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Fungal involvement in bioweathering and biotransformation of rocks and minerals
Abstract
Abstract In the Earth’s lithosphere, fungi are of fundamental importance as decomposer organisms, animal and plant pathogens and symbionts (e.g. lichens and mycorrhizas), being ubiquitous in sub-aerial and subsoil environments. The ability of fungi to interact with minerals, metals, metalloids and organic compounds through biomechanical and biochemical processes, makes them ideally suited as biological weathering agents of rock and building stone. They also play a fundamental role in biogeochemical cycling of nutrients, (e.g. C, N, P and S) and metals (e.g. Na, Mg, Ca, Mn, Fe, Cu, Zn, Co and Ni) essential for the growth of living organisms in the biosphere. In addition they play an integral role in the mobilization and immobilization of non-essential metals (e.g. Cs, Al, Cd, Hg and Pb). Most studies on mineral-microbe interactions and microbial involvement in geological processes have concentrated on bacteria and archaea (Prokaryota): fungi (Eukaryota) have, to a certain extent, been neglected. This article addresses the role of fungi in geomicrobiological processes, emphasizing their deteriorative potential on rock, building stone and mineral surfaces and involvement in the formation of secondary mycogenic minerals. Such roles of fungi are also of importance for the global carbon reservoir and have potential biotechnological applications, e.g. in the bioremediation of xenobiotic-, metal- and/or radionuclide-contaminated soils and wastes, and metal/radionuclide recovery.
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“Several studies have demonstrated enhanced dissolution of serpentine and olivine by microbes mainly through the production of organic acids (e.g., [56][57][58]).”
From Strategizing carbon-neutral mines: A case for pilot projects (2014) · cites this paper as [58]
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Filipiak, M. (2018) · Zoological monographs · doi:10.1007/978-3-319-75937-1_13 · Cited by 52
“Rocks can be weathered by fungi and are sources of specific atoms used to build fungal mycelia, and these atoms are further translocated within the ecosystem (Burford et al. 2003; Gadd 2007, 2017a; Gadd et al. 2012; Li et al. 2016).”
BackgroundZinc Phosphate Transformations by the Paxillus involutus/Pine Ectomycorrhizal Association
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“…acidification around the growing hyphae due to release of respired CO2, proton efflux, the presence of acidic extracellular polymeric substances (EPS, Fig 2b), release of low molecular weight organic acids (LMWOAs) and precipitation of biominerals (Fig 3a) (Burford et al., 2003; Gadd, 1999, 2007).”
BackgroundPhylogenetic diversity of culturable fungi in the Heshang Cave, central China
Man, B., Wang, H., Xiang, X., Wang, R., Yun, Y., & Gong, L. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.01158 · Cited by 49
“They are ubiquitous pioneer dwellers on surfaces of rocks (Staley et al., 1982; Sterflinger, 2000; Gorbushina et al., 2001; Etienne and Dupont, 2002) and in extremely adverse and nutrient-deprived environments including caves (Burford et al., 2003a).”
BackgroundInfluentialEndolithic Microbial Communities in Polar Desert Habitats
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“…as well as buildings and monuments by endolithic microorganisms (Danin et al. 1983; Weed and Ackert 1986; Wessels and Schoeman 1988; Palmer and Hirsch 1991; Hirsch et al. 1995; Ortega-Calvo et al. 1995; Ascaso et al. 1998; Burford et al. 2003; Gaylarde and Gaylarde 2004; Omelon et al. 2008).”
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“Fungi have the ability to degrade mineral substrates through biomechanical and biochemical processes (e.g., Burgstaller and Schinner, 1993; Banfield et al., 1999; Burford et al., 2003; Fomina et al., 2005; Bonneville et al., 2009).”
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Fungi and Their Role in the Biosphere
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“…environmental scanning electron microscopy (ESEM), proved to be useful for the surface visualization of fungi in association with minerals (e.g., Burford et al. 2003a, 2003b; Rosling et al. 2007; Smits 2009; Fomina et al. 2010) providing spatial information at the micrometer-to sub-micrometer…”
BackgroundInfluentialA coupled microscopy approach to assess the nano-landscape of weathering
Lybrand, R. A., Austin, J. C., Fedenko, J., Gallery, R. E., Rooney, E. C., Schroeder, P. A., Zaharescu, D. G., & Qafoku, O. S. (2019) · Scientific Reports · doi:10.1038/s41598-019-41357-0 · Cited by 42
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Lichens as Agents of Biodeterioration
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“Many fungi, including A. niger, are well known for lowering the pH of their surrounding environment (Burford et al., 2003; Fomina et al., 2005; Boswell et al., 2007; Gadd et al., 2012), and acidolysis was the prime mechanism for toxic metal mineral solubilization by various Data are given as means…”
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“Fungi have the potential to interact with many different substrates including minerals and, hence, can play a key role in biological weathering of rocks and minerals (Burford et al., 2003).”
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Gonçalves, V. N., de Oliveira, F. S., de Carvalho, C. R., Schaefer, C. E. G. R., Rosa, C. A., & Rosa, L. H. (2017) · Extremophiles · doi:10.1007/s00792-017-0947-x · Cited by 39
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“The role of fungi in the weathering and biomineralization of rocks and minerals is well documented (Burford et al. 2003; Burford et al. 2006; Chen et al. 2000; Gadd 2007).”
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“This can result in the formation of secondary biogenic minerals, for example, calcium oxalate (Burford et al. 2003; Fomina et al. 2010; Gadd 2017b; Gadd et al. 2014).”
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The roles of endolithic fungi in bioerosion and disease in marine ecosystems. I. General concepts
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“Fungi are directly involved in the biogeochemical transformation of elements on a global scale by excreting organic acids [63,64].”
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“Researchers have speculated that rock varnish genesis may be a result of biological processes in which bacteria and fungi facilitate the accumulation and transformation of minerals (TaylorGeorge et al. 1983; Golden et al. 1992; Burford et al. 2003; Gadd 2007, Wang et al. 2011).”
BackgroundFungal communities on speleothem surfaces in Kartchner Caverns, Arizona, USA
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“Metabolic products such as H+, various organic acids and CO2 can chemically attack minerals (Burford et al., 2003).”
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“…of the so-called “heterotrophic leaching” by employing several mechanisms, including protonation (acidolysis), chelation (complexolysis) and metal accumulation, where the biomass functions as a metal sink (Burford et al. 2003; Fomina et al. 2004; Kraemer 2004; Adeyemi and Gadd 2005; Gadd 2007).”
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“These solubilization processes are important in terrestrial environment for the release of metal elements (e.g., Na, Mg, Ca, Mn, Fe, Cu, Zn, Co and Ni) and some associated anionic nutrients (e.g., C, N, P and S) into biogeochemical cycles (Burford et al. 2003).”
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“Secreted oxalate may promote brown rot by weathering soil minerals (2), mobilizing Fe(3) (3, 11), and detoxifying metals (21).”
BackgroundNoack-Schönmann, S., Spagin, O., Gründer, K.-P., Breithaupt, M., Günter, A., Muschik, B., & Gorbushina, A. A. (2013) · International Biodeterioration & Biodegradation · doi:10.1016/j.ibiod.2013.09.020 · Cited by 28
A systematic review of sustainable gold extraction from raw ores using alternative leaching reagents
Sousa, R., Regufe, M. J., Fiúza, A., Leite, M. M., & Futuro, A. (2021) · The Extractive Industries and Society · doi:10.1016/j.exis.2021.101018 · Cited by 27
Interaction of U(VI) with Schizophyllum commune studied by microscopic and spectroscopic methods
Günther, A., Raff, J., Merroun, M. L., Roßberg, A., Kothe, E., & Bernhard, G. (2014) · BioMetals · doi:10.1007/s10534-014-9772-1 · Cited by 27
“The ability of several fungi to release metals from minerals and other metal compounds and to take them up into the cell and to form secondary minerals like phosphates e.g. (e.g. Burford et al. 2003; Fomina et al. 2005, 2007a, b; Gadd 2007) is well known.”
Fungal Iron Biomineralization in Río Tinto
Oggerin, M., Tornos, F., Rodríguez, N., Pascual, L., & Amils, R. (2016) · Minerals · doi:10.3390/min6020037 · Cited by 27
“All major microbial groups are capable of immobilizing metal ions and carrying out mineralization processes through organic and inorganic precipitation of secondary associated minerals as well as depositing crystalline material on and within cell walls [31,34,35].”
Background6.36 Solutional Weathering and Karstic Landscapes on Quartz Sandstones and Quartzite
Wray, R. A. L. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-374739-6.00140-8 · Cited by 26
Understanding Microbially Active Biogeochemical Environments
Gleeson, D. B., McDermott, F. P., & Clipson, N. (2007) · Advances in applied microbiology · doi:10.1016/s0065-2164(07)62004-8 · Cited by 26
Microbes on carbonate rocks and pedogenesis in karst regions
Lian, B., Chen, Y., & Tang, Y. (2010) · Journal of Earth Science · doi:10.1007/s12583-010-0240-8 · Cited by 26
Tolerance of Chemoorganotrophic Bioleaching Microorganisms to Heavy Metal and Alkaline Stresses
Monballiu, A., Cardon, N., Nguyen, M. T., Cornelly, C., Meesschaert, B. D., & Chiang, Y. W. (2015) · Bioinorganic Chemistry and Applications · doi:10.1155/2015/861874 · Cited by 23
“These microorganisms are associated with silica-richminerals in nature, compounds commonly found in alkaline industrial residues, but in their natural environment they are not exposed to, and thus do not become adapted to, high levels of mobile heavy metals and metalloids [24, 25].”
BackgroundChemoorganotrophic Bioleaching of Olivine for Nickel Recovery
Chiang, Y. W., Santos, R. M., Audenaerde, A. V., Monballiu, A., Gerven, T. V., & Meesschaert, B. D. (2014) · Minerals · doi:10.3390/min4020553 · Cited by 25
“preferentially chelated by the biogenic substances, and or (ii) some elements, for example magnesium, may re-precipitate in the form of inorganic or organic compounds such as (hydr)oxides, carbonates and oxalates [3].”
InfluentialWiktor, V., Grosseau, P., Guyonnet, R., Garcia-Diaz, É., & Lors, C. (2010) · Materials and Structures · doi:10.1617/s11527-010-9653-1 · Cited by 25
“The development of cracks, fissures and weathering rinds in rocks accelerates biological weathering by providing a niche that can easily be exploited by opportunistic micro-organisms [5].”
BackgroundMasaphy, S., Zabari, L., Pastrana, J., & Dultz, S. (2009) · Geomicrobiology Journal · doi:10.1080/01490450903060798 · Cited by 25
“…induced by fungal activity, although fungi are found in lime and calcareous soil (Burford et al. 2003a, 2006), and fungal filaments that mineralized with calcite together with whewellite have been reported in limestone and calcareous soils (Burford et al. 2003b; Kahle 1977; Verrecchia 2000).”
BackgroundToxic Metals and Fungal Communities
Fomina, M., Burford, E. P., & Gadd, G. M. (2005) · CRC Press eBooks · doi:10.1201/9781420027891-46 · Cited by 25
Mycorrhizal Studies in Temperate Rainforests of Southern Chile
Godoy, R., & Marín, C. (2019) · Fungal biology · doi:10.1007/978-3-030-15228-4_16 · Cited by 24
Nir, I., Barak, H., Kramarsky‐Winter, E., Kushmaro, A., & Rı́os, A. D. L. (2021) · Environmental Microbiology · doi:10.1111/1462-2920.15635 · Cited by 24
“Indeed it has been previously reported that biodegradation of calcareous rocks is enhanced by microbial colonization (Ban fi eld et al ., 1999; Ster fl inger, 2000; Burford et al ., 2003; De los Ríos et al ., 2004; De los Ríos et al ., 2009).”
BackgroundMicrobial Community Diversity of Moonmilk Deposits at Ballynamintra Cave, Co. Waterford, Ireland
Rooney, D. C., Hutchens, E., Clipson, N., Baldini, J. U. L., & McDermott, F. P. (2010) · Microbial Ecology · doi:10.1007/s00248-010-9693-7 · Cited by 24
“Fungi play major roles in the transformation of organic and inorganic substrates [17] and also participate in mineral dissolution and secondary mineral formation [ 8 ].”
BackgroundBiological Weathering in the Terrestrial System
Zaharescu, D. G., Burghelea, C. I., Dontsova, K. M., Reinhard, C. T., Chorover, J., & Lybrand, R. A. (2020) · Geophysical monograph · doi:10.1002/9781119413332.ch1 · Cited by 26
Mechanisms of olivine dissolution by rock-inhabiting fungi explored using magnesium stable isotopes
Pokharel, R., Gerrits, R., Schuessler, J. A., & von Blanckenburg, F. (2019) · Chemical Geology · doi:10.1016/j.chemgeo.2019.07.001 · Cited by 23
Molecular Characterization of Fungal Communities in Sandstone
Gleeson, D. B., Melville, K., McDermott, F. P., CLIPSON, N. J. W., & Gadd, G. M. (2010) · Geomicrobiology Journal · doi:10.1080/01490451003702982 · Cited by 23
“Fungal involvement in bioweathering of rocks and minerals is well documented (Sterflinger 2000; Burford et al. 2003; Adeyemi and Gadd 2005; Fomina et al. 2005; Fomina et al. 2007; Gadd 2007, 2010; Gorbushina et al. 2008) although the majority of research focuses on fungal communities found in…”
BackgroundMethodResultInfluentialSiderophores of Symbiotic Fungi
Haselwandter, K., & Winkelmann, G. (2007) · Springer eBooks · doi:10.1007/978-3-540-71160-5_4 · Cited by 24
“The ability of fungi to interact with a great variety of different substrates including minerals, metals and organic compounds in biophysical and biochemical processes makes them ideally suited as biological weathering agents of rock and minerals ( Burford et al. 2003 ).”
BackgroundMajor element residence times in humus from a beech forest: The role of element forms and recycling
Dincher, M., Calvaruso, C., & Turpault, M. (2019) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2019.107674 · Cited by 22
Lichens Bite the Dust – A Bioweathering Scenario in the Atacama Desert
Jung, P., Baumann, K., Emrich, D., Springer, A., Felde, V. J. M. N. L., Dultz, S., Baum, C., Frank, M., Büdel, B., & Leinweber, P. (2020) · iScience · doi:10.1016/j.isci.2020.101647 · Cited by 22
Ward, M., Kapitulčinová, D., Brown, A., Heard, P. J., Cherns, D., Cockell, C. S., Hallam, K., & Ragnarsdottir, K. V. (2013) · Micron · doi:10.1016/j.micron.2012.12.006 · Cited by 22
Ogórek, R., Pusz, W., Lejman, A., & Uklanska-Pusz, C. M. (2014) · Journal of Cave and Karst Studies · doi:10.4311/2013mb0123 · Cited by 22
“According to other authors, the most abundant fungal taxa isolated from rocks, especially from granite, were from the family Mucorales, and the genera Penicillium, Phoma, Auerobasidium, and Trichoderma (Hirsch et al., 1995; Burford et al., 2003 a,b; Brunner et al., 2011).”
BackgroundWilson, M. J., Certini, G., Campbell, C. D., Anderson, I. C., & Hillier, S. (2008) · Die Naturwissenschaften · doi:10.1007/s00114-008-0394-8 · Cited by 22
“Fungi appear to be a particularly efficient group in promoting “bioweathering” of primary minerals and the biosynthesis of new minerals (Burford et al. 2003; Gadd 2007).”
BackgroundInfluentialAdvancements in improving gold recovery from refractory gold ores/concentrates: a review
Barbouchi, A., Louarrat, M., Mikali, M., Barfoud, L., Alaoui-Chrifi, M. A. E., Faqir, H., Benzakour, I., Idouhli, R., Khadiri, M.-E., & Benzakour, J. (2024) · Canadian Metallurgical Quarterly · doi:10.1080/00084433.2024.2441548 · Cited by 21
“This treatment aims to oxidise the mineral sulphide by acid-ophilic bacteria and to deactivate the carboneous matter (Figure 3), promoting the liberation of gold [48 – 58].”
Bio-oxidation of Gold from Refractory Sulfide Ores: A Journey Ahead
Darvanjooghi, M. H. K., Magdouli, S., Brar, S. K., Abdollahi, H., & Zolfaghari, M. (2021) · Geomicrobiology Journal · doi:10.1080/01490451.2021.1977431 · Cited by 21
“Furthermore, these microorganisms may produce ferric iron-complexing agents that directly increase the promote rock weathering (Brehm et al. 2005; Burford et al. 2003).”
BackgroundRoutes of phlogopite weathering by three fungal strains
Pinzari, F., Cuadros, J., Napoli, R., Canfora, L., & Bardají, D. B. (2016) · Fungal Biology · doi:10.1016/j.funbio.2016.08.007 · Cited by 21
“…(Boyle & Voigt, 73 1973; Leyval & Berthelin, 1991; Paris et al., 1995, 1996; Jongmans et al., 1997; Wallander & 74 Wickman, 1999; Crawford et al., 2000; Blum et al., 2002; Burford et al., 2003a; Yuan et al., 75 2004; Rosling et al., 2004a; Balogh-Brunstad et al., 2008a, 2008b; Arocena et al. 2012).”
BackgroundWu, Y., Zhang, J., Guo, X., Wang, Y., & Wang, Q. (2017) · European Journal of Soil Biology · doi:10.1016/j.ejsobi.2017.06.011 · Cited by 21
Humusica 2, article 13: Para humus systems and forms
Zanella, A., Ponge, J., Fritz, I., Pietrasiak, N., Matteodo, M., Nadporozhskaya, M., Juilleret, J., Tatti, D., Bayon, R. L., Rothschild, L. J., et al. (2017) · Applied Soil Ecology · doi:10.1016/j.apsoil.2017.09.043 · Cited by 21
“Fungi, bacteria and algae colonize and deteriorate even other structural materials like concrete, plastic and metal (Burford et al., 2003).”
BackgroundGałązka, A., Marzec-Grządziel, A., Grządziel, J., Varsadiya, M., & Pawlik, Ł. (2022) · Ecological Indicators · doi:10.1016/j.ecolind.2022.109136 · Cited by 20
Kirtzel, J., Siegel, D. R. N., Krause, K., & Kothe, E. (2017) · Advances in applied microbiology · doi:10.1016/bs.aambs.2017.01.002 · Cited by 20
Arocena, J. M., Siddique, T., Thring, R. W., & Kapur, S. (2007) · CATENA · doi:10.1016/j.catena.2006.11.006 · Cited by 20
“In addition, lichens exert mechanical pressure and break the minerals during thalli growth (Burford et al., 2003; Carter and Viles, 2004).”
BackgroundThe isotopic biosignatures of photo‐ vs. thiotrophic bivalves: are they preserved in fossil shells?
Dreier, A., Loh, W. K. W., Blumenberg, M., Thiel, V., Hause-Reitner, D., & Hoppert, M. (2014) · Geobiology · doi:10.1111/gbi.12093 · Cited by 19
“Endolithic micro-organisms boring in carbonates shells and substrates are widespread in marine environments; fungi, microalgae, and cyanobacteria have been described to date (Golubic, 1969; Burford et al., 2003; Hoppert et al., 2004).”
BackgroundLi, Z., Xu, J., Teng, H. H., Liu, L., Chen, J., Chen, Y., Zhao, L., & Ji, J. (2013) · Geomicrobiology Journal · doi:10.1080/01490451.2013.835888 · Cited by 19
“Meanwhile, fungi and fungal symbionts have also been recognized for their enhancing roles in rock weathering and mineral dissolution (Banfield et al. 1999; Burford et al. 2003a, 2003b; Favero-Longo et al. 2007; Gadd and Raven 2010).”
BackgroundSierra-Fernández, A., la Rosa‐García, S. D., Macías, R. Y., Guerrero‐Sánchez, C., Gomez-Villalba, L. S., Gómez‐Cornelio, S., Rabanal, M. E., Schubert, U. S., González, R. F., & Quintana, P. (2018) · Journal of Sol-Gel Science and Technology · doi:10.1007/s10971-018-4890-9 · Cited by 19
Šebesta, M., Nemček, L., Urík, M., Kolenčík, M., Bujdoš, M., Hagarová, I., & Matúš, P. (2020) · Agronomy · doi:10.3390/agronomy10111833 · Cited by 19
“Soil microorganisms also partially contribute to this process [25] via complexolysis by excreting extracellular biogenic chelating metabolites.”
BackgroundMeteoric lithification of catastrophic rockslide deposits: Diagenesis and significance
Sanders, D., Ostermann, M., Brandner, R., & Prager, C. (2009) · Sedimentary Geology · doi:10.1016/j.sedgeo.2009.11.007 · Cited by 19
“Because we did not observe rhizocretions in our samples, we prefer to interpret these alveolar structures as a result of fungal and/ or lichen-induced calcification (cf. Wright, 1989; Burford et al., 2003).”
BackgroundThe role of microorganisms and biofilms in the breakdown and dissolution of quartz and glass
Brehm, U., Gorbushina, A. A., & Mottershead, D. N. (2005) · Elsevier eBooks · doi:10.1016/b978-0-444-52019-7.50011-5 · Cited by 19
Gadd, G. M. (2011) · Encyclopedia of earth sciences series/Encyclopedia of earth sciences · doi:10.1007/978-1-4020-9212-1_102 · Cited by 19
Endolithic Microorganisms and Their Habitats
Omelon, C. R. (2016) · Advances in environmental microbiology · doi:10.1007/978-3-319-28071-4_4 · Cited by 19
Metadata
- Authors
- Burford, E. P., Fomina, M., & Gadd, G. M.
- Affiliations
- University of Dundee (GB)
- Venue
- Mineralogical Magazine
- Publisher
- Mineralogical Society
- Published
- 2003-12
- Volume
- 67
- Issue
- 6
- Pages
- 1127-1155
- ISSN
- 0026-461X (ISSN-L)
- 1471-8022
- OpenAlex
- W2106222412
- Cited by
- 392
- References
- 236
- Citations by year
- 2026: 15 · 2025: 12 · 2024: 12 · 2023: 12 · 2022: 20 · 2021: 21 · 2020: 26 · 2019: 21 · 2018: 14 · 2017: 24 · 2016: 14 · 2015: 13 · 2014: 30 · 2013: 27 · 2012: 17
- FWCI
- 19.39
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Mineralogical Magazine (publishedVersion)
- Discovery Research Portal (University of Dundee) (submittedVersion)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Earth-Surface Processes › Building materials and conservation
- Physical Sciences › Materials Science › Metals and Alloys › Metal Extraction and Bioleaching
- Physical Sciences › Earth and Planetary Sciences › Geochemistry and Petrology › Geochemistry and Elemental Analysis
- Keywords
- fungi, bioweathering, biotransformation, rock weathering, building stone deterioration, mineral-microbe interactions, metal mobilization, metal immobilization, biogeochemical cycles, bioremediation, radionuclide recovery, metal recovery, geomicrobiology
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