la Torre et al. 1993; Mandal et al. to tolerance (Canovas et al. 2003a,b). Mn oxidation/reduc-
2002). Geoactive metabolites may be excreted into the bulk tion has been described previously.
phase but may also be produced by adhering organisms on
surfaces of silica or silicates, resulting in etching (Bennett 9.4.7 Other Mycogenic Minerals
et al. 2001; Wei et al. 2012b). After colonization of sheets
of muscovite, a phyllosilicate mineral, by Aspergillus niger, A range of minerals other than those mentioned above
mineral dissolution was clearly observed by a network of have been found in association with fungi (Fomina et  al.
fungal “footprints” that reflected coverage by the mycelium 2007a,b, 2008; Gadd 2007a, 2010; Gadd and Raven 2010;
(Wei et  al. 2012b). New biominerals resulted from fungal Liang et al. 2015, 2016a,b). Mycogenic secondary minerals
interactions with both zinc silicate and zinc sulfide, largely associated with fungal hyphae and lichen thalli include
resulting from organic acid excretion. Zinc oxalate dihy- desert varnish (MnO and FeO), ferrihydrite (5Fe2O3.9H2O),
drate was formed and mineral surfaces showed varying iron gluconate, calcium formate, forsterite, goethite
patterns of bioweathering and biomineral formation (Wei [α-Fe3+O(OH)], moolooite [Cu(C2O4).0.4H2O], halloysite
et  al. 2013). Such mechanisms of silicate dissolution may [Al2Si2O5(OH)4], and hydrocerussite [Pb3(CO3)2(OH)2] (Grote
release limiting nutrients such as bound P and Fe. In lichen and Krumbein 1992; Hirsch et  al. 1995; Verrecchia 2000;
weathering of silicates, calcium, potassium, iron, clay min- Gorbushina et  al. 2001; Arocena et  al. 2003; Burford et  al.
erals, and nanocrystalline aluminous iron, oxyhydroxides 2003a,b). Lichenothelia spp. can oxidize manganese and iron
become mixed with fungal organic polymers (Barker and in metal-bearing minerals, such as siderite (FeCO3) and rho-
Banfield 1998), while biotite [K(Mg, Fe(II))3AlSi3O10(OH, dochrosite (MnCO3), and precipitate them as oxides (Grote
O,F)2] was penetrated by fungal hyphae along cleavages, and Krumbein 1992). Oxidation of Fe(II) and Mn(II) by fungi
partially converting it to vermiculite [(Mg, Fe(II),Al)3(Al, can lead to the formation of dark patinas on glass surfaces
Si)4O10(OH)2.4H2O] (Barker and Banfield 1996). The fungal (Eckhardt 1985). Another biogenic mineral (tepius) has been
partner has also been reported to be involved in formation identified in association with a lichen carpet occurring in high
of secondary silicates, such as opal (SiO2.nH2O) and forster- mountain ranges in Venezuela (Gorbushina et al. 2001).
ite (Mg2SiO4), in lichen thalli (Gorbushina et al. 2001). The
transformation rate of mica (general formula for minerals
of the mica group is XY2–3Z 4O10(OH, F)2  with X  =  K, Na, 9.5 FUNGAL SYMBIOSES IN GEOMYCOLOGY
Ba, Ca, Cs, (H3O), (NH4); Y  =  Al, Mg, Fe2+, Li, Cr, Mn,
V, Zn; and Z = Si, Al, Fe3+, Be, Ti) and chlorite [(Mg, Fe, Many fungi form partnerships with plants (mycorrhizas)
Li)6AlSi3O10(OH)8] to 2:1 expandable clays was pronounced and algae or cyanobacteria (lichens) that are significant geo-
in ectomycorrhizosphere soil. This was probably a result of active agents. In general terms, the mycobiont is provided
production of organic acids and direct extraction of K+ and with carbon by the photobionts, while the mycobiont may
Mg2+ by fungal hyphae (Arocena et al. 1999). Fungal–clay protect the symbiosis from harsh environmental conditions

(e.g., desiccation and metal toxicity) and provide increased siderophores, causing dissolution of Al silicates (Jongmans
access to inorganic nutrients such as phosphate and essential et al. 1997; van Breemen et al. 2000). Such excretions can
metals. also release elements from apatite and wood ash (K, Ca, Ti,
Mn, and Pb) (Wallander et al. 2003). Ericoid mycorrhizal
9.5.1 Lichens and ectomycorrhizal fungi can dissolve several cadmium,
copper, zinc, and lead-bearing minerals, including metal
Lichens are fungi that exist in facultative or obligate phosphates (Leyval and Joner 2001; Martino et  al. 2003;
symbioses with one or more photosynthesizing partners, Fomina et al. 2004, 2005b, 2006). Mobilization of phospho-
which occur in almost all surface terrestrial environments: rus from inorganic and organic phosphorus sources is gen-
an estimated 6%–8% of the earth’s land surface is dominated erally regarded as one of the most important functions of
by lichens (Haas and Purvis 2006). Lichens play important mycorrhizal fungi, and this can also result in redistribution
roles in retention and distribution of nutrient (e.g., C and N) of incorporated metals and the formation of other second-
and trace elements, in soil formation, and in rock bioweath- ary minerals, including other metal phosphates. The ericoid
ering (Banfield et al. 1999; Adamo and Violante 2000; Chen mycorrhiza Oidiodendron maius can solubilize zinc oxide
et al. 2000). Lichens can accumulate metals such as lead (Pb) and phosphate (Martino et al. 2003). Many ericoid mycor-
and copper (Cu) and many other elements, including radio- rhizal and ectomycorrhizal fungi are able to solubilize zinc,
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nuclides (Purvis and Pawlik-Skowronska 2008). They also cadmium, copper phosphates, and lead chlorophosphate
form a variety of metal-organic biominerals, for example, (pyromorphite), releasing phosphate and component metals
oxalates, especially during growth on metal-rich substrates (Fomina et  al. 2004, 2006). An association of arbuscular
(Chen et al. 2000; Adamo et al. 2002). On copper-sulfide- mycorrhizal fungi (AMF) with Lindenbergia philippen-
bearing rocks, precipitation of copper oxalate (moolooite) sis, sampled from a Zn-contaminated settling pond at a
can occur within lichen thalli (Purvis 1996; Purvis and zinc smelter, enhanced Zn accumulation in Zn-loaded rhi-
Halls 1996). zosphere sediment compared with treatments that sup-
pressed AMF colonization. A significant proportion of
9.5.2 Mycorrhizas Zn was present as crystalline and other solid materials
that were associated with the root mucilaginous sheath
The majority of terrestrial plants depend on symbiotic (Kangwankraiphaisan et  al. 2013). Such results may indi-
mycorrhizal fungi (Smith and Read 1997; Wang and Qui cate a role for AMF in enhancing Zn immobilization in the
2006). These include endomycorrhizas, where the fungus rhizosphere of plants that successfully colonize Zn mining
colonizes the interior of plant host root cells (e.g., ericoid and smelting disposal sites (Christie et  al. 2004; Turnau
and arbuscular mycorrhizas), and ectomycorrhizas, where et al. 2012; Kangwankraiphaisan et al. 2013).
the fungus is located outside the plant root. Mycorrhizal
fungi can mediate metal and phosphate solubilization, from
mineral sources, and extracellular precipitation of metal 9.6 ENVIRONMENTAL AND APPLIED
oxalates and immobilize metals within biomass (Lapeyrie SIGNIFICANCE OF GEOMYCOLOGY
et al. 1990, 1991; Blaudez et al. 2000; Christie et al. 2004;
Fomina et al. 2004, 2005b, 2006; Bellion et al. 2006; Finlay The kinds of processes detailed previously can impact
et al. 2009; McMaster 2012; Smits et al. 2012). Such activi- human society not only through their environmental signifi-
ties can lead to changes in the physico-chemical character- cance and biotechnological applications but also in deleterious
istics of the root environment and enhanced bioweathering contexts such as biodeterioration. Microbial biodeterioration
of soil minerals (McMaster 2012; Bonneville et  al. 2009, of metal due to microbial activity is termed biocorrosion or
2011). Furthermore, ectomycorrhizal mycelia may respond microbially influenced corrosion (MIC) (Beech and Sunner
to different soil silicate and phosphate minerals (e.g., apatite, 2004). While certain groups of bacteria are more commonly
quartz, and potassium feldspar) by regulating growth and associated with biocorrosion, various fungi may be present
metabolic activity (Rosling et al. 2004a,b). within biofilm communities on metal surfaces (Beech and
Mycorrhizal fungi often excrete low-molecular-weight Sunner 2004; Gu 2009). As mentioned earlier, certain fungi
carboxylic acids and siderophores (Martino et  al. 2003; may mediate transformation of metallic lead into pyromor-
Fomina et  al. 2004). Ectomycorrhizal fungi can produce phite (Rhee et al. 2012) and of depleted uranium into ura-
micro- to millimolar concentrations of organic acids nium phosphate minerals (Fomina et al. 2008).
such as oxalic, citric, succinic, formic, and malic acids in The importance of rock and mineral dissolution mech-
their soil microenvironments; this can result in enhanced anisms in bioweathering has been discussed earlier. In
weathering of hornblendes, feldspars, and granitic bed- a societal context, structural decay of stone and mineral
rock. Ectomycorrhizal fungi can also form narrow pores artifacts represents a loss of cultural heritage (Scheerer
in weatherable minerals in podzol E horizons, probably et  al. 2009; Cutler and Viles 2010). The most common
by exuding low-molecular-weight organic acids and/or stone types affected are marble, limestone, sandstone, and

granite. Materials used to stabilize building blocks (mortar) municipal solid waste incineration), contaminated soil,
and to coat surfaces before painting (plaster or stucco) are electronic scrap, and other waste materials by fungal activ-
also susceptible to biodeterioration (Scheerer et  al. 2009). ity (Brandl 2001; Brandl and Faramarzi 2006). Although
Microbial colonization of external stone surfaces generally the efficiency of fungal systems cannot be compared to
initiates with phototrophic cyanobacteria and algae, proba- that of bacterial bioleaching, they may be more suited to
bly followed by lichens, and then with general heterotrophs; specific bioreactor applications (Burgstaller and Schinner
however, establishment of heterotrophic rock communi- 1993). A variety of fungal mechanisms results in metal
ties is possible without initial involvement of phototroph immobilization. Biosorption is a physico-chemical process,
(Roeselers et al. 2007; Scheerer et al. 2009). Highly deterio- simply defined as “the removal of substances from solution
rated stone surfaces provide a ‘‘proto-soil’’ for colonization by biological material.” It is a property of both living and
by mosses, ferns, and higher plants (Cutler and Viles 2010). dead organisms (and their components) and is frequently
Mechanisms of stone deterioration are complex and include proposed as a promising biotechnology for removal (and/
most of the direct and indirect mechanisms, previously dis- or recovery) of metals, radionuclides, and other substances
cussed for mineral dissolution (Sand 1997; Scheerer et  al. (Gadd and Mowll 1985; Gadd 1986, 1990, 2001a,b, 2009a;
2009). Biofilm extracellular polymeric substances (EPS) are De Rome and Gadd 1987; Gadd and de Rome 1988; Gadd
also capable of metal complexation and weakening of min- and White 1989, 1990, 1992, 1993; Volesky 1990, 2007;
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eral lattices through wetting and drying cycles, as well as Garnham et  al. 1992; White et  al. 1995; Wang and Chen
the production of efflorescences, that is, secondary miner- 2006, 2009; Fomina and Gadd 2014). Modification of bio-
als produced through reaction of anions from excreted acids mass has been attempted to improve efficiency or selec-
with cations from the stone (Wright 2002). Physical damage tivity of microbial biosorbents (Fomina and Gadd 2002a,
may be caused by hyphal penetration of weakened areas of 2014). However, there has been little or no exploitation in
the stone (Hirsch et  al. 1995; Cockell and Herrera 2008). an industrial context, nor does this seem likely, largely due
Lichens cause damage due to penetration by their rhizines, to the greater selectivity and efficiency of commercial ion-
composed of fungal filaments, and expansion/contraction of exchange resins (Gadd 2009a). Urease-positive fungi can
the thallus on wetting or drying (Gaylarde and Morton 2002; be used to precipitate metal-containing carbonates, some in
De los Rios et al. 2004). “Lichen acids,” mainly oxalic acid, nanoscale dimensions, thus providing a means of metal bio-
cause damage at the stone/lichen interface, and lichen thalli recovery, as well as potentially useful nanoscale biomineral
may accumulate up to 50% calcium oxalate, depending on products (Li et al. 2014, 2015). Similarly, the formation of
the substrate (Lisci et al. 2003; Seaward 2003). In addition, other insoluble metal compounds by fungi or their metabo-
carbonic acid formed in the lichen thallus can solubilize cal- lites could also be considered as a means to biorecover met-
cium and magnesium carbonates in calcareous stone (Tiano als, metalloids, and radionuclides, for example, oxalates,
2002). Fungal biodeterioration of ancient ivory (natural oxides, oxalates, and phosphates, as well as the production
apatite; walrus tusk) was accompanied by widespread etching of elemental metal or metalloid forms at nanoscale and
and tunneling by hyphae and extensive formation of cal- above (Gadd 2010; Gadd et al. 2012).
cium oxalate monohydrate, whewellite (Pinzari et al. 2013). The ability of fungi and bacteria to transform metal-
Concrete and cement can be biodeteriorated, and in some loids has been successfully used for bioremediation of con-
environments, fungi dominate the concrete-deteriorating taminated land and water. Selenium methylation results in
microbiota (Gu et  al. 1998; Nica et  al. 2000; Gu 2009; volatilization, and this has been used to remove selenium
Scheerer et al. 2009; Cutler and Viles 2010). Microbial attack from the San Joaquin Valley and Kesterson Reservoir,
on concrete is mediated by protons, inorganic and organic California (Thomson-Eagle and Frankenberger 1992).
acids, and the production of hydrophilic slimes, leading to Mycorrhizal associations may have application in phy-
biochemical and biomechanical deterioration (Sand 1997; toremediation (Rosen et  al. 2005; Gohre and Paszkowski
Fomina et al. 2007c; Scheerer et al. 2009). Several species 2006), the use of plants to remove or detoxify environ-
of microfungi were able to colonize samples of the concrete mental pollutants (Salt et  al. 1998) by metal phytoex-
used as radioactive waste barrier in the Chernobyl reactor. traction or by acting as biological barriers (Leyval et  al.
They leached iron, aluminum, silicon, and calcium and 1997; Krupa and Kozdroj 2004; Adriaensen et  al. 2005).
reprecipitated silicon and calcium oxalate in their microen- Glomalin, an insoluble glycoprotein, is produced in
vironment (Fomina et al. 2007c). copious amounts on hyphae of arbuscular mycorrhizal
Mineral and metal solubilization mechanisms enable fungi and can sequester metals such as Cu, Cd, and Pb
metal removal from industrial wastes, low-grade ores, and (Gonzalez-Chavez et  al. 2004). Arbuscular mycorrhizal
metal-bearing minerals. This may have application in bio- fungi can also decrease U translocation from plant roots to
remediation, metal biorecovery, and recycling (Burgstaller shoot (Rufyikiri et al. 2004; Chen et al. 2005a,b). For eri-
and Schinner 1993; Gadd 2000a; Gadd and Sayer 2000; caceous mycorrhizas, the fungus prevents translocation of
Brandl 2001; Santhiya and Ting 2005; Kartal et al. 2006). Cu and Zn to host plant shoots (Bradley et al. 1981, 1982;
Metals can be solubilized from fly ash (originating from Smith and Read 1997). The development of stress-tolerant

plant–mycorrhizal associations may be a promising strat- 9.7 CONCLUSIONS

egy for phytoremediation and soil amelioration (Perotto
et  al. 2002; Schutzendubel and Polle 2002; Cairney and Roles of fungi have often received scant attention in
Meharg 2003; Martino et al. 2003). geomicrobiological contexts, but they are of clear importance
Some of the geomycological processes detailed previ- in several key areas. These include a plethora of organic and
ously may have consequences for various abiotic soil treat- inorganic transformations that are important in nutrient and
ment processes, notably the immobilization of toxic metals element cycling, rock and mineral bioweathering, mycogenic
by phosphate formation. Apatite [Ca 5(PO4)3(F, Cl, OH)], biomineral formation, and metal–fungal interactions. Fungi
pyromorphite [Pb5(PO4)3Cl], mimetite [Pb5(AsO4)3Cl], and have mutualistic relationships with phototrophs, lichens (algae
vanadinite [Pb5(VO4)3Cl] are the most common prototypes and cyanobacteria) and mycorrhizas (plants), and are therefore
of the apatite mineral family. Such minerals hold prom- of special significance as geoactive agents. Transformations
ise for stabilization and recycling of industrial and nuclear of metals and minerals are central to many geomicrobial pro-
waste and have been explored for treatment of lead- cesses, and fungi can effect changes in metal speciation, tox-
contaminated soils and waters (Ruby et  al. 1994; Cotter- icity and mobility, as well as mediate mineral formation or
Howells 1996; Cotter-Howells and Caporn 1996; Ioannidis dissolution. Such mechanisms are important components of
and Zouboulis 2003; Manning 2008; Oelkers and Montel natural biogeochemical cycles for metals and associated ele-
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2008; Oelkers and Valsami-Jones 2008). The stability of ments in biomass, soil, rocks and minerals, for example S and
these minerals is therefore of interest in any soil reme- P, as well as for metalloids, actinides, and metal radionuclides.
diation strategy to reduce the effects of potentially toxic It is within the terrestrial environment where fungi have the
elements, such as Pb, V, and As. For example, pyromor- greatest geochemical influence, especially when considering
phite is a highly insoluble lead phosphate mineral under soil, rock, mineral and plant surfaces, and the plant root–soil
a wide range of geochemical conditions and has often interface. However, they are also important in aquatic habitats
been suggested as a means to reduce the Pb bioavailability. and are now recognized as significant components of aquatic
However, solubilization of pyromorphite and formation sediments. Apart from being important in natural biosphere
of lead oxalate by several free-living and symbiotic fungi processes, geomycological processes can have beneficial or
demonstrate that pyromorphite may not be as effective detrimental consequences in a human context. Beneficial
in immobilizing lead as some previous studies have sug- applications in environmental biotechnology include metal
gested (Sayer et  al. 1999; Fomina et  al. 2004). Similarly, and radionuclide bioleaching, biorecovery, detoxification, and
despite the insolubility of vanadinite, fungi exerted both bioremediation; they also have applications in the production
biochemical and biophysical effects on the mineral, includ- or deposition of biominerals or metallic elements with cata-
ing etching, penetration, and the formation of new biomin- lytic or other properties in nanoparticle, crystalline, or colloi-
erals (Ceci et al. 2015a). Lead oxalate was precipitated by dal forms. These may be relevant to the development of novel
Aspergillus niger during the bioleaching of vanadinite and biomaterials for technological and antimicrobial purposes.
mimetite, and this suggests a general fungal mechanism Adverse effects include spoilage and destruction of natu-
for the transformation of lead-containing apatite group ral and synthetic materials; rock and mineral-based building
minerals (e.g., vanadinite, pyromorphite, and mimetite) materials (e.g., concrete); biocorrosion of metals, alloys, and
(Ceci et al. 2015a,b). This pattern of fungal bioweathering related substances; and adverse effects on radionuclide specia-
of lead apatites could be extended to other metal apatites, tion, mobility, and containment. The ubiquity and importance
such as calcium apatite [Ca 5(PO4)3(OH, F, Cl)]. Here, the of fungi in biosphere processes underline the importance of
formation of monohydrated (whewellite) and dihydrated geomycology as a conceptual framework encompassing the
(weddellite) calcium oxalate can be accomplished by many environmental activities of fungi, their impact, and their
different fungal species (Burford et  al. 2006; Guggiari applied significance.
et al. 2011; Pinzari et al. 2013; Gadd et al. 2014). The abil-
ity of free-living and mycorrhizal fungi to transform toxic
metal-containing minerals should therefore be taken into 9.8 ACKNOWLEDGMENTS
account in risk assessments of the long-term environmen-
tal consequences of in situ chemical remediation tech- The author gratefully acknowledges research support from
niques, revegetation strategies, or natural attenuation of the Natural Environment Research Council, the Biotechnology
contaminated sites. The bioweathering potential of fungi and Biological Sciences Research Council, the Royal Societies
has been suggested as a possible means for the bioremedia- of London and Edinburgh, CCLRC Daresbury SRS, British
tion of asbestos-rich soils. Several fungi could extract iron Nuclear Fuels plc, the National Nuclear Laboratory, and the
from asbestos mineral fibres (e.g., 7.3% from crocidolite Nuclear Decommissioning Agency. The author also acknowl-
and 33.6% from chrysotile by a Verticillium sp.), thereby edges an award under the Chinese Government’s 1000 Talents
removing the reactive iron ions responsible for DNA dam- Plan with the Xinjiang Institute of Ecology and Geography,
age (Daghino et al. 2006). Chinese Academy of Sciences, Urumqi, China.

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