Skip to main content
Log in

Molecular Characterization and Geological Microenvironment of a Microbial Community Inhabiting Weathered Receding Shale Cliffs

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Shales play an important role in many earth system processes including coastal erosion, and they form the foundations of many engineering structures. The geobiology of the interior of pyrite-containing receding shale cliffs on the coast of northeast England was examined. The surface of the weathered shales was characterised by a thin layer of disordered authigenic iron oxyhydroxides and localised acicular, platy and aggregated gypsum, which was characterised by Raman spectroscopy, XAS and SEM. These chemical changes are likely to play an important role in causing rock weakening along fractures at the micron scale, which ultimately lead to coastal retreat at the larger scale. The surface of the shale hosts a novel, low-diversity microbial community. The bacterial community was dominated by Proteobacteria, with phylotypes closely associating with Methylocella and other members of the γ-subdivision. The second largest phylogenetic group corresponded to Nitrospira. The archaeal 16S rRNA phylotypes were dominated by a single group of sequences that matched phylotypes reported from South African gold mines and possessed ammonia monooxygenase (amoA) genes. Both the phylogenetic and the mineral data show that acidic microenvironments play an important role in shale weathering, but the shale has a higher microbial diversity than previously described pyritic acid mine drainage sites. The presence of a potentially biogeochemically active microbial population on the rock surface suggests that microorganisms may contribute to early events of shale degradation and coastal erosion.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  1. Agar R (1960) Post-glacial erosion of the North Yorkshire coast from the Tees estuary to Ravenscar. Proc Yorkshire Geol Soc 32:409–428

    Article  Google Scholar 

  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  3. Baker BJ, Banfield JF (2003) Microbial communities in acid mine drainage. FEMS Microbiol Ecol 44:139–152

    Article  CAS  PubMed  Google Scholar 

  4. Banwart S, Evans KA, Croxford S (2002) Predicting mineral weathering rates at field scale for mine water risk assessment. Geological Society, London, Special Publications 198:137–157

    Article  CAS  Google Scholar 

  5. Bennett PC, Rogers JR, Choi WJ, Hiebert FK (2001) Silicates, silicate weathering, and microbial ecology. Geomicrobiol J 18:3–19

    Article  CAS  Google Scholar 

  6. Bird E (2000) Coastal geomorphology: an introduction. John Wiley and Sons, Inc, New York

    Google Scholar 

  7. Bolton EW, Berner RA, Petsch ST (2006) The weathering of sedimentary organic matter as a control on atmospheric O2: II. Theoretical modelling. Amer J Sci 306:575–615

    Article  CAS  Google Scholar 

  8. Bowden SA, Farrimond P, Snape CE, Love GD (2006) Compositional differences in biomarker constituents of the hydrocarbon, resin, asphaltene and kerogen fractions: an example from the Jet Rock (Yorkshire, UK). Organic Geochem 37:369–383

    Article  CAS  Google Scholar 

  9. Brown DA, Sherriff BL, Sawicki JA (1997) Microbial transformation of magnetite to hematite. Geochim Cosmochim Acta 61:3341–3348

    Article  CAS  Google Scholar 

  10. Bruce KD, Hiorns WD, Hobman JL, Osborn AM, Strike P, Ritchie DA (1992) Amplification of DNA from native populations of soil bacteria by using the polymerase chain reaction. Appl Environ Microbiol 58:3413–3416

    CAS  PubMed  Google Scholar 

  11. Buneel O, Duran R, Koffi K, Casiot C, Fourçans A, Elbaz-Poulichet F, Personné J-C (2005) Microbial diversity in a pyrite-rich tailings impoundment (Carnoulès, France). Geomicrobiol J 22:249–257

    Article  Google Scholar 

  12. Clark AR, Fort S (2009) Recent UK experience of coastal cliff stabilisation. Proceed Instit Civil Engineers Geotech Engineering 162:49–58

    Google Scholar 

  13. Cockell CS, Kennerley N, Lindstrom M, Watson J, Ragnarsdottir V, Sturkell E, Ott S, Tindle AG (2007) Geomicrobiology of a weathering crust from an impact crater and a hypothesis for its formation. Geomicrobiology J 24:425–440

    Article  CAS  Google Scholar 

  14. Cockell CS, Osinski GR, Howard K, Watson JS (2009) The microbe-mineral environment and gypsum neogenesis in a weathered polar evaporite. Geobiology (in press)

  15. Cole JR, Chai B, Marsh TL, Farris RJ, Wang Q, Kulam SA, Chandra S, McGarrell DM, Schmidt TM, Garrity GM, Tiedje JM (2003) The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31:442–443

    Article  CAS  PubMed  Google Scholar 

  16. Copard Y, Amiotte-Suchet P, Di-Giovanni C (2007) Storage and release of fossil organic carbon related to weathering of sedimentary rocks. Earth Planet Sci Lett 258:345–357

    Article  CAS  Google Scholar 

  17. Coupland K, Johnson DB (2008) Evidence that the potential for dissimilatory ferric ron reduction is widespread among acidophilic heterotrophic bacteria. FEMS Microbiol Lett 279:30–35

    Article  CAS  PubMed  Google Scholar 

  18. Coyne SR, Craw PD, Norwood DA, Ulrich MP (2004) Comparative analysis of the Schliecher and Schuell IsoCode Stix DNA isolation device and the Qiagen QIAamp DNA mini kit. J Clin Microbiol 42:4859–4862

    Article  CAS  PubMed  Google Scholar 

  19. Cruz-Martinez K, Suttle KB, Brodie EL, Power ME, Andersen GL, Banfield JL (2009) Despite strong seasonal responses, soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland. ISME J 3:738–744

    Article  CAS  PubMed  Google Scholar 

  20. Dedysh SN, Kneif C, Dunfield PF (2005) Methylocella species are facultatively methanotrophic. J Bacteriol 187:4665–4670

    Article  CAS  PubMed  Google Scholar 

  21. DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89:5685–5689

    Article  CAS  PubMed  Google Scholar 

  22. Dong H, Kostka JE, Kim J (2003) Microscopic evidence for microbial dissolution of smectite. Clays Clay Miner 51:502–512

    Article  CAS  Google Scholar 

  23. Drever JI, Stillings LL (1997) The role of organic acids in mineral weathering. Colloids Surf, A Physicochem Eng Asp 120:167–181

    Article  CAS  Google Scholar 

  24. Edgcomb VP, McDonald JH, Devereux R, Smith DW (1999) Estimation of bacterial cell numbers in humic acid-rich salt marsh sediments with probes directed to 16S ribosomal DNA. Appl Environ Microbiol 65:1516–1523

    CAS  PubMed  Google Scholar 

  25. Edwards KJ, Screnk MO, Hamers R, Banfield JF (1998) Microbial oxidation of pyrite: experiments using microorganisms from an extreme acidic environment. Am Mineral 83:1444–1453

    CAS  Google Scholar 

  26. Evans KA, Banwart SA (2006) Rate controls on the chemical weathering of natural polymineralic materials. I. Dissolution behavior of polymineralic assemblages determined using batch and unsaturated column experiments. Appl Geochem 21:352–376

    Article  CAS  Google Scholar 

  27. Evans E, Ashley R, Hall J, Penning-Rowsell E, Saul A, Sayers P, Thorne C, Watkinson A (2004) Foresight. Future flooding. Scientific summary: volume I—Future risks and their drivers. Office of Science and Technology, London

    Google Scholar 

  28. Falk H, Lavergren U, Bergback B (2006) Metal mobility in alum shale from Oland, Sweden. J Geochem Explor 90:157–165

    Article  CAS  Google Scholar 

  29. Farges F, Lefrère Y, Rossano S, Berthereau A, Calas G, Brown GE (2004) The effect of redox state on the local structural environment of iron in silicate glasses: a combined XAFS spectroscopy, molecular dynamics, and bond valence study. J Non-Cryst Solids 344:176–188

    Article  CAS  Google Scholar 

  30. Fischer C, Gaupp R (2005) Change of black shale organic material surface area during oxidative weathering: implications for rock-water surface evolution. Geochim Cosmcochim Acta 69:1213–1224

    Article  CAS  Google Scholar 

  31. Floyd M, Czerewko MA, Cripps JC, Spears DA (2003) Pyrite oxidation in Lower Lias Clay at concrete highway structures affected by thaumasite, Gloucestershire, UK. Cem Concr Compos 25:1015–1024

    Article  CAS  Google Scholar 

  32. French PW (2004) The changing nature of, and approaches to, UK coastal managements at the start of the twenty-first century. Geograph J 170:116–125

    Article  Google Scholar 

  33. Gad MA, Gatt JA, Le Riche HH (1969) Geochemistry of the Whitbian (Upper Lias) sediments of the Yorkshire Coast. Proc Yorks Geol Soc 37:105–139

    Article  CAS  Google Scholar 

  34. Galoisy L, Calas G, Arrio MA (2001) High-resolution XANES spectra of iron in minerals and glasses: structural information from the pre-edge region. Chem Geol 174:307–319

    Article  CAS  Google Scholar 

  35. Glowa KR, Arocena JM, Massicotte HB (2003) Extraction of potassium and/or magnesium from selected soil minerals by Piloderma. Geomicrobiol J 20:99–111

    Article  CAS  Google Scholar 

  36. Han B, Chen Y, Abell G, Jiang H, Bodrossy L, Zhao J, Murrell JC, Xing XH (2009) Diversity and activity of methanotrophs in alkaline soil from a Chinese coal mine. FEMS Microbiol Ecol 70:196–207

    Article  CAS  Google Scholar 

  37. He Z, Xiao S, Xie X, Zhong H, Hu Y, Li Q, Gao F, Li G, Liu J, Qiu G (2007) Molecular diversity of microbial community in acid mine drainages of Yunfu sulfide mine. Extremophiles 11:305–314

    Article  CAS  PubMed  Google Scholar 

  38. He J, Shen J, Zhang L, Zhu Y, Zheng Y, Xu M, Di H (2007) Quantitative analyses of the abundance and composition of ammonia-oxidising bacteria and ammonia-oxidising archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol 9:2364–2374

    Article  CAS  PubMed  Google Scholar 

  39. Herrmann M, Saunders AM, Schramm A (2008) Archaea dominate the ammonia-oxidising community in the rhizosphere of the freshwater macrophyte Littorella uniflora. Appl Environ Microbiol 74:3279–3283

    Article  CAS  PubMed  Google Scholar 

  40. Hiebert FK, Bennett PC (1992) Microbial control of silicate weathering in organic-rich ground water. Science 258:278–281

    Article  CAS  PubMed  Google Scholar 

  41. Hovanec TA, Taylor LT, Blakis A, Delong EF (1998) Nitrospira-like bacteria associated with nitrite oxidation in freshwater aquaria. Appl Environ Microbiol 64:258–264

    CAS  PubMed  Google Scholar 

  42. Hurai V, Göttlicher J, Majzlan J, Huraiová M (2008) Contrasting ferric iron contents in conjugate Fe oxide and silicate melts from southern Slovakia determined using micro-XANES spectroscopy. Can Mineral 46:1173–1181

    Article  CAS  Google Scholar 

  43. Joeckel RM, Clement BJA, Van Fleets Bates LR (2005) Sulfate-mineral crusts from pyrite weathering and acid rock drainage in the Dakota formation and Graneros Shale, Jefferson County, Nebraska. Chem Geol 215:433–452

    Article  CAS  Google Scholar 

  44. Kalinowski BE, Liermann LJ, Givens S, Brantley SL (2000) Rates of bacteria-promoted solubilization of Fe from minerals: a review of problems and approaches. Chem Geol 169:357–370

    Article  CAS  Google Scholar 

  45. Kalinowski BE, Oskarsson A, Arlinger J, Odegaard-Jensen A, Andlid T, Pedersen K (2004) Microbial leaching of uranium and other trace elements from shale mine tailings at Ransted. Geoderma 122:177–194

    Article  CAS  Google Scholar 

  46. Kawano M, Tomita K (2001) Microbial biomineralisation in weathered volcanic ash deposit and formation of biogenic minerals by experimental incubation. Am Mineral 86:400–410

    CAS  Google Scholar 

  47. Kennedy CB, Scott SD, Ferris FG (2003) Characterisation of bacteriogenic iron oxide deposits from Axial Volcano, Juan de Fuca Ridge, Northeast Pacific Ocean. Geomicrobiol J 20:199–214

    Article  CAS  Google Scholar 

  48. Kim B-Y, Weon H-Y, Lee K-H, Soek S-J, Kwon S-W, Go S-J, Stackebrandt E (2006) Dyella yeojuensis sp. nov., isolated from greenhouse soil in Korea. Int J Syst Evol Microbiol 56:2079–2082

    Article  CAS  PubMed  Google Scholar 

  49. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  50. Konhauser KO, Schultze-Lam S, Ferris FG, Fyfe WS, Longstaffe FJ, Beveridge TJ (1994) Mineral precipitation by epilithic biofilms in the Speed River, Ontario, Canada. Appl Environ Microbiol 60:549–553

    CAS  PubMed  Google Scholar 

  51. Konhauser KO, Urrutia MM (1999) Bacterial clay authigenesis: a common biogeochemical process. Chem Geol 161:399–413

    Article  CAS  Google Scholar 

  52. Krumholz LR, Harris SH, Sulfita JM (2002) Anaerobic microbial growth from components of Cretaceous shales. Geomicrobiol J 19:593–602

    Article  CAS  Google Scholar 

  53. Kumar S, Dudley J, Nei M, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306

    Article  CAS  PubMed  Google Scholar 

  54. Kussmaul M, Wilimzig M, Bock E (1998) Methanotrophs and methanogens in masonry. Appl Environ Microbiol 64:4530–4532

    CAS  PubMed  Google Scholar 

  55. Lim M, Petley DN, Rosser NJ, Allisom RJ, Long AJ, Pybus D (2005) Combined digital photogrammetry and time-of-flight laser scanning for monitoring cliff evolution. Photogramm Rec 20:109–129

    Article  Google Scholar 

  56. Masselink G, Russell P (2008) Coastal erosion and coastal geomorphology. MCCIP (Marine Climate Group Impacts Partnership) Annual Report Card 2007–2008 Scientific Review, UK

    Google Scholar 

  57. Mendez MO, Neilson JW, Maier RM (2008) Characterisation of a bacterial community in an abandoned semiarid lead-zinc mine tailing site. Appl Environ Microbiol 74:3899–3907

    Article  CAS  PubMed  Google Scholar 

  58. Mosselmans JFW, Quinn PD, Rosell JR, Atkinson KD, Dent AJ, Cavill SI, Hodson ME, Kirk CA, Schofield PF (2008) The first environmental science experiments on the new microfocus spectroscopy beamline at Diamond. Mineral Mag 72:197–200

    Article  CAS  Google Scholar 

  59. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes encoding for 16S rRNA. Appl Environ Microbiol 59:695–700

    CAS  PubMed  Google Scholar 

  60. Nalin R, Simonet P, Vogel TM, Normand P (1999) Rhodanobacter lindaniclasticus gen. nov., sp. nov., a lindane-degrading bacterium. Int J Syst Bacteriol 49:19–23

    Article  PubMed  Google Scholar 

  61. Neff D, Bellot-Gurlet L, Cillmann P, Reguer S, Legrand L (2006) Raman imaging of ancient rust scales on archaeological iron artefacts for long-term atmospheric corrosion mechanisms study. J Raman Spectrosc 37:1228–1237

    Article  CAS  Google Scholar 

  62. Pacheco FAL, Alencoão AMP (2006) Role of fractures in weathering of solid rocks: narrowing the gap between laboratory and field weathering rates. J Hydrol 316:248–265

    Article  Google Scholar 

  63. Phillips DH, Watson DB, Roh Y, Mehlhorn TL, Moon JW, Jardine PM (2006) Distribution of uranium contamination in weathered fractured saprolite/shale and ground water. J Environ Qual 35:1715–1730

    Article  CAS  PubMed  Google Scholar 

  64. Pradhan N, Das B, Acharya S, Kar RN, Sukla SB, Misra VN (2004) Removal of phosphorus from LD slag using a heterotrophic bacterium. Miner Metall Process 21:149–152

    CAS  Google Scholar 

  65. Pye K, Miller JA (1990) Chemical and biochemical weathering of pyritic mudrocks in a shale embankment. Q J Eng Geol 23:365–381

    Article  Google Scholar 

  66. Quince C, Curtis TP, Sloan WT (2008) The rational exploration of microbial diversity. ISME J 2:997–1006

    Article  CAS  PubMed  Google Scholar 

  67. Ravel B, Newville M (2005) ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT. J Synchrotron Radiat 12:537–540

    Article  CAS  PubMed  Google Scholar 

  68. Rosser NJ, Petley DN, Lim M, Dunning SA, Allison RJ (2005) Terrestrial laser scanning for monitoring the process of hard rock coastal cliff erosion. Q J Eng Geol Hydrogeol 38:363–375

    Article  Google Scholar 

  69. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  70. Sakai S, Imachi H, Sekiguchi Y, Ohashi A, Harada H, Kamagata Y (2007) Isolation of key methanogens for global methane emission from rice paddy field: a novel isolate affiliated with a clone cluster, the Rice Cluster 1. Appl Environ Microbiol 73:4326–4331

    Article  CAS  PubMed  Google Scholar 

  71. Santelli CM, Welch SA, Westrich HR, Banfield JF (2001) The effect of Fe-oxidising bacteria on Fe-silicate dissolution. Chem Geol 180:99–115

    Article  CAS  Google Scholar 

  72. Schillawski S, Petsch S (2008) Release of biodegradable dissolved organic matter from ancient sedimentary rocks. Glob Biogeochem Cycle 22:GB3002. doi:10.1029/2007GB002980

    Article  Google Scholar 

  73. Schwieger F, Tebbe CC (1998) A new approach to utilize PCR-single-strand-conformation polymorphism for 16S rRNA gene-based microbial community analysis. Appl Environ Microbiol 64:4870–4876

    CAS  PubMed  Google Scholar 

  74. Schwertmann U, Cornell RM (2008) Iron oxides in the laboratory. Wiley-VCH, Weinheim, Germany

    Google Scholar 

  75. Stein LY, La Duc MT, Grundl TJ, Nealson KH (2001) Bacterial and archaeal populations associated with freshwater ferromanganous micronodules and sediments. Environ Microbiol 3:10–18

    Article  CAS  PubMed  Google Scholar 

  76. Steward HE, Cripps JC (1983) Some engineering implications of chemical weathering of pyritic shale. Q J Eng Geol London 16:281–289

    Article  Google Scholar 

  77. Swensen B, Bakken LR (1999) Release of fossil methane from mineral soil particles and its implication for estimation of methane oxidation in a mineral subsoil. Biogeochemistry 47:1–14

    CAS  Google Scholar 

  78. Swings J (2006) The genus Frateuria. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 844–845

    Chapter  Google Scholar 

  79. Takai K, Moser DP, DeFlaun M, Onstott T, Fredrickson JK (2001) Archaeal diversity in waters from deep South African gold mines. Appl Environ Microbiol 67:5750–5760

    Article  CAS  PubMed  Google Scholar 

  80. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  Google Scholar 

  81. Torsvik VL, Goksoyr J (1978) Determination of bacterial DNA in soil. Soil Bio Biochem 10:7–11

    Article  Google Scholar 

  82. Ullman WJ, Kirchman DL, Welch SA, Vandevivere P (1996) Laboratory evidence for microbially mediated silicate mineral dissolution in nature. Chem Geol 132:11–17

    Article  CAS  Google Scholar 

  83. Uroz S, Calvaruso C, Turpault MP, Frey-Klett P (2009) Mineral weathering by bacteria: ecology, actors and mechanisms. Trends Microbiol 17:378–387

    Article  CAS  PubMed  Google Scholar 

  84. Varadachari C, Barman AK, Ghosh K (1994) Weathering of silicate minerals by organic acids II. Nature of residual products. Geoderma 61:251–268

    Article  CAS  Google Scholar 

  85. Welch SA, Barker WW, Banfield JF (1999) Microbial extracellular polysaccharides and plagioclase dissolution. Geochim Cosmochim Acta 63:1405–1419

    Article  CAS  Google Scholar 

  86. Wilke M, Farges F, Petit P-E, Brown GE, Martin F (2001) Oxidation state and coordination of Fe in minerals: an Fe K-XANES spectroscopic study. Am Mineral 86:714–730

    CAS  Google Scholar 

  87. Wilke M, Partzsch GM, Bernhardt R, Lattard D (2004) Determination of the iron oxidation state in basaltic glasses using XANES at the K-edge. Chem Geol 213:71–87

    Article  CAS  Google Scholar 

  88. Yu Y, Wan M, Shi W, Hong P, Qiu G, Zhou J, Liu X (2007) Bacterial diversity and community structure in acid mine drainage from Dabaoshan Mine, China. Aquat Microb Ecol 47:141–151

    Article  Google Scholar 

  89. Yu Y, Breitbart M, McNairnie P, Rohwer F (2006) FastGroupII: a web-based bioinformatics platform for analyses of large 16S rDNA libraries. BMC Bioinformatics 7:57

    Article  PubMed  Google Scholar 

  90. Xie XH, Xiao SM, Liu JS (2009) Microbial communities in acid mine drainage and their interaction with pyrite surface. Curr Microbiol 59:71–77

    Article  CAS  PubMed  Google Scholar 

  91. Zoppi A, Lofrumento C, Castellucci E, Migliorini MG (2005) The Raman spectrum of hematite: possible indicator for compositional or firing distinction among Terra Sigillata wares. Ann Chim 95:239–246

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Cleveland Potash Ltd. for financial support for this work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Charles S. Cockell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cockell, C.S., Pybus, D., Olsson-Francis, K. et al. Molecular Characterization and Geological Microenvironment of a Microbial Community Inhabiting Weathered Receding Shale Cliffs. Microb Ecol 61, 166–181 (2011). https://doi.org/10.1007/s00248-010-9730-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-010-9730-6

Keywords

Navigation