The Microbial Diversity of Caves

  • Olivia S. Hershey
  • Hazel A. BartonEmail author
Part of the Ecological Studies book series (ECOLSTUD, volume 235)


Oligotrophic caves represent an important environment for studying microbial community adaptation, where diversity is likely driven by available energy and nutrient sources, from the heterotrophic breakdown of scant allochthonous organic carbon delivered by vadose-zone groundwater to autotrophic growth using in situ redox-active compounds. While historically cave microbiology was based on cultivation approaches, the inherent bias of such techniques provided an incomplete view of cave diversity. Modern molecular techniques demonstrate that microbial populations in caves are remarkably diverse and demonstrate both community and organismal adaptations to the resource limitation of the subsurface. While most studies in caves have focused on the role and diversity of bacterial populations, the fungi and archaea also appear to play important roles in community structure and energetics, albeit at polar ends of the nutrient spectrum. Together these data suggest that current cave microbiology research is starting to reveal the potential for a cave microbiome that represents the core of microbial diversity in caves.



The authors would like to thank Dr. Raina Maier for access to sequencing data, Drs. Soumya Ghosh and Naowarat Cheeptham in compiling the list of international research groups, and Dr. Max Wisshak for the SEM images used in Fig. 5.8.


  1. Adey A, Morrison HG, Xun X et al (2010) Rapid, low-input, low-bias construction of shotgun fragment libraries by high-density in vitro transposition. Genome Biol 11:1–17CrossRefGoogle Scholar
  2. Ajello L, Manson-Bahr PEC, Moore JC (1960) Amboni Caves, Tanganyika, a new endemic area for Histoplasma capsulatum. Am J Trop Med Hyg 9:633–638PubMedCrossRefPubMedCentralGoogle Scholar
  3. Amann RI, Snaidr J, Wagner M et al (1996) In situ visualization of high genetic diversity in a natural community. J Bacteriol 178:3496–3500PubMedPubMedCentralCrossRefGoogle Scholar
  4. Anderson IC, Cairney JWG (2004) Diversity and ecology of soil fungal communities: increased understanding through the application of molecular techniques. Environ Microbiol 6:769–779PubMedCrossRefPubMedCentralGoogle Scholar
  5. Angert ER, Northup DE, Reysenbach A-L et al (1998) Molecular phylogenetic analysis of a bacterial community in Sulphur River, Parker Cave, Kentucky. Am Mineral 83:1583–1592CrossRefGoogle Scholar
  6. Ansorge WJ (2009) Next-generation DNA sequencing techniques. New Biotechnol 25:195–203CrossRefGoogle Scholar
  7. Baas-Becking LGM (1934) Geobiologie; of inleiding tot de milieukunde. WP Van Stockum & Zoon NV, Den HaagGoogle Scholar
  8. Banks ED, Taylor NM, Gulley J et al (2010) Bacterial calcium carbonate precipitation in cave environments: a function of calcium homeostasis. Geomicrobiol J 27:444–454CrossRefGoogle Scholar
  9. Barton HA (2006) Introduction to cave microbiology: a review for the non-specialist. J Cave Karst Stud 68:43–54Google Scholar
  10. Barton HA (2015) Starving artists: bacterial oligotrophic heterotrophy in caves. In: Summers Engel A (ed) Life in extreme environments: microbial life of cave systems, vol 1. DeGruyter, Berlin, GermanyGoogle Scholar
  11. Barton MD, Barton HA (2012) Scaffolder—software for manual genome scaffolding. Source Code Biol Med 7:4PubMedPubMedCentralCrossRefGoogle Scholar
  12. Barton HA, Northup DE (2007) Geomicrobiology in cave environments: past, current and future prospectives. J Cave Karst Stud 69:163–178Google Scholar
  13. Barton HA, Taylor MR, Pace NR (2004) Molecular phylogenetic analysis of a bacterial community in an oligotrophic cave environment. Geomicrobiol J 21:11–20CrossRefGoogle Scholar
  14. Barton HA, Taylor NM, Lubbers BR et al (2006) DNA extraction from low-biomass carbonate rock: an improved method with reduced contamination and the low-biomass contaminant database. J Microbiol Methods 66:21–31PubMedCrossRefPubMedCentralGoogle Scholar
  15. Barton HA, Taylor NM, Kreate M et al (2007) The impact of host rock geochemistry on bacterial community structure in oligotrophic cave environments. Int J Speleol 36:93–104CrossRefGoogle Scholar
  16. Barton MD, Petronio M, Giarrizzo JG et al (2013) The genome of Pseudomonas fluorescens strain R124 demonstrates phenotypic adaptation to the mineral environment. J Bacteriol 195:4793–4803PubMedPubMedCentralCrossRefGoogle Scholar
  17. Barton HA, Giarrizzo JG, Suarez P et al (2014) Microbial diversity in a Venezuelan orthoquartzite cave is dominated by the Chloroflexi (Class Ktedonobacterales) and Thaumarchaeota Group I.1c. Front Microbiol 5:1–14CrossRefGoogle Scholar
  18. Bhullar K, Waglechner N, Pawlowski A et al (2012) Antibiotic resistance is prevalent in an isolated cave microbiome. PLoS One 7:e34953PubMedPubMedCentralCrossRefGoogle Scholar
  19. Boyles JG, Cryan PM, McCracken GF et al (2011) Conservation. Economic importance of bats in agriculture. Science 332:41–42PubMedCrossRefPubMedCentralGoogle Scholar
  20. Branton D, Deamer DW, Marziali A et al (2008) The potential and challenges of nanopore sequencing. Nat Biotechnol 26:1146–1153PubMedPubMedCentralCrossRefGoogle Scholar
  21. Brochier-Armanet C, Boussau B, Gribaldo S et al (2008) Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245–252PubMedCrossRefPubMedCentralGoogle Scholar
  22. Brochier-Armanet C, Gribaldo S, Forterre P (2012) Spotlight on the Thaumarchaeota. ISME J 6:227–230PubMedCrossRefPubMedCentralGoogle Scholar
  23. Burford EP, Kierans M, Gadd GM (2003) Geomycology: fungi in mineral substrata. Mycologist 17:98–107CrossRefGoogle Scholar
  24. Campbell BJ, Engel AS, Porter ML et al (2006) The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4:458–468PubMedCrossRefPubMedCentralGoogle Scholar
  25. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336PubMedPubMedCentralCrossRefGoogle Scholar
  26. Carmichael MJ, Carmichael SK, Santelli CM et al (2013) Mn (II)-oxidizing bacteria are abundant and environmentally relevant members of ferromanganese deposits in caves of the upper Tennessee River Basin. Geomicrobiol J 30:779–800CrossRefGoogle Scholar
  27. Caumartin V (1963) Review of the microbiology of underground environments. NSS Bull 25:1–14Google Scholar
  28. Chandler DP, Fredrickson JK, Brockman FJ (1997) Effect of PCR template concentration on the composition and distribution of total community 16S rDNA clone libraries. Mol Ecol 6:475–482PubMedCrossRefPubMedCentralGoogle Scholar
  29. Chelius MK, Moore JC (2004) Molecular phylogenetic analysis of Archaea and bacteria in Wind Cave, South Dakota. Geomicrobiol J 21:123–134CrossRefGoogle Scholar
  30. Chu H, Fierer N, Lauber CL et al (2010) Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ Microbiol 12:2998–3006PubMedCrossRefPubMedCentralGoogle Scholar
  31. Connell L, Staudigel H (2013) Fungal diversity in a dark oligotrophic volcanic ecosystem (DOVE) on Mount Erebus, Antarctica. Biology 2:798–809PubMedPubMedCentralCrossRefGoogle Scholar
  32. Cuezva S, Fernandez-Cortes A, Porca E et al (2012) The biogeochemical role of Actinobacteria in Altamira Cave, Spain. FEMS Microbiol Ecol 81:281–290PubMedCrossRefPubMedCentralGoogle Scholar
  33. Cunningham KI, Northup DE, Pollastro RM et al (1995) Bacteria, fungi and biokarst in Lechuguilla Cave, Carlsbad Caverns National Park, New Mexico. Environ Geol 25:2–8CrossRefGoogle Scholar
  34. de Araujo JC, Schneider RP (2008) DGGE with genomic DNA: suitable for detection of numerically important organisms but not for identification of the most abundant organisms. Water Res 42:5002–5010PubMedCrossRefPubMedCentralGoogle Scholar
  35. Derewacz DK, Goodwin CR, McNees CR et al (2013) Antimicrobial drug resistance affects broad changes in metabolomic phenotype in addition to secondary metabolism. Proc Natl Acad Sci USA 110:2336–2341PubMedCrossRefPubMedCentralGoogle Scholar
  36. Derewacz DK, McNees CR, Scalmani G et al (2014) Structure and stereochemical determination of hypogeamicins from a cave-derived Actinomycete. J Nat Prod 77:1759–1763PubMedPubMedCentralCrossRefGoogle Scholar
  37. Desai MS, Assig K, Dattagupta S (2013) Nitrogen fixation in distinct microbial niches within a chemoautotrophy-driven cave ecosystem. ISME J 7:2411–2423PubMedPubMedCentralCrossRefGoogle Scholar
  38. DeSantis TZ, Brodie EL, Moberg JP et al (2007) High-density universal 16S rRNA microarray analysis reveals broader diversity than typical clone library when sampling the environment. Microbiol Ecol 53:371–383CrossRefGoogle Scholar
  39. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMedPubMedCentralCrossRefGoogle Scholar
  40. Engel AS (2010) Microbial diversity in cave ecosystems. In: Loy A, Mandl M, Barton LL (eds) Geomicrobiology: molecular and environmental perspective. Springer, New York, pp 219–238CrossRefGoogle Scholar
  41. Engel AS (2015) Bringing microbes into focus for speleology: an introduction. In: Engel AS (ed) Microbial life of cave systems. DeGruyter, Germany, pp 1–18CrossRefGoogle Scholar
  42. Engel AS, Porter ML, Stern LA et al (2004a) Bacterial diversity and ecosystem function of filamentous microbial mats from aphotic (cave) sulfidic springs dominated by chemolithoautotrophic “Epsilonproteobacteria”. FEMS Microbiol Ecol 51:31–53PubMedCrossRefPubMedCentralGoogle Scholar
  43. Engel AS, Stern LA, Bennett PC (2004b) Microbial contributions to cave formation: new insights into sulfuric acid speleogenesis. Geology 32:369–372CrossRefGoogle Scholar
  44. Engel AS, Meisinger DB, Porter ML et al (2010) Linking phylogenetic and functional diversity to nutrient spiraling in microbial mats from Lower Kane Cave (USA). ISME J 4:98–110PubMedCrossRefPubMedCentralGoogle Scholar
  45. Fisher MC, Henk DA, Briggs CJ et al (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–194PubMedCrossRefPubMedCentralGoogle Scholar
  46. Fliermans C, Schmidt E (1977) Nitrobacter in Mammoth Cave. Int J Speleol 9:1–19CrossRefGoogle Scholar
  47. Forde BM, O’Toole PW (2013) Next-generation sequencing technologies and their impact on microbial genomics. Brief Funct Genomics 12:440–453PubMedCrossRefGoogle Scholar
  48. Frick WF, Pollock JF, Hicks AC et al (2010) An emerging disease causes regional population collapse of a common North American bat species. Science 329:670–682CrossRefGoogle Scholar
  49. Gan HY, Gan HM, Tarasco AM et al (2014) Whole-genome sequences of five oligotrophic bacteria isolated from deep within Lechguilla Cave, New Mexico. Genome Announc 2:6Google Scholar
  50. Ganzert L, Bajerski F, Wagner D (2014) Bacterial community composition and diversity of five different permafrost-affected soils of Northeast Greenland. FEMS Microbiol Ecol 89:426–441PubMedCrossRefPubMedCentralGoogle Scholar
  51. Gargas A, Trest MT, Christensen M et al (2009) Geomyces destructans sp. nov. associated with bat White-nose Syndrome. Mycotaxon 108:147–154CrossRefGoogle Scholar
  52. Gerič B, Pipan T, Mulec J (2004) Diversity of culturable bacteria and meiofauna in the epikarst of Škocjanske Jame Caves (Slovenia). Acta Carsol 33:301–309Google Scholar
  53. Gonzalez I, Laiz L, Hermosin B et al (1999) Bacteria isolated from rock art paintings: the case of Atlanterra shelter (south Spain). J Microbiol Methods 36:123–127PubMedCrossRefPubMedCentralGoogle Scholar
  54. Grady F, Garton R, Homes MG (2000) The Pleistocene peccary Platygonus vetus from Poorfarm Cave, Pocahantas County, WV. J Cave Karst Stud 62:41Google Scholar
  55. Grunenwald H, Baas B, Caruccio NC et al (2010) Rapid, high-throughput library preparation for next-generation sequencing. Nat Methods 7:8CrossRefGoogle Scholar
  56. Handelsman J (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68:669–685PubMedPubMedCentralCrossRefGoogle Scholar
  57. Harmon DR, Rannen KM, Keenan SW et al (2013) Drip water chemistry from the Cascade Cave system, Kentucky, and implications for epikarst-derived microbial communities. In: GSA Annual Meeting, Denver, CO, 27–30 October, p 778Google Scholar
  58. Hasenclever HF, Shacklette MH, Young RV et al (1967) The natural occurrence of Histoplasma capsulatum in a cave. 1. Epidemiologic aspects. Am J Epidemiol 86:238–245PubMedCrossRefPubMedCentralGoogle Scholar
  59. Hess WH (1900) The origin of nitrates in cavern earths. J Geol 8:129–134CrossRefGoogle Scholar
  60. Høeg OA (1946) Cyanophyceae and bacteria in calcareous sediments in the interior of limestone caves in Nord-Rana, Norway. Nytt Mag Naturvidensk 85:99–104Google Scholar
  61. Iker BC, Kambesis P, Oehrle SA et al (2010) Microbial atrazine breakdown in a karst groundwater system and its effect on ecosystem energetics. J Environ Qual 39:509–518PubMedCrossRefPubMedCentralGoogle Scholar
  62. Ikner LA, Toomey RS, Nolan G et al (2007) Culturable microbial diversity and the impact of tourism in Kartchner Caverns, Arizona. Microb Ecol 53:30–42PubMedCrossRefPubMedCentralGoogle Scholar
  63. Ivanova V, Tomova I, Kamburov A et al (2013) High phylogenetic diversity of bacteria in the area of prehistoric paintings in Magura Cave, Bulgaria. J Cave Karst Stud 75:218–228CrossRefGoogle Scholar
  64. Jiao JY, Liu L, Park DJ et al (2015) Draft genome sequence of Jiangella alkaliphila KCTC 19222T, isolated from Cave Soil in Jeju, Republic of Korea. Genome Announc 3:4CrossRefGoogle Scholar
  65. Johnston MD, Muench BA, Banks ED et al (2012) Human urine in Lechuguilla Cave: the microbiological impact and potential for bioremediation. J Cave Karst Stud 74:278–291CrossRefGoogle Scholar
  66. Jones DS, Macalady JL (2016) The snotty and the stringy: energy for subsurface life in caves. In: Hurst CJ (ed) Their World: a diversity of microbial environments. Springer, New York, pp 203–224CrossRefGoogle Scholar
  67. Jurado V, Porca E, Cuezva S et al (2010) Fungal outbreak in a show cave. Sci Total Environ 408:3632–3638PubMedCrossRefPubMedCentralGoogle Scholar
  68. Kembel SW, Wu M, Eisen JA et al (2012) Incorporating 16S gene copy number information improves estimates of microbial diversity and abundance. PLoS Comput Biol 8:e1002743PubMedPubMedCentralCrossRefGoogle Scholar
  69. Klimchouk AB, Ford DC, Palmer AN et al (2000) Speleogenesis: evolution of Karstic Aquifers. National Speleological Society, Huntsville, ALGoogle Scholar
  70. Könneke M, Bernhard AE, de la Torre JR et al (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546PubMedCrossRefPubMedCentralGoogle Scholar
  71. Kuczynski J, Stombaugh J, Walters WA et al (2012) Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Curr Protocol Microbiol 27:E1–E5Google Scholar
  72. Kumar Y, Westram R, Kipfer P et al (2006) Evaluation of sequence alignments and oligonucleotide probes with respect to three-dimensional structure of ribosomal RNA using ARB software package. BMC Bioinformatics 7:240PubMedPubMedCentralCrossRefGoogle Scholar
  73. Laiz L, Gonzalez JM, Saiz-Jimenez C (2003) Microbial communities in caves: ecology, physiology, and effects on Paleolithic paintings. In: Koestler RJ, Koestler VH, Charola AE, Nieto-Fernandez FE (eds) Art, biology and conservation: biodeterioration of works of art. Metropolitan Museum of Art, New York, pp 211–225Google Scholar
  74. Land M, Pukall R, Abt B et al (2009) Complete genome sequence of Beutenbergia cavernae type strain (HKI 0122). Stand Genomic Sci 1:21–28PubMedPubMedCentralCrossRefGoogle Scholar
  75. Lander ES (2011) Initial impact of the sequencing of the human genome. Nature 470:187–197PubMedCrossRefPubMedCentralGoogle Scholar
  76. Lauber CL, Hamady M, Knight R et al (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the Continental Scale. Appl Environ Microbiol 75:5111–5120PubMedPubMedCentralCrossRefGoogle Scholar
  77. Lee SD (2008) Jiangella alkaliphila sp. nov., an actinobacterium isolated from a cave. Int J Syst Evol Microbiol 58:1176–1179PubMedCrossRefPubMedCentralGoogle Scholar
  78. Lee NM, Meisinger DB, Aubrecht R et al (2012) Caves and karst environments. In: Bell EM (ed) Life at extremes: environments, organisms and strategies for survival. CAB International, Egham, UK, pp 320–344CrossRefGoogle Scholar
  79. Leinonen R, Sugawara H, Shumway M (2010) The sequence read archive. Nucl Acids Res 39:D19–D21PubMedCrossRefPubMedCentralGoogle Scholar
  80. Lynch MDJ, Neufeld JD (2015) Ecology and exploration of the rare biosphere. Nat Rev Microbiol 13:217–229PubMedCrossRefPubMedCentralGoogle Scholar
  81. Martens-Habbena W, Berube PM, Urakawa H et al (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976–979PubMedCrossRefPubMedCentralGoogle Scholar
  82. McDonald D, Price MN, Goodrich J et al (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618PubMedCrossRefPubMedCentralGoogle Scholar
  83. McMurray DN, Russel LH (1982) Contribution of bats to the maintenance of Histoplasma capsulatum in a cave microfocus. Am J Trop Med Hyg 31:527–531PubMedCrossRefPubMedCentralGoogle Scholar
  84. Miller CS, Baker BJ, Thomas BC et al (2011) EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data. Genome Biol 12:1–14CrossRefGoogle Scholar
  85. Minnis AM, Lindner DL (2013) Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biol 117:638–649PubMedCrossRefPubMedCentralGoogle Scholar
  86. Northup DE, Barnes SM, Yu LE et al (2003) Diverse microbial communitiens inhabiting ferromanganese deposits in Lechuguilla and Spider Caves. Environ Microbiol 5:1071–1086PubMedCrossRefPubMedCentralGoogle Scholar
  87. Ortiz M, Neilson JW, Nelson WM et al (2013) Profiling bacterial diversity and taxonomic composition on speleothem surfaces in Kartchner Caverns, AZ. Microb Ecol 65:371–383PubMedCrossRefPubMedCentralGoogle Scholar
  88. Ortiz M, Legatzki A, Neilson JW et al (2014) Making a living while starving in the dark: metagenomic insights into the energy dynamics of a carbonate cave. ISME J 8:478–491PubMedCrossRefPubMedCentralGoogle Scholar
  89. Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276:734–740PubMedCrossRefPubMedCentralGoogle Scholar
  90. Pace NR, Stahl DA, Lane DJ et al (1986) The analysis of natural microbial populations by ribosomal RNA sequences. Adv Microb Ecol 9:1–55CrossRefGoogle Scholar
  91. Palmer AN (2007) Cave geology. Cave Books, Dayton, OHGoogle Scholar
  92. Parker CW, Wolf JA, Bresser WJ et al (2013) Microbial reducibility of Fe(III) phases associated with the genesis of iron ore caves in the Iron Quadrangle, Minas Gerais, Brazil. Fortschr Mineral 3:395–411CrossRefGoogle Scholar
  93. Peck SB (1986) Bacterial deposition of iron and manganese oxides in North American caves. NSS Bull 48:26–30Google Scholar
  94. Pel J, Broemeling D, Mai L et al (2009) Nonlinear electrophoretic response yields a unique parameter for separation of biomolecules. Proc Natl Acad Sci USA 106:14796–14801PubMedCrossRefPubMedCentralGoogle Scholar
  95. Peuchmaille SJ, Wibbelt G, Korn V et al (2011) Pan-European distribution of White-nose Syndrome (Geomyces destructans) not associated with mass mortality. PLoS One 6:e19167CrossRefGoogle Scholar
  96. Polyak VJ, Güven N (1996) Alunite, natroalunite and hydrated halloysite in Carlsbad Cavern and Lechuguilla Cave, New Mexico. Clays Clay Miner 44:843–850CrossRefGoogle Scholar
  97. Polyak VJ, Güven N (2000) Clays in caves of the Guadalupe Mountains, New Mexico. J Cave Karst Stud 62:120–126Google Scholar
  98. Polz MF, Cavanaugh CM (1998) Bias in template-to-product rations in multitemplate PCR. Appl Environ Microbiol 64:3724–3730PubMedPubMedCentralGoogle Scholar
  99. Porca E, Jurado V, Žgur-Bertok D et al (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 81:255–266PubMedCrossRefPubMedCentralGoogle Scholar
  100. Posada D (2003) Using MODELTEST and PAUP* to select a model of nucleotide substitution. Current Protocols in Bioinformatics Chapter 6:Unit 6.5Google Scholar
  101. Pruesse E, Quast C, Knittel K et al (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196PubMedPubMedCentralCrossRefGoogle Scholar
  102. Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596CrossRefGoogle Scholar
  103. Reynolds HT, Barton HA (2014a) Comparison of the White-nose Syndrome agent Pseudogymnoascus destructans to cave-dwelling relatives suggests reduced saprophytic enzyme activity. PLoS One 9:e86347CrossRefGoogle Scholar
  104. Reynolds HT, Barton HA (2014b) White-nose Syndrome: human activity in the emergence of an extirpating mycosis. In: One health: people, animals, and the environment. ASM Press, Washington, DC, p 167Google Scholar
  105. Reynolds HT, Ingersoll T, Barton HA (2015) The environmental growth of Pseudogymnoascus destructans and its impact on the White-nose Syndrome epidemic in Little Brown Bats (Myotis lucifugus). J Wildl Dis 51:318–331PubMedCrossRefPubMedCentralGoogle Scholar
  106. Reynolds HT, Barton HA, Slot JC (2016) Phylogenomic analysis supports a recent change in nitrate assimilation in the White-nose Syndrome pathogen, Pseudogymnoascus destructans. Fungal Ecol 23:20–29CrossRefGoogle Scholar
  107. Rhoads A, Au KF (2015) PacBio sequencing and its applications. Genomics Proteom Bioinformatics 13:278–289CrossRefGoogle Scholar
  108. Rinke C, Schwientek P, Sczyrba A et al (2013) Insights into the phylogeny and coding potential of microbial dark matter. Nature 499:431–437PubMedCrossRefGoogle Scholar
  109. Rusznyak A, Akob DM, Nietzsche S et al (2012) Calcite biomineralization by bacterial isolates from the recently discovered pristine karstic Herrenberg cave. Appl Environ Microbiol 78:1157–1167PubMedPubMedCentralCrossRefGoogle Scholar
  110. Sanger F, Air GM, Barrell BG et al (1977) Nucleotide sequence of bacteriophage φX174 DNA. Nature 265:687–695PubMedCrossRefPubMedCentralGoogle Scholar
  111. Sarbu SM, Kane TC, Kinkle BK (1996) A chemoautotrophically based cave ecosystem. Science 272:1953–1955CrossRefGoogle Scholar
  112. Sasowsky ID, Palmer MV (1994) Breakthroughs in karst geomicrobiology and redox geochemistry, vol 1. Karst Waters Institute, Charles Town, WVGoogle Scholar
  113. Saw JHW, Schatz M, Brown MV et al (2013) Cultivation and complete genome sequencing of Gloeobacter kilaueensis sp. nov., from a lava cave in Kīlauea Caldera, Hawai'i. PLoS One 8:e76376PubMedPubMedCentralCrossRefGoogle Scholar
  114. Schabereiter-Gurtner C, Saiz-Jimenez C, Pinar G et al (2002) Altamira cave Paleolithic paintings harbor partly unknown bacterial communities. FEMS Microbiol Lett 211:7–11PubMedCrossRefPubMedCentralGoogle Scholar
  115. Schneider T, Keiblinger KM, Schmid E et al (2012) Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions. ISME J 6:1749–1762PubMedPubMedCentralCrossRefGoogle Scholar
  116. Scott W (1909) An ecological study of the plankton of Shawnee Cave, with notes on the cave environment. Biol Bull 17:386–407CrossRefGoogle Scholar
  117. Shabarova T, Pernthaler J (2010) Karst pools in subsurface environments: collectors of microbial diversity or temporary residence between habitat types. Environ Microbiol 12:1061–1074PubMedCrossRefPubMedCentralGoogle Scholar
  118. Shapiro J, Pringle A (2009) Anthropogenic influences on the diversity of fungi isolated from caves in Kentucky and Tennessee. Am Midl Nat 163:76–86CrossRefGoogle Scholar
  119. Shendure J, Mitra RD, Varma C et al (2004) Advanced sequencing technologies: methods and goals. Nat Rev Genet 5:335–344PubMedCrossRefPubMedCentralGoogle Scholar
  120. Snyder LA, Loman N, Pallen MJ et al (2009) Next-generation sequencing—the promise and perils of charting the great microbial unknown. Microb Ecol 57:1–3PubMedCrossRefPubMedCentralGoogle Scholar
  121. Sogin ML, Morrison HG, Huber JA et al (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA 103:12115–12120PubMedCrossRefPubMedCentralGoogle Scholar
  122. Stahl DA, Lane DJ, Olsen GJ, Pace NR (1984) Analysis of hydrothermal vent-associated symbionts by ribosomal RNA sequences. Science 224:409–411PubMedCrossRefPubMedCentralGoogle Scholar
  123. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313PubMedPubMedCentralCrossRefGoogle Scholar
  124. Sterflinger K (2000) Fungi as geologic agents. Geomicrobiol J 17:97–124CrossRefGoogle Scholar
  125. Summons RE, Sessions AL, Allwood AC et al (2014) Planning considerations related to the organic contamination of Martian samples and implications for the Mars 2020 Rover. Astrobiology 14:969–1027PubMedCrossRefPubMedCentralGoogle Scholar
  126. Tan SC, Yiap BC (2009) DNA, RNA, and protein extraction: the past and the present. J Biomed Biotechnol 2009:574398PubMedPubMedCentralCrossRefGoogle Scholar
  127. Tedersoo L, Bahram M, Põlme S et al (2014) Global diversity and geography of soil fungi. Science 346:1256688PubMedCrossRefPubMedCentralGoogle Scholar
  128. Tetu SG, Breakwell K, Elbourne LD et al (2013) Life in the dark: metagenomic evidence that a microbial slime community is driven by inorganic nitrogen metabolism. ISME J 7:1227–1236PubMedPubMedCentralCrossRefGoogle Scholar
  129. Thomas T, Gilbert JA, Meyer F (2012) Metagenomics—a guide from sampling to data analysis. Microb Inform Exp 2:1–12CrossRefGoogle Scholar
  130. Tomczyk-Żak K, Zielenkiewicz U (2016) Microbial diversity in caves. Geomicrobiol J 33:20–38CrossRefGoogle Scholar
  131. Tyson GW, Chapman J, Hugenholtz P et al (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37–43PubMedCrossRefPubMedCentralGoogle Scholar
  132. Valentine DL (2007) Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat Rev Microbiol 5:316–323PubMedCrossRefPubMedCentralGoogle Scholar
  133. Vanderwolf KJ, Malloch D, McAlpine DF et al (2013) A world review of fungi, yeasts, and slime molds in caves. Int J Speleol 42:9CrossRefGoogle Scholar
  134. Venter JC, Remington K, Heidelberg JF et al (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74PubMedCrossRefPubMedCentralGoogle Scholar
  135. Vlăsceanu L, Popa R, Kinkle BK (1997) Characterization of Thiobacillus thioparus LV43 and its distribution in a chemoautotrophically based groundwater ecosystem. Appl Environ Microbiol 63:3123–3127PubMedPubMedCentralGoogle Scholar
  136. Warnecke L, Turner JM, Bollinger TK et al (2012) Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of White-nose Syndrome. Proc Natl Acad Sci USA 109:6999–7003PubMedCrossRefPubMedCentralGoogle Scholar
  137. Wilgenbusch JC, Swofford D (2003) Inferring evolutionary trees with PAUP*. Current Protocols in Bioinformatics Chapter 6:Unit 6.4Google Scholar
  138. Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74:5088–5090PubMedCrossRefPubMedCentralGoogle Scholar
  139. Yun Y, Xiang X, Wang H et al (2015) Five-year monitoring of bacterial communities in dripping water from the Heshang Cave in central China: implication for paleoclimate reconstruction and ecological functions. Geomicrobiol J 33:1–11CrossRefGoogle Scholar
  140. Zhalnina K, Dias R, de Quadros PD et al (2015) Soil pH determines microbial diversity and composition in the Park Grass Experiment. Microb Ecol 69:395–406PubMedCrossRefPubMedCentralGoogle Scholar
  141. Zhou JP, Gu Y, Zou C et al (2007) Phylogenetic diversity of bacteria in an earth-cave in Guizhou Province, southwest of China. J Microbiol 45:105–112PubMedPubMedCentralGoogle Scholar

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Authors and Affiliations

  1. 1.Department of BiologyUniversity of AkronAkronUSA

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