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The Snotty and the Stringy: Energy for Subsurface Life in Caves

  • Daniel S. JonesEmail author
  • Jennifer L. Macalady
Chapter
Part of the Advances in Environmental Microbiology book series (AEM, volume 1)

Abstract

Caves are subterranean environments that support life largely in the absence of light. Because caves are completely or almost completely removed from the photosynthetic productivity of the sunlit realm, most cave ecosystems are supported either by inputs of organic matter from the surface or by in situ sources of inorganic chemical energy. The majority of caves have very low energy and nutrient availability and thus, generally low biological activity and productivity. However, those caves that have abundant inorganic chemical energy or high organic carbon influx represent subterranean oases that support robust microbial communities and diverse animal life. In this chapter, we review the energy resources available to cave microbiota and describe several examples that illustrate the vast diversity of subsurface habits contained within caves.

Keywords

Ferromanganese Crust Lava Tube Cave Environment Acidithiobacillus Thiooxidans Cave Stream 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We would like to extend gratitude to everyone who has assisted and supported our cave microbiology research, especially to Alessandro Montanari for continued logistical support and the use of facilities at the Osservatorio Geologico di Coldigioco and to S. Carnevali, S. Cerioni, S. Galdenzi, M. Mainiero, S. Mariani, and the Gruppo Speleologico C.A.I. di Fabriano for technical support and scientific discussions in Italy. We also thank L. Hose, L. Rosales-Lagarde, I. Schaperdoth, S. Dattagupta, E. Lyon, T. Jones, K. Dawson, and R. McCauley for assistance in the field and lab. Our work has been supported by generous funding from the National Science Foundation, the NASA Astrobiology Institute, the Cave Conservancy Foundation, and the Marche Regional Government and the Marche Speleologic Federation. Special thanks to C. Hurst for organizing and editing this volume.

References

  1. Amend JP, Teske A (2005) Expanding frontiers in deep subsurface microbiology. Palaeogeogr Palaeocl 219(1):131–155CrossRefGoogle Scholar
  2. Anelli F, Graniti A (1967) Aspetti microbiologici nella genesi delle vermicolazioni argillose delle Grotte di Castellana (Murge di Bari). Le Grotte d‚ Italia Ser 4:131–138Google Scholar
  3. Angert ER, Northup DE, Reysenbach A-L, Peek AS, Goebel BM, Pace NR (1998) Molecular phylogenetic analysis of a bacterial community in Sulphur River, Parker Cave, Kentucky. Am Mineral 83:1583–1592CrossRefGoogle Scholar
  4. Azúa-Bustos A, González-Silva C, Mancilla R, Salas L, Palma R, Wynne J, McKay C, Vicuña R (2009) Ancient photosynthetic eukaryote biofilms in an Atacama Desert coastal cave. Microb Ecol 58(3):485–496PubMedCrossRefGoogle Scholar
  5. Barton HA, Jurado V (2007) What’s up down there? Microbial diversity in caves. Microbe 3:132–138Google Scholar
  6. Barton HA, Taylor NM, Kreate MP, Springer AC, Oehrle SA, Bertog JL (2007) The impact of host rock geochemistry on bacterial community structure in oligotrophic cave environments. Int J Speleol 36(2):93–104CrossRefGoogle Scholar
  7. Bini A, Gori MC, Gori S (1978) A critical review of hypotheses on the origin of vermiculations. Int J Speleol 10(1):11–34CrossRefGoogle Scholar
  8. Blyth AJ, Frisia S (2008) Molecular evidence for bacterial mediation of calcite formation in cold high-altitude caves. Geomicrobiol J 25(2):101–111CrossRefGoogle Scholar
  9. Borsato A, Frisia S, Jones B, Van Der Borg K (2000) Calcite moonmilk: crystal morphology and environment of formation in caves in the Italian Alps. J Sediment Res 70(5):1179–1190CrossRefGoogle Scholar
  10. Boston P, Spilde M, Northup D, Melim L, Soroka D, Kleina L, Lavoie K, Hose L, Mallory L, Dahm C, Crossey L, Schelble R (2001) Cave biosignature suites: microbes, minerals, and Mars. Astrobiology 1(1):25–55PubMedCrossRefGoogle Scholar
  11. Boston P, Curnutt J, Gomez E, Schubert K, Strader B (2009) Patterned growth in extreme environments. In: Proceedings of the third IEEE international conference on space mission challenges for information technology, Citeseer, pp 221–226Google Scholar
  12. Brigmon R, Martin H, Morris T, Bitton G, Zam S (1994) Biogeochemical ecology of Thiothrix spp. in underwater limestone caves. Geomicrobiol J 12(3):141–159CrossRefGoogle Scholar
  13. Bullen HA, Oehrle SA, Bennett AF, Taylor NM, Barton HA (2008) Use of attenuated total reflectance Fourier transform infrared spectroscopy to identify microbial metabolic products on carbonate mineral surfaces. Appl Environ Microbiol 74(14):4553–4559PubMedPubMedCentralCrossRefGoogle Scholar
  14. Cacchio P, Contento R, Ercole C, Cappuccio G, Martinez MP, Lepidi A (2004) Involvement of microorganisms in the formation of carbonate speleothems in the Cervo Cave (L’Aquila-Italy). Geomicrobiol J 21(8):497–509CrossRefGoogle Scholar
  15. Camassa MM, Febbroriello P (2003) Le foval della grotta zinzulusa in Puglia (SE-Italia). Thalassia Salent 26:207–218Google Scholar
  16. Cañaveras J, Hoyos M, Sanchez-Moral S, Sanz-Rubio E, Bedoya J, Soler V, Groth I, Schumann P, Laiz L, Gonzalez I (1999) Microbial communities associated with hydromagnesite and needle-fiber aragonite deposits in a karstic cave (Altamira, Northern Spain). Geomicrobiol J 16(1):9–25CrossRefGoogle Scholar
  17. Cañaveras JV, Sloer C, Saiz-Jimenez J (2001) Microorganisms and microbially induced fabrics in cave walls. Geomicrobiol J 18(3):223–240CrossRefGoogle Scholar
  18. Cañaveras J, Cuezva S, Sanchez-Moral S, Lario J, Laiz L, Gonzalez JM, Saiz-Jimenez C (2006) On the origin of fiber calcite crystals in moonmilk deposits. Naturwissenschaften 93(1):27–32PubMedCrossRefGoogle Scholar
  19. Cardman Z, Macalady JL, Schaperdoth I, Broad K, Kakuk B (2015) Fast-growing slime curtains reveal a dynamic nitrogen (and iron?) world in the shallow subsurface. Geological Society of America Abstracts with Programs, Vol 47, No. 7, p 56Google Scholar
  20. Carmichael MJ, Carmichael SK, Santelli CM, Strom A, Bräuer SL (2013) Mn (II)-oxidizing bacteria are abundant and environmentally relevant members of ferromanganese deposits in caves of the upper Tennessee River Basin. Geomicrobiol J 30(9):779–800CrossRefGoogle Scholar
  21. Chen Y, Wu L, Boden R, Hillebrand A, Kumaresan D, Moussard H, Baciu M, Lu Y, Murrell JC (2009) Life without light: microbial diversity and evidence of sulfur-and ammonium-based chemolithotrophy in Movile Cave. ISME J 3(9):1093–1104PubMedCrossRefGoogle Scholar
  22. Chroňáková A, Horák A, Elhottová D, Krištůfek V (2009) Diverse archaeal community of a bat guano pile in Domica Cave (Slovak Karst, Slovakia). Folia Microbiol 54(5):436–446CrossRefGoogle Scholar
  23. Contos A, James J, Pitt BHK, Rogers P (2001) Morphoanalysis of bacterially precipitated subaqueous calcium carbonate from Weebubbie Cave, Australia. Geomicrobiol J 18(3):331–343CrossRefGoogle Scholar
  24. Culver DC, Pipan T (2009) The biology of caves and other subterranean habitats. Oxford University Press, OxfordGoogle Scholar
  25. Culver DC, Sket B (2000) Hotspots of subterranean biodiversity in caves and wells. J Cave Karst Stud 62(1):11–17Google Scholar
  26. Cunningham K, Northup D, Pollastro R, Wright W, LaRock E (1995) Bacteria, fungi and biokarst in Lechuguilla Cave, Carlsbad Caverns National Park, New Mexico. Environ Geol 25(1):2–8CrossRefGoogle Scholar
  27. Danielli H, Edington M (1983) Bacterial calcification in limestone caves. Geomicrobiol J 3(1):1–16CrossRefGoogle Scholar
  28. Dattagupta S, Schaperdoth I, Montanari A, Mariani S, Kita N, Valley JW, Macalady JL (2009) A novel symbiosis between chemoautotrophic bacteria and a freshwater cave amphipod. ISME J 3(8):935–943PubMedCrossRefGoogle Scholar
  29. Davis DG (2000) Extraordinary features of Lechuguilla Cave, Guadalupe Mountains, New Mexico. J Cave Karst Stud 62(2):147–157Google Scholar
  30. Dupraz C, Visscher PT (2005) Microbial lithification in marine stromatolites and hypersaline mats. Trends Microbiol 13(9):429–438PubMedCrossRefGoogle Scholar
  31. Engel AS (2010) Microbial diversity of cave ecosystems. In: Barton LL, Mandl M, Loy A (eds) Geomicrobiology. Molecular and Environmental Perspective. Springer, Netherlands, pp 219–238CrossRefGoogle Scholar
  32. Engel AS, Northup DE (2008) Caves and karst as model systems for advancing the microbial sciences. In: Martin JB, White WB (eds) Frontiers of Karst Research: Proceedings and recommendations of the workshop held May 3 through 5, 2007, in San Antonio, TX. Karst Waters Institute, Ashland, OHGoogle Scholar
  33. Engel AS, Randall KW (2011) Experimental evidence for microbially mediated carbonate dissolution from the saline water zone of the Edwards Aquifer, central Texas. Geomicrobiol J 28(4):313–327CrossRefGoogle Scholar
  34. Engel AS, Porter ML, Kinkle BK, Kane TC (2001) Ecological assessment and geological significance of microbial communities from Cesspool Cave, Virginia. Geomicrobiol J 18(3):259–274CrossRefGoogle Scholar
  35. Engel AS, Lee N, Porter ML, Stern LA, Bennett PC, Wagner M (2003) Filamentous “Epsilonproteobacteria” dominate microbial mats from sulfidic cave springs. Appl Environ Microbiol 69(9):5503–5511PubMedPubMedCentralCrossRefGoogle Scholar
  36. Engel AS, Stern LA, Bennett PC (2004) Microbial contributions to cave formation: new insights into sulfuric acid speleogenesis. Geology 32(5):369–372CrossRefGoogle Scholar
  37. Engel AS, Meisinger DB, Porter ML, Payn RA, Schmid M, Stern LA, Schleifer K, Lee NM (2010) Linking phylogenetic and functional diversity to nutrient spiraling in microbial mats from Lower Kane Cave (USA). ISME J 4(1):98–110PubMedCrossRefGoogle Scholar
  38. Engel AS, Paoletti MG, Beggio M, Dorigo L, Pamio A, Gomiero T, Furlan C, Brilli M, Dreon AL, Bertoni R (2013) Comparative microbial community composition from secondary 1 carbonate (moonmilk) deposits: implications for the Cansiliella servadeii cave hygropetric food web. Int J Speleol 42(3):181–192CrossRefGoogle Scholar
  39. Faimon J, Štelcl J, Kubešová S, Zimák J (2003) Environmentally acceptable effect of hydrogen peroxide on cave “lamp-flora”, calcite speleothems and limestones. Environ Pollut 122(3):417–422PubMedCrossRefGoogle Scholar
  40. Ford DC, Williams PW (2007) Karst hydrogeology and geomorphology. Wiley, West Sussex, EnglandCrossRefGoogle Scholar
  41. Galdenzi S (1990) Un modello genetico per la Grotta Grande del Vento. In: Galdenzi S, Menichetti M (eds) Il carsismo della Gola di Frasassi: Memorie Istituto Italiano di Speologia, vol 4. vol 2, pp 123–142Google Scholar
  42. Galdenzi S, Maruoka T (2003) Gypsum deposits in the Frasassi Caves, central Italy. J Cave Karst Stud 65(2):111–125Google Scholar
  43. Galdenzi S, Sarbu S (2000) Chemiosintesi e speleogenesi in un ecosistema ipogeo: I Rami Sulfurei delle Grotte di Frasassi (Italia centrale). Le Grotte d’Italia 1:3–18Google Scholar
  44. Galdenzi S, Cocchioni F, Filipponi G, Morichetti L, Scuri S, Selvaggio R, Cocchioni M (2010) The sulfidic thermal caves of Acquasanta Terme (central Italy). J Cave Karst Stud 72(1):43–58CrossRefGoogle Scholar
  45. Giordano M, Mobili F, Pezzoni V, Hein MK, Davis JS (2000) Photosynthesis in the caves of Frasassi (Italy). Phycologia 39(5):384–389CrossRefGoogle Scholar
  46. Gradziński M, Banaś M, Uchman A (1995) Biogenic origin of manganese flowstones from Jaskinia Czarna Cave, Tatra Mts., Western Carpathians. Acta Soc Geol Pol 65:19–27Google Scholar
  47. Halliday WR (2007) Pseudokarst in the 21st century. J Cave Karst Stud 69(1):103–113Google Scholar
  48. Hathaway JJM, Garcia MG, Balasch MM, Spilde MN, Stone FD, Dapkevicius MDLN, Amorim IR, Gabriel R, Borges PA, Northup DE (2014) Comparison of bacterial diversity in Azorean and Hawai’ian lava cave microbial mats. Geomicrobiol J 31(3):205–220CrossRefGoogle Scholar
  49. Head IM, Jones DM, Larter SR (2003) Biological activity in the deep subsurface and the origin of heavy oil. Nature 426(6964):344–352PubMedCrossRefGoogle Scholar
  50. Hedges J (1993) A review on vermiculations. Bol Soc Venezolana Espeleol 27:2–6Google Scholar
  51. Hill C (1995) Sulfur redox reactions: hydrocarbons, native sulfur, Mississippi Valley-type deposits, and sulfuric acid karst in the Delaware Basin, New Mexico and Texas. Environ Geol 25(1):16–23CrossRefGoogle Scholar
  52. Hill CA, Forti P (1997) Cave minerals of the world, vol 238. National Speleological Society, Huntsville, ALGoogle Scholar
  53. Holmes AJ, Tujula NA, Holley M, Contos A, James JM, Rogers P, Gillings MR (2001) Phylogenetic structure of unusual aquatic microbial formations in Nullarbor caves, Australia. Environ Microbiol 3(4):256–264PubMedCrossRefGoogle Scholar
  54. Hose L, Northup D (2004) Biovermiculations: living vermiculation-like deposits in Cueva de Villa Luz, Mexico: Proceedings of the Society: Selected Abstracts, National Speleological Society Convention, Marquette, MI. J Cave Karst Stud 66:112Google Scholar
  55. Hose LD, Pisarowicz JA (1999) Cueva de Villa Luz, Tabasco, Mexico: Reconnaissance study of an active sulfur spring cave and ecosystem. J Cave Karst Stud 61(1):13–21Google Scholar
  56. Hose LD, Palmer AN, Palmer MV, Northup DE, Boston PJ, DuChene HR (2000) Microbiology and geochemistry in a hydrogen-sulfide-rich karst environment. Chem Geol 169:399–423CrossRefGoogle Scholar
  57. Hutchens E, Radajewski S, Dumont MG, McDonald IR, Murrell JC (2004) Analysis of methanotrophic bacteria in Movile Cave by stable isotope probing. Environ Microbiol 6(2):111–120PubMedCrossRefGoogle Scholar
  58. Jones B (1992) Manganese precipitates in the karst terrain of Grand Cayman, British West Indies. Can J Earth Sci 29(6):1125–1139CrossRefGoogle Scholar
  59. Jones B (2001) Microbial activity in caves—a geological perspective. Geomicrobiol J 18(3):345–357CrossRefGoogle Scholar
  60. Jones B (2010) Microbes in caves: agents of calcite corrosion and precipitation. Geol Soc Lond, Spec Publ 336(1):7–30CrossRefGoogle Scholar
  61. Jones DS, Polerecky L, Dempsey BA, Galdenzi S, Macalady JL (2015) Fate of sulfide in the Frasassi cave system and implications for sulfuric acid speleogenesis. Chem Geol 410:21CrossRefGoogle Scholar
  62. Jones DS, Lyon EH, Macalady JL (2008) Geomicrobiology of biovermiculations from the Frasassi cave system, Italy. J Cave Karst Stud 70(2):78–93Google Scholar
  63. Jones D, Tobler D, Schaperdoth I, Mainiero M, Macalady J (2010) Community structure of subsurface biofilms in the thermal sulfidic caves of Acquasanta Terme, Italy. Appl Environ Microbiol 76(17):5902–5910PubMedPubMedCentralCrossRefGoogle Scholar
  64. Jones D, Albrecht H, Dawson K, Schaperdoth I, Freeman K, Pi Y, Pearson A, Macalady J (2012) Community genomic analysis of an extremely acidophilic sulfur-oxidizing biofilm. ISME J 6(1):158–170PubMedPubMedCentralCrossRefGoogle Scholar
  65. Jones DS, Schaperdoth I, Macalady JL (2014) Metagenomic evidence for sulfide oxidation in extremely acidic cave biofilms. Geomicrobiol J 31:194–204CrossRefGoogle Scholar
  66. Jørgensen BB (1982) Mineralization of organic matter in the sea bed—the role of sulphate reduction. Nature 296:643–645CrossRefGoogle Scholar
  67. Laiz L, Groth I, Gonzalez I, Sáiz-Jiménez C (1999) Microbiological study of the dripping waters in Altamira cave (Santillana del Mar, Spain). J Microbiol Methods 36(1):129–138PubMedCrossRefGoogle Scholar
  68. Lavoie K, Northup D (2009) Invertebrate colonization and deposition rates of guano in a man-made bat cave, the Chiroptorium, Texas USA. Int Cong Speleol Proc 2:1297–1301Google Scholar
  69. Lee NM, Meisinger DB, Aubrecht IR, Kovačik L, Saiz-Jimenez C, Baskar S, Baskar R, Liebl W, Porter ML, Engel AS (2012) Caves and Karst environments. In: Bell EM (ed) Life at extremes: environments, organisms, and strategies for survival, vol 1. CAB International, Oxfordshire, UK, pp 320–344CrossRefGoogle Scholar
  70. Léveillé RJ, Datta S (2010) Lava tubes and basaltic caves as astrobiological targets on Earth and Mars: a review. Plan Space Sci 58(4):592–598CrossRefGoogle Scholar
  71. Lin L-H, Wang P-L, Rumble D, Lippmann-Pipke J, Boice E, Pratt LM, Lollar BS, Brodie EL, Hazen TC, Andersen GL (2006) Long-term sustainability of a high-energy, low-diversity crustal biome. Science 314(5798):479–482PubMedCrossRefGoogle Scholar
  72. Lowe D, Gunn J (1995) The role of strong acid in speleo-inception and subsequent cave development. Acta Geographica 34:33–60Google Scholar
  73. Lyon E, Koffman B, Meyer K, Cleaveland L, Mariani S, Galdenzi S, Macalady J (2005) Geomicrobiology of the Frasassi Caves. In: Galdenzi S (ed) Frasassi 1989-2004: Gli sviluppi nella ricerca, pp 152–157Google Scholar
  74. Macalady JL, Lyon EH, Koffman B, Albertson LK, Meyer K, Galdenzi S, Mariani S (2006) Dominant microbial populations in limestone-corroding stream biofilms, Frasassi cave system, Italy. Appl Environ Microbiol 72(8):5596–5609PubMedPubMedCentralCrossRefGoogle Scholar
  75. Macalady JL, Jones DS, Lyon EH (2007) Extremely acidic, pendulous microbial biofilms from the Frasassi cave system, Italy. Environ Microbiol 9(6):1402–1414PubMedCrossRefGoogle Scholar
  76. Macalady J, Jones D, Schaperdoth I, Bloom D, McCauley R (2008a) Meter-long microbial ropes from euxinic cave lakes. In: AGU Fall Meeting Abstracts, p 0514Google Scholar
  77. Macalady JL, Dattagupta S, Schaperdoth I, Jones DS, Druschel GK, Eastman D (2008b) Niche differentiation among sulfur-oxidizing bacterial populations in cave waters. ISME J 2(6):590–601PubMedCrossRefGoogle Scholar
  78. Macalady JL, Hamilton TL, Grettenberger CL, Jones DS, Tsao LE, Burgos WD (2013) Energy, ecology and the distribution of microbial life. Phil Trans R Soc B 368(1622):20120383PubMedPubMedCentralCrossRefGoogle Scholar
  79. Mariani S, Mainiero M, Barchi M, Van Der Borg K, Vonhof H, Montanari A (2007) Use of speleologic data to evaluate Holocene uplifting and tilting: an example from the Frasassi anticline (northeastern Apennines, Italy). Earth Planet Sci Lett 257(1–2):313–328CrossRefGoogle Scholar
  80. McCauley R, Jones D, Schaperdoth I, Steinberg L, Macalady J (2010) Metabolic strategies in energy-limited microbial communities in the anoxic subsurface (Frasassi Cave System, Italy). In: AGU Fall Meeting Abstracts, p 0317Google Scholar
  81. Meisinger DB, Zimmermann J, Ludwig W, Schleifer KH, Wanner G, Schmid M, Bennett PC, Engel AS, Lee NM (2007) In situ detection of novel Acidobacteria in microbial mats from a chemolithoautotrophically based cave ecosystem (Lower Kane Cave, WY, USA). Environ Microbiol 9(6):1523–1534PubMedCrossRefGoogle Scholar
  82. Melim LA (2011) Stable isotopic evidence for microbial precipitation of calcite in cave pool fingers. Geological Society of America Abstracts with Programs 43(5):329Google Scholar
  83. Melim LA, Shinglman KM, Boston PJ, Northup DE, Spilde MN, Queen JM (2001) Evidence for microbial involvement in pool finger precipitation, Hidden Cave, New Mexico. Geomicrobiol J 18(3):311–329CrossRefGoogle Scholar
  84. Melim LA, Northup DE, Spilde MN, Jones B, Boston PJ, Bixby RJ (2008) Reticulated filaments in cave pool speleothems: microbe or mineral? J Cave Karst Stud 70(3):135–141Google Scholar
  85. Melim L, Liescheidt R, Northup D, Spilde M, Boston P, Queen J (2009) A biosignature suite from cave pool precipitates, Cottonwood Cave, New Mexico. Astrobiology 9(9):907–917PubMedCrossRefGoogle Scholar
  86. Montechiaro F, Giordano M (2006) Effect of prolonged dark incubation on pigments and photosynthesis of the cave-dwelling cyanobacterium Phormidium autumnale (Oscillatoriales, Cyanobacteria). Phycologia 45(6):704–710CrossRefGoogle Scholar
  87. Northup DE, Lavoie KH (2001) Geomicrobiology of caves: a review. Geomicrobiol J 18(3):199–222CrossRefGoogle Scholar
  88. Northup DE, Dahm CN, Melim LA, Spilde MN, Crossey LJ, Lavoie KH, Mallory LM, Boston PJ, Cunningham KI, Barns SM (2000) Evidence for geomicrobiological interactions in Guadalupe caves. J Cave Karst Stud 62(2):80–90Google Scholar
  89. Northup DE, Barns SM, Yu LE, Spilde MN, Schelble RT, Dano KE, Crossey LJ, Connolly CA, Boston PJ, Natvig DO (2003) Diverse microbial communities inhabiting ferromanganese deposits in Lechuguilla and Spider Caves. Environ Microbiol 5(11):1071–1086PubMedCrossRefGoogle Scholar
  90. Northup D, Melim L, Spilde M, Hathaway J, Garcia M, Moya M, Stone F, Boston P, Dapkevicius M, Riquelme C (2011) Lava cave microbial communities within mats and secondary mineral deposits: implications for life detection on other planets. Astrobiology 11(7):601–618PubMedPubMedCentralCrossRefGoogle Scholar
  91. Orsi WD, Edgcomb VP, Christman GD, Biddle JF (2013) Gene expression in the deep biosphere. Nature 499(7457):205–208PubMedCrossRefGoogle Scholar
  92. Ortiz M, Legatzki A, Neilson JW, Fryslie B, Nelson WM, Wing RA, Soderlund CA, Pryor BM, Maier RM (2014) Making a living while starving in the dark: metagenomic insights into the energy dynamics of a carbonate cave. ISME J 8(2):478–491PubMedPubMedCentralCrossRefGoogle Scholar
  93. Palmer AN (1991) Origin and morphology of limestone caves. Geol Soc Am Bull 103(1):1–21CrossRefGoogle Scholar
  94. Palmer AN (2007) Cave geology. Cave Books, Dayton, OHGoogle Scholar
  95. Pašić L, Kovče B, Sket B, Herzog‐Velikonja B (2010) Diversity of microbial communities colonizing the walls of a Karstic cave in Slovenia. FEMS Microbiol Ecol 71(1):50–60PubMedCrossRefGoogle Scholar
  96. Peck S (1986) Bacterial deposition of iron and manganese oxides in North American caves. NSS Bull 48(1):26–30Google Scholar
  97. Pedersen K (2000) Exploration of deep intraterrestrial microbial life: current perspectives. FEMS Microbiol Lett 185(1):9–16PubMedCrossRefGoogle Scholar
  98. Popa R, Smith AR, Popa R, Boone J, Fisk M (2012) Olivine-respiring bacteria isolated from the rock-ice interface in a lava-tube cave, a Mars analog environment. Astrobiology 12(1):9–18PubMedPubMedCentralCrossRefGoogle Scholar
  99. Por FD (2007) Ophel: a groundwater biome based on chemoautotrophic resources. The global significance of the Ayyalon cave finds. Israel Hydrobiol 592(1):1–10CrossRefGoogle Scholar
  100. Porca E, Jurado V, Žgur‐Bertok D, Saiz‐Jimenez C, Pašić L (2012) Comparative analysis of yellow microbial communities growing on the walls of geographically distinct caves indicates a common core of microorganisms involved in their formation. FEMS Microbiol Ecol 81(1):255–266PubMedCrossRefGoogle Scholar
  101. Portillo MC, Gonzalez JM (2011) Moonmilk deposits originate from specific bacterial communities in Altamira Cave (Spain). Microb Ecol 61(1):182–189PubMedCrossRefGoogle Scholar
  102. Rossi C, Lozano RP, Isanta N, Hellstrom J (2010) Manganese stromatolites in caves: El Soplao (Cantabria, Spain). Geology 38(12):1119–1122CrossRefGoogle Scholar
  103. Rossmassler K, Engel AS, Twing KI, Hanson TE, Campbell BJ (2012) Drivers of epsilonproteobacterial community composition in sulfidic caves and springs. FEMS Microbiol Ecol 79(2):421–432PubMedCrossRefGoogle Scholar
  104. Sarbu S, Kinkle B, Vlasceanu L, Kane T, Popa R (1994) Microbiological characterization of a sulfide‐rich groundwater ecosystem. Geomicrobiol J 12(3):175–182CrossRefGoogle Scholar
  105. Sarbu SM, Kane TC, Kinkle BK (1996) A chemoautotrophically based cave ecosystem. Science 272(5270):1953–1955PubMedCrossRefGoogle Scholar
  106. Secord D, Muller-Parker G (2005) Symbiont distribution along a light gradient within an intertidal cave. Limnol Oceanogr 50(1):272–278CrossRefGoogle Scholar
  107. Shabarova T, Widmer F, Pernthaler J (2013) Mass effects meet species sorting: transformations of microbial assemblages in epiphreatic subsurface karst water pools. Environ Microbiol 15(9):2476–2488PubMedCrossRefGoogle Scholar
  108. Simon KS, Benfield EF (2002) Ammonium retention and whole-stream metabolism in cave streams. Hydrobiologia 482(1–3):31–39CrossRefGoogle Scholar
  109. Simon K, Benfield E, Macko S (2003) Food web structure and the role of epilithic biofilms in cave streams. Ecology 84(9):2395–2406CrossRefGoogle Scholar
  110. Simon KS, Pipan T, Culver DC (2007) A conceptual model of the flow and distribution of organic carbon in caves. J Cave Karst Stud 69(2):279–284Google Scholar
  111. Smith T, Olson R (2007) A taxonomic survey of lamp flora (Algae and Cyanobacteria) in electrically lit passages within Mammoth Cave National Park, Kentucky. Int J Speleol 36(2):105–114CrossRefGoogle Scholar
  112. Spear JR, Barton HA, Robertson CE, Francis CA, Pace NR (2007) Microbial community biofabrics in a geothermal mine adit. Appl Environ Microbiol 73(19):6172–6180PubMedPubMedCentralCrossRefGoogle Scholar
  113. Spilde MN, Northup DE, Boston PJ, Schelble RT, Dano KE, Crossey LJ, Dahm CN (2005) Geomicrobiology of cave ferromanganese deposits: a field and laboratory investigation. Geomicrobiol J 22(3-4):99–116CrossRefGoogle Scholar
  114. Steinhauer ES, Omelon CR, Bennett PC (2010) Limestone corrosion by neutrophilic sulfur-oxidizing bacteria: a coupled microbe-mineral system. Geomicrobiol J 27(8):723–738CrossRefGoogle Scholar
  115. Strader B, Schubert K, Quintana M, Gomez E, Curnutt J, Boston P (2011) Estimation, modeling, and simulation of patterned growth in extreme environments. In: Software tools and algorithms for biological systems. Springer, pp 157–170Google Scholar
  116. Teske AP (2005) The deep subsurface biosphere is alive and well. Trends Microbiol 13(9):402–404PubMedCrossRefGoogle Scholar
  117. Tetu SG, Breakwell K, Elbourne LD, Holmes AJ, Gillings MR, Paulsen IT (2013) Life in the dark: metagenomic evidence that a microbial slime community is driven by inorganic nitrogen metabolism. ISME J 7:1227–1236PubMedPubMedCentralCrossRefGoogle Scholar
  118. Vlasceanu L, Sarbu SM, Engel AS, Kinkle BK (2000) Acidic cave-wall biofilms located in the Frasassi Gorge, Italy. Geomicrobiol J 17(2):125–139CrossRefGoogle Scholar
  119. White WB (1988) Geomorphology and hydrology of karst terrains. Oxford University Press, New YorkGoogle Scholar
  120. White WB, Vito C, Scheetz BE (2009) The mineralogy and trace element chemistry of black manganese oxide deposits from caves. J Cave Karst Stud 71(2):136–143Google Scholar
  121. Whiticar MJ, Faber E, Schoell M (1986) Biogenic methane formation in marine and freshwater environments: CO2 reduction vs acetate fermentation—Isotope evidence. Geochim Cosmochim Acta 50(5):693–709CrossRefGoogle Scholar
  122. Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci USA 95(12):6578–6583PubMedPubMedCentralCrossRefGoogle Scholar
  123. Wigley T, Plummer L (1976) Mixing of carbonate waters. Geochim Cosmochim Acta 40(9):989–995CrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Earth SciencesUniversity of MinnesotaMinneapolisUSA
  2. 2.Department of GeosciencesPenn State UniversityUniversity ParkUSA

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