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Fungi in Biofilms of Highly Acidic Soils

  • Martina Hujslová
  • Milan Gryndler
Chapter

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.

Keywords

Acidity Biofilm Soil Extremophilic fungi Diversity 

Notes

Acknowledgements

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.

References

  1. Aguilera A (2013) Eukaryotic organisms in extreme acidic environments, the Río Tinto Case. Life 3:363–374CrossRefGoogle Scholar
  2. 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 107–118CrossRefGoogle Scholar
  3. Aliaga-Goltsman DS, Comolli LR, Thomas BC, Banfield JF (2015) Community transcriptomics reveals unexpected high microbial diversity in acidophilic biofilm communities. ISME J 9:1014–1023CrossRefGoogle Scholar
  4. Amaral-Zettler LA (2013) Eukaryotic diversity at pH extremes. Front Microbiol 3:1–17CrossRefGoogle Scholar
  5. Amaral-Zettler LA, Gomez F, Zettler E, Keenan BG, Amils R, Sogin ML (2002) Eukaryotic diversity in Spain’s river of fire. Nature 417:137CrossRefGoogle Scholar
  6. 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 204:205–209CrossRefGoogle Scholar
  7. Baker BJ, Banfield JF (2003) Microbial communities in acid mine drainage. FEMS Microbiol Ecol 44:139–152CrossRefGoogle Scholar
  8. 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):6264–6271CrossRefGoogle Scholar
  9. 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):2192–2199CrossRefGoogle Scholar
  10. 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):4962–4971CrossRefGoogle Scholar
  11. Brock TD (1978) Thermophilic micro-organisms and life at high temperatures. Springer-Verlag, New York, p 465CrossRefGoogle Scholar
  12. 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 47:66–77CrossRefGoogle Scholar
  13. 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 317–337Google Scholar
  14. Cooke WB (1976) Fungi in and near streams carrying acid mine-drainage. Ohio J Sci 76(5):231Google Scholar
  15. 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):1637–1646CrossRefGoogle Scholar
  16. 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 43:883–894CrossRefGoogle Scholar
  17. 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 57:139–148CrossRefGoogle Scholar
  18. 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 2:109–118Google Scholar
  19. 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 2:119–127Google Scholar
  20. Gimmler H, de Jesus J, Greiser A (2001) Heavy metal resistance of the extreme acidotolerant filamentous fungus Bispora sp. Microb Ecol 42:87–98CrossRefGoogle Scholar
  21. Gostinčar C, Grube M, de Hoog S, Zalar P, Gunde-Cimerman G (2010) Extremotolerance in fungi: evolution on the edge. FEMS Microbiol Ecol 71:2–11CrossRefGoogle Scholar
  22. Gould WD, Fujikawa JI, Cook FD (1974) A soil fungus tolerant to extreme acidity and high salt concentrations. Can J Microbiol 20:1023–1027CrossRefGoogle Scholar
  23. Gross S, Robbins EI (2000) Acidophilic and acid-tolerant fungi and yeasts. Hydrobiologia 433:91–109CrossRefGoogle Scholar
  24. 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 14:465–474CrossRefGoogle Scholar
  25. Harris JE (1985) Gelrite as an agar substitute for the cultivation of mesophilic Methanobacter and Methanobrevibacter species. Appl Environ Microbiol 50:1107–1109PubMedPubMedCentralGoogle Scholar
  26. 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 86:287–294CrossRefGoogle Scholar
  27. 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 9:1–15CrossRefGoogle Scholar
  28. 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 58:33–45CrossRefGoogle Scholar
  29. 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 13:819–831Google Scholar
  30. 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 73:321–337CrossRefGoogle Scholar
  31. Johnson DB (1998) Biodiversity and ecology of acidophilic microorganisms. FEMS Microbiol Ecol 27:307–317CrossRefGoogle Scholar
  32. Johnson DB (2009) Extremophiles: acid environments. In: Schaechter M (ed) Encyclopedia of microbiology. Academic Press, Oxford, pp 107–126CrossRefGoogle Scholar
  33. Johnson DB (2012) Geomicrobiology of extremely acidic subsurface environments. FEMS Microbiol Ecol 81:2–12CrossRefGoogle Scholar
  34. Joseph JM (1953) Microbiological study of acid mine waters: preliminary study. Ohio J Sci 53(2):123Google Scholar
  35. Kolařík M, Hujslová M, Vázquez-Campos X (2015) Acidotolerant genus Fodinomyces (Ascomycota: Capnodiales) is a synonym of Acidiella. Czech Mycol 67:37–38CrossRefGoogle Scholar
  36. 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/s41598-017-03315-6CrossRefPubMedPubMedCentralGoogle Scholar
  37. 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.2017.00683CrossRefPubMedPubMedCentralGoogle Scholar
  38. López-Archilla AI, Amils R (1999) A comparative ecological study of two acidic rivers in southwestern Spain. Microb Ecol 38:146–156CrossRefGoogle Scholar
  39. López-Archilla AI, Marin I, Amils R (2001) Microbial community composition and ecology of an acidic aquatic environment: the Tinto River, Spain. Microb Ecol 41:20–35PubMedGoogle Scholar
  40. 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 235:221–228CrossRefGoogle Scholar
  41. 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 50:923–934CrossRefGoogle Scholar
  42. Macalady JL, Jones DS, Lyon EH (2007) Extremely acidic, pendulous cave wall biofilms from the Frasassi cave system, Italy. Environ Microbiol 9(6):1402–1414CrossRefGoogle Scholar
  43. Magan N (1997) Fungi in extreme environments. In: Wicklow DT, Soderstrom BE (eds) The Mycota IV. Environmental and microbial relationships. Springer-Verlag, Berlin, pp 99–114Google Scholar
  44. 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.2015.00475CrossRefPubMedPubMedCentralGoogle Scholar
  45. 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.2017.01756CrossRefPubMedPubMedCentralGoogle Scholar
  46. 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.00484-12CrossRefGoogle Scholar
  47. 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 7:238CrossRefGoogle Scholar
  48. 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):2228–2237CrossRefGoogle Scholar
  49. 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/min6020037CrossRefGoogle Scholar
  50. 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 43:139–147CrossRefGoogle Scholar
  51. 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 433:15–23CrossRefGoogle Scholar
  52. 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 61:1–20CrossRefGoogle Scholar
  53. Sigler L, Carmichael JW (1974) A new acidophilic Scytalidium. Can J Microbiol 20:267–268CrossRefGoogle Scholar
  54. Sletten O, Skinner CE (1948) Fungi capable of growing in strongly acid media and in concentrated copper sulfate solutions. J Bacteriol 56:679–681PubMedPubMedCentralGoogle Scholar
  55. Starkey RL, Waksman SA (1943) Fungi tolerant to extreme acidity and high concentrations of copper sulfate. J Bacteriol 45:509–519PubMedPubMedCentralGoogle Scholar
  56. Tiquia-Arashiro SM, Rodrigues D (2016) Alkaliphiles and Acidophiles in Nanotechnology. In: Extremophiles: applications in nanotechnology. Springer International Publishing, New York, pp 129–162CrossRefGoogle Scholar
  57. 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):1073–1089CrossRefGoogle Scholar
  58. 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 3:266–270CrossRefGoogle Scholar
  59. Yamazaki A, Toyama K, Nakagiri A (2010) A new acidophilic fungus Teratosphaeria acidotherma (Capnodiales, Ascomycota) from a hot spring. Mycoscience 51:443–455CrossRefGoogle Scholar
  60. 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 303–315CrossRefGoogle Scholar
  61. 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):83–94CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Laboratory of Fungal BiologyInstitute of Microbiology ASCRPrague 4Czech Republic
  2. 2.Faculty of Science, Department of BiologyJan Evangelista Purkyně University in Ústí nad LabemÚstí nad LabemCzech Republic

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