Abstract
Acidophilic fungi colonize highly acidic environments (including soils), where other closely taxonomically related fungi cannot grow. Currently known fungal species inhabiting highly acidic sites can be regarded as extreme or moderate acidophiles with broad ecological amplitude. No obligate acidophilic fungus has been described to date. The most abundant biological structures encountered in highly acidified water environments are the microbial communities forming biofilms, which reflects the notion of biofilm formation as adaptation to extreme conditions (here the extreme acidity). Because the majority of soil microorganisms are living in the biofilm, significant analogies in ecology of acidophilic organisms inhabiting the soil and organisms inhabiting biofilms in other acidic environments (streamers, slimes, mats, snottites) are probable. Observations of extremophilic fungal taxa in acidic soils and other acidic environments suggest that it is the acidity of the environment and not its type what substantially determines the community of the inhabiting fungi. Acidophily of fungi (including those living in acidic soils) is probably connected with their life strategy as biofilm inhabitants and represents a general ecological phenomenon that merits serious scientific study.
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References
Aguilera A (2013) Eukaryotic organisms in extreme acidic environments, the Río Tinto Case. Life 3:363–374
Aguilera A, Olsson S, Puerte-Sánchez F (2016) Physiological and phylogenetic diversity of acidophilic eukaryotes. In: Quatrini R, Johnson DB (eds) Acidophiles. Life in extremely acidic environment. Caister Academic Press, Norfolk, pp 107–118
Aliaga-Goltsman DS, Comolli LR, Thomas BC, Banfield JF (2015) Community transcriptomics reveals unexpected high microbial diversity in acidophilic biofilm communities. ISME J 9:1014–1023
Amaral-Zettler LA (2013) Eukaryotic diversity at pH extremes. Front Microbiol 3:1–17
Amaral-Zettler LA, Gomez F, Zettler E, Keenan BG, Amils R, Sogin ML (2002) Eukaryotic diversity in Spain’s river of fire. Nature 417:137
Amaral-Zettler LA, Messerli MA, Laatsch AD, Smith PJS, Sorgin ML (2003) From genes to genomes: beyond biodiversity in Spain’s Rio Tinto. Biol Bull 204:205–209
Baker BJ, Banfield JF (2003) Microbial communities in acid mine drainage. FEMS Microbiol Ecol 44:139–152
Baker BJ, Lutz MA, Dawson SC, Bond PL, Banfield JF (2004) Metabolically active eukaryotic communities in extremely acidic mine drainage. Appl Environ Microbiol 70(10):6264–6271
Baker BJ, Tyson GW, Goosherst L, Banfield JF (2009) Insights into the diversity of eukaryotes in acid mine drainage biofilm communities. Appl Environ Microbiol 75(7):2192–2199
Bond PL, Druschel GK, Banfield JF (2000) Comparison of acid mine drainage microbial communities in physically and geochemically distinct ecosystems. Appl Environ Microbiol 66(11):4962–4971
Brock TD (1978) Thermophilic micro-organisms and life at high temperatures. Springer-Verlag, New York, p 465
Bühring SI, Schubotz F, Harms C, Lipp JS, Amils R, Hinrichs K-U (2012) Lipid signatures of acidophilic microbial communities in an extreme acidic environment – Río Tinto, Spain. Org Geochem 47:66–77
Cavicchioli R, Thomas T (2000) Extremophiles. In: Lederberg J, Alexander M, Bloom BR, Hopwood D, Hull R, Iglewski BH, Laskin AI, Oliver SG, Schaechter M, Summers WC (eds) Encyclopedia of microbiology. Academic Press, San Diego, CA, pp 317–337
Cooke WB (1976) Fungi in and near streams carrying acid mine-drainage. Ohio J Sci 76(5):231
de Goes KCGP, da Silva JJ, Lovato GM, Iamanaka BT, Massi FP, Andrade DS (2017) Talaromyces sayulitensis, Acidiella bohemica and Penicillium citrinum in Brazilian oil shale by-products. Antonie Van Leeuwenhoek 110(12):1637–1646
Das BK, Roy A, Koschorreck M, Mandal SM, Wendt-Potthoff K, Bhattacharya J (2009) Occurrence and role of algae and fungi in acid mine drainage environment with special reference to metals and sulfate immobilization. Water Res 43:883–894
Gadanho M, Sampaio JP (2006) Microeukaryotic diversity in the extreme environments of the Iberian Pyrite Belt: a comparison between universal and fungi-specific primer sets, temperature gradient gel electrophoresis and cloning. FEMS Microbiol Ecol 57:139–148
Gherman VD, Bréheret J-G, Bularda M-D (2007a) Microorganism populations within gelatinous formations from Kiesberg mine in Banat Mountains, Romania. Studia Universitates Babeş-Bollyai Biologia LII 2:109–118
Gherman VD, Bréheret J-G, Bularda M-D (2007b) Microorganism associations within a thin acid solution film from an old mine in Banat Mountains. Studia Universitates Babeş-Bollyai Biologia LII 2:119–127
Gimmler H, de Jesus J, Greiser A (2001) Heavy metal resistance of the extreme acidotolerant filamentous fungus Bispora sp. Microb Ecol 42:87–98
Gostinčar C, Grube M, de Hoog S, Zalar P, Gunde-Cimerman G (2010) Extremotolerance in fungi: evolution on the edge. FEMS Microbiol Ecol 71:2–11
Gould WD, Fujikawa JI, Cook FD (1974) A soil fungus tolerant to extreme acidity and high salt concentrations. Can J Microbiol 20:1023–1027
Gross S, Robbins EI (2000) Acidophilic and acid-tolerant fungi and yeasts. Hydrobiologia 433:91–109
Hao C, Wang L, Gao Y, Zhang L, Dong H (2010) Microbial diversity in acid mine drainage of Xiang Mountain sulfide mine, Anhui Province, China. Extremophiles 14:465–474
Harris JE (1985) Gelrite as an agar substitute for the cultivation of mesophilic Methanobacter and Methanobrevibacter species. Appl Environ Microbiol 50:1107–1109
Hölker U, Bend J, Pracht R, Tetsch L, Müller T, Höfer M, de Hoog GS (2004) Hortaea acidophila, a new acid-tolerant black yeast from lignite. Antonie Van Leeuwenhoek 86:287–294
Hujslová M, Kubátová A, Chudíčková M, Kolařík M (2010) Diversity of fungal communities in saline and acidic soils in the Soos National Natural Reserve, Czech Republic. Mycol Prog 9:1–15
Hujslová M, Kubátová A, Kostovčík M, Kolařík M (2013) Acidiella bohemica gen. et sp. nov. and Acidomyces spp. (Teratosphaeriaceae), the indigenous inhabitants of extremely acidic soils in Europe. Fungal Divers 58:33–45
Hujslová M, Kubátová A, Kostovčík M, Blanchette RA, de Beer ZW, Chudíčková M, Kolařík M (2014) Three new genera of fungi from extremely acidic soils. Mycol Prog 13:819–831
Hujslová M, Kubátová A, Bukovská P, Chudíčková M, Kolařík M (2017) Extremely acidic soils are dominated by species-poor and highly specific fungal communities. Microb Ecol 73:321–337
Johnson DB (1998) Biodiversity and ecology of acidophilic microorganisms. FEMS Microbiol Ecol 27:307–317
Johnson DB (2009) Extremophiles: acid environments. In: Schaechter M (ed) Encyclopedia of microbiology. Academic Press, Oxford, pp 107–126
Johnson DB (2012) Geomicrobiology of extremely acidic subsurface environments. FEMS Microbiol Ecol 81:2–12
Joseph JM (1953) Microbiological study of acid mine waters: preliminary study. Ohio J Sci 53(2):123
Kolařík M, Hujslová M, Vázquez-Campos X (2015) Acidotolerant genus Fodinomyces (Ascomycota: Capnodiales) is a synonym of Acidiella. Czech Mycol 67:37–38
Krause S, Bremges A, Münch PC, McHardy AC, Gescher J (2017) Characterisation of a stable laboratory co-culture of acidophilic nanoorganisms. Sci Rep 7:3289. https://doi.org/10.1038/s41598-017-03315-6
Li X, Kappler U, Jiang G, Bond PL (2017) The ecology of acidophilic microorganisms in the corroding concrete sewer environment. Front Microbiol 8:683. https://doi.org/10.3389/fmicb.2017.00683
López-Archilla AI, Amils R (1999) A comparative ecological study of two acidic rivers in southwestern Spain. Microb Ecol 38:146–156
López-Archilla AI, Marin I, Amils R (2001) Microbial community composition and ecology of an acidic aquatic environment: the Tinto River, Spain. Microb Ecol 41:20–35
López-Archilla AI, Gérard E, Moreira D, López-García P (2004a) Macrofilamentous microbial communities in the metal-rich and acidic River Tinto, Spain. FEMS Microbiol Lett 235:221–228
López-Archilla AI, González AE, Terrón MC, Amils R (2004b) Ecological study of the fungal populations of the acidic Tinto River in southwestern Spain. Can J Microbiol 50:923–934
Macalady JL, Jones DS, Lyon EH (2007) Extremely acidic, pendulous cave wall biofilms from the Frasassi cave system, Italy. Environ Microbiol 9(6):1402–1414
Magan N (1997) Fungi in extreme environments. In: Wicklow DT, Soderstrom BE (eds) The Mycota IV. Environmental and microbial relationships. Springer-Verlag, Berlin, pp 99–114
Méndez-García C, Peláez AI, Mesa V, Sánchez J, Golyshina OV, Ferrer M (2015) Microbial diversity and metabolic networks in acid mine drainage habitats. Front Microbiol 6:475. https://doi.org/10.3389/fmicb.2015.00475
Mesa V, Gallego JLR, Gonzáles-Gil R, Lauga B, Sánchez J, Méndez-García PAI (2017) Bacterial, archaeal, and eukaryotic diversity across distinct microhabitats in an acid mine drainage. Front Microbiol 8:1756. https://doi.org/10.3389/fmicb.2017.01756
Mosier AC, Justice NB, Bowen BP, Baran R, Thomas BC, Northen TR, Banfield JF (2013) Metabolites associated with adaptation of microorganisms to an acidophilic, metal-rich environment identified by stable-isotope-enabled metabolomics. mBio 4(2):00484–00412. https://doi.org/10.1128/mBio.00484-12
Mosier AC, Miller CS, Frischkorn KR, Ohm RA, Li Z, LaButti K, Lapidus A, Lipzen A, Chen C, Johnson J, Lindquist EA, Pan C, Hettich RL, Grigoriev IV, Singer SW, Banfield JF (2016) Fungi contribute critical but spatially varying roles in nitrogen and carbon cycling in acid mine drainage. Front Microbiol 7:238
Oggerin M, Tornos F, Rodríguez N, del Moral C, Sánchez-Román M, Amils R (2013) Specific jarosite biomineralization by Purpureocillium lilacinum, an acidophilic fungi isolated from Río Tinto. Environ Microbiol 15(8):2228–2237
Oggerin M, Tornos F, Rodriguez N, Pascual L, Amils R (2016) Fungal iron biomineralization in Rio Tinto. Fortschr Mineral 6(2):37. https://doi.org/10.3390/min6020037
Quatrini R, Johnson DB (2018) Microbiomes in extremely acidic environments: functionalities and interactions that allow survival and growth of prokaryotes at low pH. Curr Opin Microbiol 43:139–147
Robbins EI, Rodgers TM, Alpers CN, Nordstrom DK (2000) Ecogeochemistry of the surface food web at pH 0-2.5 in Iron Mountain, California, USA. Hydrobiologia 433:15–23
Selbmann L, Hoog GS, de Zucconi L, Isola D, Ruisi S, Gerrits van den Ende AHG, Ruibal C, De Leo F, Urzì C, Onofri S (2008) Drought meets acid: three new genera in a dothidealean clade of extremotolerant fungi. Stud Mycol 61:1–20
Sigler L, Carmichael JW (1974) A new acidophilic Scytalidium. Can J Microbiol 20:267–268
Sletten O, Skinner CE (1948) Fungi capable of growing in strongly acid media and in concentrated copper sulfate solutions. J Bacteriol 56:679–681
Starkey RL, Waksman SA (1943) Fungi tolerant to extreme acidity and high concentrations of copper sulfate. J Bacteriol 45:509–519
Tiquia-Arashiro SM, Rodrigues D (2016) Alkaliphiles and Acidophiles in Nanotechnology. In: Extremophiles: applications in nanotechnology. Springer International Publishing, New York, pp 129–162
Vázquez-Campos X, Kinsela AS, Waite TD, Collins RN, Neilan BA (2014) Fodinomyces uranophilus gen. nov. sp. nov. and Coniochaeta fodinicola sp. nov., two uranium mine-inhabiting Ascomycota fungi from northern Australia. Mycologia 106(6):1073–1089
Wilmes P, Remis JP, Hwang M, Auer M, Thelen MP, Banfield JF (2009) Natural acidophilic biofilm communities reflect distinct organismal and functional organization. ISME J 3:266–270
Yamazaki A, Toyama K, Nakagiri A (2010) A new acidophilic fungus Teratosphaeria acidotherma (Capnodiales, Ascomycota) from a hot spring. Mycoscience 51:443–455
Zak JC, Wildman HG (2004) Fungi in stressful environments. In: Mueller GM, Bills GF, Foster MS (eds) Biodiversity of fungi, inventory and monitoring methods. Elsevier Academic Press, London, pp 303–315
Zirnstein I, Arnold T, Krawczyk-Bärsch E, Jenk U, Bernhard G, Röske I (2012) Eukaryotic life in biofilms formed in a uranium mine. Microbiologyopen 1(2):83–94
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Footnote: This text has been created within the frame of the project 17-09946S supported by the Czech Science Foundation. We would like to thank Dr. Miroslav Kolařík (Institute of Microbiology ASCR, The Czech Republic) for providing microscopic photos.
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Hujslová, M., Gryndler, M. (2019). Fungi in Biofilms of Highly Acidic Soils. In: Tiquia-Arashiro, S., Grube, M. (eds) Fungi in Extreme Environments: Ecological Role and Biotechnological Significance. Springer, Cham. https://doi.org/10.1007/978-3-030-19030-9_11
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