Environmental Earth Sciences

, Volume 72, Issue 8, pp 2779–2796 | Cite as

Spatial and temporal distribution and characteristics of eukaryote-dominated microbial biofilms in an acid mine drainage environment: implications for development of iron-rich stromatolites

  • S. S. Brake
  • I. Arango
  • S. T. Hasiotis
  • K. R. Burch
Original Article

Abstract

Spatial and temporal distribution and characteristics of three eukaryotic biofilms were monitored for an 18-month period in an acid mine drainage environment at the Green Valley coalmine in Indiana, USA. Each biofilm is dominated (>90 %) by a single eukaryotic microorganism based on enumeration: Euglena mutabilis, the diatom species Nitzschia tubicola, and a filamentous alga belonging to the genus Klebsormidium sp. The E. mutabilis-dominated biofilm occurs year round, covering up to 100 % of the channel bottom in spring and fall. The N. tubicola-dominated biofilm is less abundant, exists as small patches in spring and fall, expands from these patches to cover up to 50 % of the channel bottom in June, and is absent in winter. The Klebsormidium-dominated biofilm is restricted to small patches covering <5 % of the channel bottom from spring through fall and is absent in winter. Also present are floating microbial scum layers. The eukaryotic biofilms and scum layers contribute to the attenuation of precipitates and to the formation of organosedimentary structures, or stromatolites, by trapping and binding chemical precipitates via aerotaxis and phototaxis and by serving as a medium for passive accumulation of precipitates. Each stromatolite layer represents the morphological characteristics of each eukaryotic biofilm that served as the architect of the layer and the time of year the biofilm populated the channel. Processes involved in stromatolite formation also attenuate chemical sediments by binding them to the channel bottom and prior stromatolite surface rather than allowing them to be carried to the adjacent drainage system where they may become bioavailable to other forms of life.

Keywords

Euglena mutabilis Nitzschia tubicola Klebsormidium Biofilms Stromatolites 

References

  1. Aguilera A, Souza-Egipsy V, Gómez F, Amils R (2007a) Development and structure of eukaryotic biofilms in an extreme acidic environment, Río Tinto (SW, Spain). Microb Ecol 53:294–305CrossRefGoogle Scholar
  2. Aguilera A, Zettler E, Gómez F, Amaral-Zettler L, Rodríguez N, Amils R (2007b) Distribution and seasonal variability in the benthic eukaryotic community of Río Tinto (SW, Spain), an acidic, high metal extreme environment. Syst Appl Microbiol 30:531–546CrossRefGoogle Scholar
  3. Awramik SM, Margulis L, Barghoorn ES (1976) Evolutionary processes in the formation of stromatolites. In: Walter MR (ed) Stromatolites. Elsevier, New York, pp 149–162CrossRefGoogle Scholar
  4. Banfield JF, Welch SA, Zhang H, Ebert TT, Penn RL (2000) Aggregation-based crystal growth and microstructure development in natural iron oxyhydroxide biomineralization products. Science 289:751–754CrossRefGoogle Scholar
  5. Bauld J, D’Amelio E, Farmer JD (1992) Modern microbial mats. In: Schopf J, Klein C (eds) The Proterozoic biosphere. Cambridge University Press, New York, pp 261–269Google Scholar
  6. Beveridge TJ (1989) Role of cellular design in bacterial metal accumulation and mineralization. Ann Rev Microbiol 43:147–171CrossRefGoogle Scholar
  7. Bigham JM, Nordstrom DK (2000) Iron and aluminum hydroxysulfates from acid sulfate water. In: Alpers CN, Jambor JL, Nordstrom DE (eds) Sulfate minerals-crystallography, geochemistry, and environmental significance, vol 40., Review in mineralogy and geochemistry. Mineralogical Society of America, Washington, DC, pp 351–403Google Scholar
  8. Bigham JM, Schwertmann U, Carlson L, Muard E (1990) A poorly crystallized oxyhydroxysulfate of iron formed by bacterial oxidation of Fe(II) in acid mine waters. Geochim Cosmochim Acta 54:2743–2758CrossRefGoogle Scholar
  9. Bosak T, Greene SE, Newman DK (2007) A likely role for anoxygenic photosynthetic microbes in the formation of ancient stromatolites. Geobiology 5:119–126CrossRefGoogle Scholar
  10. Boult S, Johnson M, Curtis C (1997) Recognition of a biofilm at the sediment-water interface of an acid mine drainage-contaminated stream, and its role in controlling iron flux. Hydrol Process 11:391–399CrossRefGoogle Scholar
  11. Brake SS, Hasiotis ST (2010) Eukaryote-dominated biofilms and their significance in acidic environments. Geomicrobiol J 27:534–558CrossRefGoogle Scholar
  12. Brake SS, Dannelly HK, Jones M, Lawson LA (1999) Acid mine drainage at the Green Valley Mine, Vigo County, Indiana: possible influence of an acidophilic alga. In: Oliver J, Dutta P (eds) Indiana Studies. Indiana State University Prof. Paper, vol 21, pp 45–52Google Scholar
  13. Brake SS, Connors KA, Romberger SB (2001) A river runs through it: impact of acid mine drainage on the geochemistry of West Little Sugar Creek pre- and post-reclamation at the Green Valley coal mine, Indiana, USA. Environ Geol 40:1471–1481CrossRefGoogle Scholar
  14. Brake SS, Hasiotis ST, Dannelly HK, Connors KA (2002) Eukaryotic stromatolite builders in acid mine drainage: implications for Precambrian iron formations and oxygenation of the atmosphere? Geology 30:599–602CrossRefGoogle Scholar
  15. Brierley JA, Brierley CL (1999) Present and future commercial applications of biohydrometallurgy. In: Amils R, Ballester A (eds) Biohydrometallurgy and the environment toward the mining of the 21st century, Part A. Elsevier, Amsterdam, pp 81–89Google Scholar
  16. Brierley CL, Brierley JA, Davidson MS (1989) Applied microbial processes for metal recovery and removal from wastewater. In: Beveridge TJ, Doyle RJ (eds) Metal ions and bacteria. Wiley, New York, pp 359–381Google Scholar
  17. Bruneel O, Duran R, Casiot C, Elbaz-Poulichet F, Personne J-C (2006) Diversity of microorganisms in Fe–As-rich acid mine drainage waters of Caroulès, France. Appl Environ Microb 72:551–556CrossRefGoogle Scholar
  18. Butcher RW (1946) The algal growth in certain highly calcareous streams. J Ecol 28:283–286Google Scholar
  19. Cohn SA, Weitzell RE (1996) Ecological considerations of diatom cell motility. I. Characterization of motility and adhesion in four diatom species. J Phycol 30:928–939CrossRefGoogle Scholar
  20. Colmer AR, Temple KL, Hinkle HE (1950) Anion-oxidizing bacterium from the acid drainage of some bituminous coal mines. J Bacteriol 59:317–328Google Scholar
  21. Costerton JW, Marrie TJ, Cheng K-J (1985) Phenomena of bacterial adhesion. In: Savage DC, Fletcher M (eds) Bacterial adhesion: mechanisms and physiological significance. Plenum Press, New York, pp 3–43CrossRefGoogle Scholar
  22. Coupland K, Johnson DB (2004) Geochemistry and microbiology of an impounded subterranean acidic water body at Mynydd Parys, Anglesey, Wales. Geobiology 2:77–86CrossRefGoogle Scholar
  23. Dach HV (1943) The effect of pH on pure cultures of Euglena mutabilis. Ohio J Sci 43:47–48Google Scholar
  24. Daniel GF, Chamberlain AHL, Jones EBG (1987) Cytochemical and electron microscopical observations on the adhesive materials of marine fouling diatoms. Br Phycol J 22:101–118CrossRefGoogle Scholar
  25. Decho AW (1994) Molecular-scale events influencing the macroscale cohesiveness of exopolymers. In: Krumbein WE, Paterson DM, Stal LJ (eds) Biostabilization of sediments. University of Oldenburg, Oldenburg, pp 135–148Google Scholar
  26. Decho AW (2000) Exopolymer microdomains as a structuring agent for heterogeneity within microbial biofilms. In: Riding RE, Awramik SM (eds) Microbial sediments. Springer, Heidelberg, pp 9–15CrossRefGoogle Scholar
  27. Decho AW, Castenholtz RW (1986) Spatial patterns and feeding of meiobenthic harpacticoid copepods in relation to resident microbial flora. Hydrobiologia 131:87–96CrossRefGoogle Scholar
  28. Dodd JJ (1987) The illustrated flora of Illinois. Southern Illinois University Press, CarbondaleGoogle Scholar
  29. Drever JI (1997) The geochemistry of natural waters, 3rd edn. Prentice Hall, Upper Saddle RiverGoogle Scholar
  30. Druschel GK, Baker BJ, Gihring TM, Banfield JF (2004) Acid mine drainage biogeochemistry at Iron Mountain, California. Geochem Trans 5:13–32CrossRefGoogle Scholar
  31. Dzombak DA, Morel FMM (1990) Surface complexation modeling-hydrous ferric oxide. John Wiley and Sons, SomersetGoogle Scholar
  32. Edwards KJ, Bond PL, Gihring TM, Banfield JF (2000) An Archeal iron-oxidizing extreme acidophile important in acid mine drainage. Science 287:1796–1799CrossRefGoogle Scholar
  33. Epply RW (1977) The growth and culture of diatoms. In: Werner D (ed) The biology of diatoms, botanical monographs, vol 13. University of California Press, Berkeley, pp 24–64Google Scholar
  34. Ferris FG, Tazaki L, Fyfe WS (1989) Iron oxides in acid mine drainage environments and their association with bacteria. Chem Geol 74:321–330CrossRefGoogle Scholar
  35. Fitch FJ (1959) Macro point counting. Am Mineral 44:667–668Google Scholar
  36. Foster JS, Green SJ (2011) Microbial diversity in modern stromatolites. In: Tewari VC, Seckback J (eds) Stromatolites: interaction of microbes with sediment. Cellular origin, life in extreme habitats, and astrobiology, vol 18, pp 383–405Google Scholar
  37. Fowler TA, Crundwell FK (1999) Leaching of zinc sulfide by Thiobacillus ferrooxidans: bacterial oxidation of the sulfur product layer increases the rate of zinc sulfide dissolution at high concentrations of ferrous ions. Appl Environ Microb 65:5285–5292Google Scholar
  38. Gadd GM (1990) Metal tolerance. In: Edwards C (ed) Microbiology of extreme environments. McGraw-Hill, New York, pp 178–209Google Scholar
  39. Golubic S (1976) Organisms that build stromatolites. In: Walter MR (ed) Stromatolites. Elsevier, New York, pp 113–126CrossRefGoogle Scholar
  40. Golubic S, Seong-Joo L, Browne KM (2000) Cyanobacteria: architects of sedimentary structures. In: Riding RE, Awramik SM (eds) Microbial sediments. Springer, Berlin, pp 57–67CrossRefGoogle Scholar
  41. Häder D-P, Hoiczyk E (1992) Gliding motility. In: Melkonian M (ed) Algal cell motility. Chapman and Hall, New York, pp 1–38CrossRefGoogle Scholar
  42. Häder D-P, Melkonian M (1983) Phototaxis in the gliding flagellate, Euglena mutabilis. Arch Microbiol 135:25–29CrossRefGoogle Scholar
  43. Hallberg KB, Johnson DB (2003) Novel acidophiles isolated from moderately acidic mine drainage waters. Hydrometallurgy 71:139–148CrossRefGoogle Scholar
  44. Hallmann R, Friedrich A, Koops H-P, Pommerening-Röser A, Rohde K, Zenneck C, Sand W (1993) Physiological characteristics of Thiobacillus ferrooxidans and Leptospirillum ferrooxidans and physiochemical factors influence microbial metal leaching. Geomicrobiol J 10:193–206CrossRefGoogle Scholar
  45. Hargreaves JW, Lloyd EJH, Whitton BA (1975) Chemistry and vegetation of highly acidic streams. Freshw Biol 5:563–576CrossRefGoogle Scholar
  46. Harper MA (1977) Movements. In: Werner D (ed) The biology of diatoms, vol 13, Botanical monograph. University of California Press, Berkley, pp 224–249Google Scholar
  47. Hoagland KD, Rosowski JR, Gretz MR, Roemer SC (1993) Diatom extracellular polymeric substances: function, fine structure, chemistry, and physiology. J Phycol 29:537–566CrossRefGoogle Scholar
  48. Hynes HBM (1970) The ecology of running waters. University of Toronto Press, TorontoGoogle Scholar
  49. Jackson ED, Ross DC (1956) A technique for modal analysis of medium- and course-grained (3-10 mm) rocks. Am Mineral 41:648–651Google Scholar
  50. Johnson DB (1998) Biodiversity and ecology of acidophilic microorganisms. FEMS Microbiol Ecol 27:307–317CrossRefGoogle Scholar
  51. Jones JRE (1951) An ecological study of the River Towy. J Anim Ecol 20:68–86CrossRefGoogle Scholar
  52. Kai T, Suenaga Y, Migita A, Takahashi T (2000) Kinetic model for simultaneous leaching of zinc sulfide and manganese dioxide in the presence of iron-oxidizing bacteria. Chem Eng Sci 55:3429–3436CrossRefGoogle Scholar
  53. Kelly MG, Bennison H, Cox EJ, Goldsmith B, Jamieson J, Juggins S, Mann DG, Telford RJ (2005) Common freshwater diatoms of Britain and Ireland: an interactive key. Environment Agency, Bristol. http://craticula.ncl.ac.uk/EADiatomKey/html/taxon13541440.html. Accessed 12 August 2011
  54. Kim JJ, Kim SJ, Tasaki K (2002) Mineralogical characterization of microbial ferrihydrite and schwertmannite, and non-biogenic Al-sulfate precipitates from acid mine drainage in the Donghae mine area, Korea. Environ Geol 42:19–31CrossRefGoogle Scholar
  55. Kleinmann RLP, Crerar DA (1979) Thiobacillus ferrooxidans and the formation of acidity in simulated coal mine environments. Geomicrobiol J 1:373–388CrossRefGoogle Scholar
  56. Krumbein WE (1986) Biotransfer of minerals by microbes and microbial mats. In: Leadbeater BSC, Riding R (eds) Biomineralization in lower plants and animals. Clarendon Press, Oxford, pp 55–72Google Scholar
  57. Krumbein WE (1994) The year of the slime. In: Krumbein WE, Paterson DM, Stal LJ (eds) Biostabilization of sediments. University of Oldenburg, Oldenburg, pp 1–7Google Scholar
  58. Kwandrans J (1993) Diatom communities of acidic mountain streams in Poland. Hydrobiologia 269(270):335–342CrossRefGoogle Scholar
  59. Lackey JB (1938) The flora and fauna of surface waters polluted by acid mine drainage. Public Health Rep 53:1499–1507CrossRefGoogle Scholar
  60. Lackey JB (1968) The biology of Euglena. I: general biology and ultrastructure. In: Buetow DE (ed) Ecology of Euglena. Academic Press, New York, pp 27–44Google Scholar
  61. Lazaroff N, Sigal W, Wasserman A (1982) Iron oxidation and precipitation of ferric hydrosulfates by resting Thiobacillus ferrooxidans cells. Appl Environ Microb 43:924–938Google Scholar
  62. Lee JJ, Leedale GF, Bradbury P (2000) The illustrated guide to the protozoa, 2nd edn. Society of Protozoologist, LawrenceGoogle Scholar
  63. Lepot K, Benzerara K, Brown GE Jr, Philppot P (2008) Microbially influenced formation of 2,724-million-year-old stromatolites. Nat Geosci 1:118–121CrossRefGoogle Scholar
  64. López-Archilla AI, Marin I, Amils R (2001) Microbial community composition and ecology of an acidic aquatic environment: the Tinto River, Spain. Microb Ecol 41:20–35Google Scholar
  65. Margulis L, Corliss JO, Melkonian M, Chapman DJ (1990) Handbook of protoctista. Jones and Bartlett Publishers, BostonGoogle Scholar
  66. Marina A, Marini L, Ottonello G, Zuccolini MV (2005) The fate of major constituents and chromium and other trace elements when acid waters from the derelict Libiola mine (Italy) are mixed with stream waters. Appl Geochem 20:1368–1390CrossRefGoogle Scholar
  67. McBride TP (1988) Preparing random distributions of diatom valves on microscopic slides. Limnol Oceanogr 33:1627–1629CrossRefGoogle Scholar
  68. Melkonian M, Meinicke-Liebelt M, Häder D-P (1986) Photokinesis and photophobic responses in the gliding flagellate, Euglena mutabilis. Plant Cell Physiol 27:505–513Google Scholar
  69. Minckley WL, Tindall DR (1963) Ecology of Batrachospermum sp. (Rhodophyta) in Doe Run, Meade County, Kentucky. Bull Torrey Bot Club 90:391–400CrossRefGoogle Scholar
  70. Moses CO, Nordstrom DK, Herman JS, Mills AL (1987) Aqueous pyrite oxidation by dissolved-oxygen and by ferric iron. Geochim Cosmochim Ac 51:1561–1571CrossRefGoogle Scholar
  71. Murayama T, Konno Y, Sakata T, Imaizumi T (1987) Application of immobilized Thiobacillus ferrooxidans for large-scale treatment of acid mine drainage. In: Mosbach K (ed) Methods in enzymology, vol 136. Academic Press, New York, pp 530–540Google Scholar
  72. Papineau D, Walker JJ, Mojzsis SJ, Pace NR (2005) Composition and structure of microbial communities from stromatolites of Hamelin Pool in Shark Bay, Western Australia. Appl Environ Microb 71:4822–4832CrossRefGoogle Scholar
  73. Patrick R, Reimer CW (1966) The diatoms of the United States, vol 13, 1st edn., Monograph Series. Academy of Natural Sciences, PhiladelphiaGoogle Scholar
  74. Pogliani C, Donati E (2000) Enhancement of copper dissolution from a sulfide ore by using Thiobacillus thiooxidans. Geomicrob J 17:35–42CrossRefGoogle Scholar
  75. Porter KG (1976) Enhancement of algal growth and productivity by grazing zooplankton. Science 192:1332–1334CrossRefGoogle Scholar
  76. PROTIST INFORMATION SERVER (2011) A digital specimen archive database, copyright 1995–2011. http://protist.i.hosei.ac.jp. Accessed November 2011
  77. Round FE, Crawford RM, Mann DG (1990) The diatoms. Biology and morphology of the genera. Cambridge University Press, CambridgeGoogle Scholar
  78. Ruttner R (1926) Bermerkungen über den Sauerstoffgehalt der Gewässer und dessen respiratorischen Wert. Naturwissenschaften 14:1237–1239CrossRefGoogle Scholar
  79. Sand W, Gerke T, Hallmann R, Schippers A (1995) Sulfur chemistry, biofilm, and the (in)direct attack mechanism—a critical evaluation of bacterial leaching. Appl Microbiol Biotechnol 43:961–966CrossRefGoogle Scholar
  80. Schopf JW, Kudryavtsev AB, Czaja AD, Tripathi AB (2007) Evidence of Archean life: stromatolites and microfossils. Precambrian Res 158:141–155CrossRefGoogle Scholar
  81. Sen AM, Johnson B (1999) Acidophilic sulphate-reducing bacteria: candidates for bioremediation of acid mine drainage. In: Amils R, Ballester A (eds) Biohydrometallurgy and the environment toward the mining of the 21st century, Part A. Elsevier, Amsterdam, pp 709–718Google Scholar
  82. Sharp RJ, Munster MJ (1986) Biotechnological implications for microorganisms from extreme environments. In: Herbert RA, Cobb GA (eds) Microbes in extreme environments. Academic Press, London, pp 215–295Google Scholar
  83. Smith KS (1999) Metal sorption on mineral surfaces-an overview with examples relating to mineral deposits. In: Plumlee GS, Logdon MJ (eds) The environmental geochemistry of mineral deposits, part A-processes, techniques, and health issues, vol 6A., Reviews in economic geology. Society of Economic Geologists, Littleton, pp 161–182Google Scholar
  84. Smithson SB (1963) A point-counter for modal analysis of stained rock slabs. Am Mineral 48:1164–1166Google Scholar
  85. Suzuki I, Takeuchi TL, Yuthasastrakosol TD, Oh JD (1990) Ferrous iron and sulfur oxidation and ferric iron reduction activities of Thiobacillus ferrooxidans are affected by growth on ferrous iron, sulfur, or a sulfide ore. Appl Environ Microb 56:1620–1626Google Scholar
  86. Swift MC (1982) Effects of coal pile runoff on stream quality and macro-invertebrate communities, vol 68., Water Resources Research Center Technical Report. University of Maryland, College ParkGoogle Scholar
  87. Torma AE (1986) Biohydrometallurgy as an emerging technology. Biotechnol Bioeng Symp 16:49–63Google Scholar
  88. Valente TM, Gomes CL (2007) The role of two acidophilic algae as ecological indicators of acid mine drainage sites. J Iber Geol 22:283–294Google Scholar
  89. Walter MR, Bauld J, Des Marais DJ, Schopf JW (1992) A general comparison of microbial mats and microbial stromatolites: bridging the gap between the modern and the fossil. In: Schopf JW, Klein C (eds) The proterozoic biosphere. Cambridge University Press, Cambridge, pp 335–338Google Scholar
  90. Werner D (1977) The biology of diatoms: botanical monograph, vol 13. University of California Press, BerkeleyGoogle Scholar
  91. Westall F, Walsh MM, Toporski J, Steele A (2003) Fossil biofilms and the search for life on Mars. In: Krumbein WE, Paterson DM, Zavarzin GA (eds) Fossil and recent biofilms. Kluwer Academic Publishers, Dordrecht, pp 447–465CrossRefGoogle Scholar
  92. Whitford LA (1960) The current effect and growth of fresh-water algae. Trans Am Microsc Soc 79:302–309CrossRefGoogle Scholar
  93. Whitford LA, Schumacher GJ (1961) Effect of current on mineral uptake and respiration by a fresh-water alga. Limnol Oceanogr 6:423–425CrossRefGoogle Scholar
  94. Whitford LA, Schumacher GJ (1964) Effect of a current on respiration and mineral uptake in Spirogyra and Oedogonium. Ecology 45:168–170CrossRefGoogle Scholar
  95. Winsborough BM (2000) Diatoms and benthic microbial carbonates. In: Riding RE, Awramik SM (eds) Microbial sediments. Spring, Berlin, pp 76–83CrossRefGoogle Scholar
  96. Wood TA, Murray KR, Burgess JG (2001) Ferrous sulphate oxidation using Thiobacillus ferrooxidans cells immobilized on sand for the purpose of treating acid mine-drainage. Appl Microbiol Biotechnol 56:560–565CrossRefGoogle Scholar
  97. Zimmerman P (1961) Experimentelle untersuchungen über den einfluss der strömungsgeschwindigkeit auf die fliesswasserbiozönose. Internat Verein Limnol 14:396–399Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • S. S. Brake
    • 1
  • I. Arango
    • 2
  • S. T. Hasiotis
    • 3
  • K. R. Burch
    • 1
  1. 1.Department of Earth and Environmental SystemsIndiana State UniversityTerre HauteUSA
  2. 2.Hydrocarbon Charge TeamChevron Energy Technology CompanyHoustonUSA
  3. 3.Department of GeologyUniversity of KansasLawrenceUSA

Personalised recommendations