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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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“Microorganisms induce chemical weathering of rocks and leaching of its minerals by the excretion of organic acids and other metabolites; even CO2 produced during metabolism can lead to carbonic acid attack on mineral surfaces [5, 10, 36].”
BackgroundMa, W., Wu, F., Tian, T., He, D., Zhang, Q., Gu, J., Duan, Y., Ma, D., Wang, W., & Feng, H. (2020) · International Biodeterioration & Biodegradation · doi:10.1016/j.ibiod.2020.104972 · Cited by 83
Gonçalves, V. N., Cantrell, C. L., Wedge, D. E., Ferreira, M. C., Soares, M. A., Jacob, M. R., de Oliveira, F. S., Galante, D., Rodrigues, F., Alves, T. M. D. A., et al. (2015) · Environmental Microbiology · doi:10.1111/1462-2920.13005 · Cited by 82
Heavy Metal Pollutants: Environmental and Biotechnological Aspects
Gadd, G. M. (2009) · Elsevier eBooks · doi:10.1016/b978-012373944-5.00149-8 · Cited by 80
Fungal strategies for dealing with environment- and agriculture-induced stresses
Rangel, D. E. N., Finlay, R. D., Hallsworth, J. E., Dadachova, E., & Gadd, G. M. (2018) · Fungal Biology · doi:10.1016/j.funbio.2018.02.002 · Cited by 78
Ceci, A., Pinzari, F., Russo, F., Maggi, O., & Persiani, A. M. (2017) · AMBIO · doi:10.1007/s13280-017-0972-0 · Cited by 77
“According to Burford et al. (2003) fungi solubilise minerals, including phosphate rocks, with active secretion of organic acids, proton efflux out the plasma membrane, formation of carbonic acid in the media as a result of respiratory CO2 production.”
BackgroundMethodInfluentialWei, Z., Hillier, S., & Gadd, G. M. (2012) · Environmental Microbiology · doi:10.1111/j.1462-2920.2012.02776.x · Cited by 76
Experimental observations on fungal diagenesis of carbonate substrates
Kolo, K., Keppens, E., Préat, A., & Claeys, P. (2007) · Journal of Geophysical Research Atmospheres · doi:10.1029/2006jg000203 · Cited by 75
“…hyphae growth produces mechanical pressure that may dislodge matrix grains and cause substrate disintegration [Chen et al., 2000; Sterflinger, 2000; Warscheid and Braams, 2000; Burford et al., 2003b; Hoffland et al., 2004], thus increasing the surface area exposed to fungal G01007 KOLO ET AL.”
BackgroundInfluentialComparison of a bio-based corrosion inhibitor versus benzotriazole on corroded copper surfaces
Albini, M., Letardi, P., Mathys, L., Brambilla, L., Schröter, J., Junier, P., & Joseph, É. (2018) · Corrosion Science · doi:10.1016/j.corsci.2018.08.020 · Cited by 75
Vítek, P., Cámara, B., Edwards, H. G. M., Jehlička, J., Ascaso, C., & Wierzchoś, J. (2013) · Geomicrobiology Journal · doi:10.1080/01490451.2012.697976 · Cited by 74
“It is well known that fungi, including lichen mycobionts, may be responsible for the formation of hydrated calcium oxalates through the excretion of oxalic acid into the surrounding environment (Burford et al. 2003; Souza-Egipsy et al. 2002).”
BackgroundPhosphate Minerals, Environmental Pollution and Sustainable Agriculture
Manning, D. A. C. (2008) · Elements · doi:10.2113/gselements.4.2.105 · Cited by 74
Gadd, G. M., & Fomina, M. (2011) · Geomicrobiology Journal · doi:10.1080/01490451.2010.508019 · Cited by 73
“…immobilization can result from metabolismindependent and -dependent processes, as well as by organic and inorganic metal precipitation as secondary mineral phases (Morley and Gadd 1995; Burford et al. 2003; Fomina et al. 2005, 2006, 2007, 2008a; Gadd 2004, 2007, 2009, 2010; Gadd and Raven 2010).”
BackgroundLi, X. S., Sato, T., 大岩, 祐., Kusumi, A., Gu, J., & Katayama, Y. (2010) · Microbial Ecology · doi:10.1007/s00248-010-9699-1 · Cited by 73
“Many studies have been conducted on the deterioration of stone by fungi concerning invasion of mycelia, deposition of and excretion of organic acids [7, 10, 11, 38].”
BackgroundMicrobial Interactions in Soil Formation and Nutrient Cycling
Ravi, R., Anusuya, S., Balachandar, M., & Muthukumar, T. (2019) · Mycorrhizosphere and Pedogenesis · doi:10.1007/978-981-13-6480-8_21 · Cited by 46
Effects of oxalic and citric acids on three clay minerals after incubation
Kong, M., Huang, L., Li, L., Zhang, Z., Zheng, S., & Wang, M. K. (2014) · Applied Clay Science · doi:10.1016/j.clay.2014.06.035 · Cited by 70
Microorganisms in Toxic Metal-Polluted Soils
Gadd, G. M. (2005) · Soil biology · doi:10.1007/3-540-26609-7_16 · Cited by 69
Pinzari, F., Zotti, M., MICO, A. D., & Calvini, P. (2010) · International Biodeterioration & Biodegradation · doi:10.1016/j.ibiod.2010.06.001 · Cited by 67
Oggerin, M., Tornos, F., Rodríguez, N., del Moral, C., Sánchez‐Román, M., & Amils, R. (2013) · Environmental Microbiology · doi:10.1111/1462-2920.12094 · Cited by 67
Phosphorous availability influences the dissolution of apatite by soil fungi
Rosling, A., Suttle, K. B., Johansson, E. M. V., van Hees, P. A. W., & Banfield, J. F. (2007) · Geobiology · doi:10.1111/j.1472-4669.2007.00107.x · Cited by 66
“The biogeochemical significance of organic acid production in fungi has been extensively studied with respect to both bioremediation of toxic metals (Gadd, 1999) and mineral weathering above and below ground (Burford et al ., 2003).”
BackgroundX‐ray absorption spectroscopy (XAS) of toxic metal mineral transformations by fungi
Fomina, M., Charnock, J., Bowen, A. D., & Gadd, G. M. (2006) · Environmental Microbiology · doi:10.1111/j.1462-2920.2006.01139.x · Cited by 65
Nutrient Cycling: Potassium Solubilization by Microorganisms and Improvement of Crop Growth
Sindhu, S. S., Parmar, P., & Phour, M. (2013) · Soil biology · doi:10.1007/978-3-642-41837-2_10 · Cited by 62
“Bioweathering is a common geochemical process involved in erosion, decay, and decomposition of rocks and minerals mediated by living organisms (Barker et al. 1997; Burford et al. 2003).”
BackgroundFungi: A Neglected Candidate for the Application of Self-Healing Concrete
Jin, C., Yu, R., & Shui, Z. (2018) · Frontiers in Built Environment · doi:10.3389/fbuil.2018.00062 · Cited by 60
Fungal Deterioration of Barrier Concrete used in Nuclear Waste Disposal
Fomina, M., Podgorsky, V. S., Olishevska, S. V., Kadoshnikov, V., Pisanska, I. R., Hillier, S., & Gadd, G. M. (2007) · Geomicrobiology Journal · doi:10.1080/01490450701672240 · Cited by 60
“1993 ; Sterflinger 2000 ; Verrecchia 2000 ; Burford et al.”
BackgroundInfluentialDupont, J., Jacquet, C., Dennetière, B., Lacoste, S., Bousta, F., Orial, G., Cruaud, C., Couloux, A., & Roquebert, M. (2007) · Mycologia · doi:10.1080/15572536.2007.11832546 · Cited by 60
“Fungi cause weathering and biotransformation of rocks and minerals in subaerial or subsoil environments through biomechanical and biochemical processes (Budford et al 2003a, b).”
BackgroundIn vitro biodegradation potential of airborne Aspergilli and Penicillia
Savković, Ž. D., Stupar, M., Unković, N., Ivanović, Ž. S., Blagojević, J. D., Vukojević, J. B., & Grbić, M. L. (2019) · Die Naturwissenschaften · doi:10.1007/s00114-019-1603-3 · Cited by 59
Pawlik, Ł., Buma, B. J., Šamonil, P., Kvaček, J., Gałązka, A., Kohout, P., & Malik, I. (2020) · Earth-Science Reviews · doi:10.1016/j.earscirev.2020.103200 · Cited by 59
Cutler, N. A., Oliver, A., VILES, H. A., Ahmad, S., & Whiteley, A. S. (2013) · International Biodeterioration & Biodegradation · doi:10.1016/j.ibiod.2013.03.010 · Cited by 58
“Lists of epilithic eukaryotes usually run to tens of species, rather than hundreds or thousands: Rindi (2007), for example, reported around 100 taxa in a review of algae in Irish urban habitats; Burford et al. (2003a) recorded w60 species in a review of fungal species on building stone worldwide.”
BackgroundXu, H. G., Tsukuda, M., Takahara, Y., Sato, T., Gu, J., & Katayama, Y. (2017) · International Biodeterioration & Biodegradation · doi:10.1016/j.ibiod.2017.10.005 · Cited by 58
“Deterioration by fungi has been found on diverse inorganic materials of natural or man-made: cave rocks, minerals, antique marbles, and concrete by means of mycelia invasion and organic acids excreting (Gorbushina et al., 1993; Gómez-Alarcón et al., 1994; Gu et al., 1998; Burford et al., 2003; Bastian and Alabouvette,…”
BackgroundLiu, D., Lian, B., Wang, B., & Jiang, G. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028803 · Cited by 57
“Bioweathering as a common geochemical process is the erosion, decay and decomposition of rocks and minerals mediated by living organisms [1,2].”
BackgroundTales from the tomb: the microbial ecology of exposed rock surfaces
Brewer, T. E., & Fierer, N. (2017) · Environmental Microbiology · doi:10.1111/1462-2920.14024 · Cited by 56
“…buffered by limestone chemistry, mechanical stress from the contraction and expansion of fungal VC 2017 Society for Applied Microbiology and John Wiley & Sons Ltd, Environmental Microbiology, 20, 958–970 filaments through wetting and drying cycles can also weather limestone (Burford et al., 2003).”
BackgroundLi, F., Liu, L., Liu, J., & Yang, K. (2019) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2019.05.091 · Cited by 56
Cold-Adapted Yeasts in Arctic Habitats
Zalar, P., & Gunde‐Cimerman, N. (2013) · Springer eBooks · doi:10.1007/978-3-642-39681-6_3 · Cited by 57
“The darkly pigmented non-lichenised yeasts inhabit the black layer, and Rhodotorula and Sporobolomyces, together with hyaline filamentous fungi, inhabit the white layer (Burford et al. 2003).”
BackgroundFungal biotransformation of zinc silicate and sulfide mineral ores
Wei, Z., Liang, X., Pendlowski, H., Hillier, S., Suntornvongsagul, K., Sihanonth, P., & Gadd, G. M. (2013) · Environmental Microbiology · doi:10.1111/1462-2920.12089 · Cited by 56
Bacterial and fungal geomicrobiology: a problem with communities?
Gadd, G. M. (2008) · Geobiology · doi:10.1111/j.1472-4669.2007.00137.x · Cited by 55
“Geomycology can be considered a subset of geomicrobiology or geobiology, and defined as the role that fungi have played and are playing in fundamental geological processes (Burford et al ., 2003a,b; Gadd, 2006, 2007).”
BackgroundThe Geomycology of Elemental Cycling and Transformations in the Environment
Gadd, G. M. (2017) · Microbiology Spectrum · doi:10.1128/microbiolspec.funk-0010-2016 · Cited by 57
“granite, sandstone, basalt, gneiss, dolerite and quartz, even from the most extreme 218 environments (9,16,48).”
BackgroundInfluentialBioweathering of chrysotile by fungi isolated in ophiolitic sites
Daghino, S., Martino, E. M. D., Vurro, E., Tomatis, M., Girlanda, M., Fubini, B., & Perotto, S. (2008) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2008.01239.x · Cited by 54
“The Aosta Valley (Italy) Previously reported to be associated with sandstone, marble, granite (Burford et al., 2003) and able to secrete organic acids (Sterflinger, 2000) (i) Trichoderma harzianum Serpentinic substrate, Balangero”
BackgroundInfluentialCarcaillet, J. T., Manighetti, I., Chauvel, C., Schlagenhauf, A., & Nicole, J.-M. (2008) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2008.03.059 · Cited by 53
“7), moisture or biogenic features (such as lichens, bacteria, etc...; Danin et al., 1983; Chen et al., 2000; White, 2000; Burford et al., 2003).”
BackgroundSoil Fungi Reduce the Iron Content and the DNA Damaging Effects of Asbestos Fibers
Daghino, S., Turci, F., Tomatis, M., Favier, A., Perotto, S., Douki, T., & Fubini, B. (2006) · Environmental Science & Technology · doi:10.1021/es060881v · Cited by 52
Kang, S., Waqas, M., Shahzad, R., You, Y., Asaf, S., Khan, M. A., Lee, K.-E., Joo, G.-J., Kim, S.-J., & Lee, I. (2017) · Soil Science & Plant Nutrition · doi:10.1080/00380768.2017.1314829 · Cited by 52
“The bioweathering process assumes a basic role in the extraction of supplements from rocks, (Burford et al. 2003; Li et al. 2006).”
Background
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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