Skip to main content
SpringerLink
Log in

The Microbial Diversity of Caves

  • Chapter
  • First Online:
Cave Ecology

Part of the book series: Ecological Studies ((ECOLSTUD,volume 235))

Abstract

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.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • 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 11:1–17

    Article  CAS  Google Scholar 

  • Ajello L, Manson-Bahr PEC, Moore JC (1960) Amboni Caves, Tanganyika, a new endemic area for Histoplasma capsulatum. Am J Trop Med Hyg 9:633–638

    Article  CAS  PubMed  Google Scholar 

  • Amann RI, Snaidr J, Wagner M et al (1996) In situ visualization of high genetic diversity in a natural community. J Bacteriol 178:3496–3500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson IC, Cairney JWG (2004) Diversity and ecology of soil fungal communities: increased understanding through the application of molecular techniques. Environ Microbiol 6:769–779

    Article  CAS  PubMed  Google Scholar 

  • 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 83:1583–1592

    Article  CAS  Google Scholar 

  • Ansorge WJ (2009) Next-generation DNA sequencing techniques. New Biotechnol 25:195–203

    Article  CAS  Google Scholar 

  • Baas-Becking LGM (1934) Geobiologie; of inleiding tot de milieukunde. WP Van Stockum & Zoon NV, Den Haag

    Google Scholar 

  • Banks ED, Taylor NM, Gulley J et al (2010) Bacterial calcium carbonate precipitation in cave environments: a function of calcium homeostasis. Geomicrobiol J 27:444–454

    Article  CAS  Google Scholar 

  • Barton HA (2006) Introduction to cave microbiology: a review for the non-specialist. J Cave Karst Stud 68:43–54

    Google Scholar 

  • 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, Germany

    Google Scholar 

  • Barton MD, Barton HA (2012) Scaffolder—software for manual genome scaffolding. Source Code Biol Med 7:4

    Article  PubMed  PubMed Central  Google Scholar 

  • Barton HA, Northup DE (2007) Geomicrobiology in cave environments: past, current and future prospectives. J Cave Karst Stud 69:163–178

    Google Scholar 

  • Barton HA, Taylor MR, Pace NR (2004) Molecular phylogenetic analysis of a bacterial community in an oligotrophic cave environment. Geomicrobiol J 21:11–20

    Article  CAS  Google Scholar 

  • 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 66:21–31

    Article  CAS  PubMed  Google Scholar 

  • 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 36:93–104

    Article  Google Scholar 

  • 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 195:4793–4803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 5:1–14

    Article  Google Scholar 

  • Bhullar K, Waglechner N, Pawlowski A et al (2012) Antibiotic resistance is prevalent in an isolated cave microbiome. PLoS One 7:e34953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boyles JG, Cryan PM, McCracken GF et al (2011) Conservation. Economic importance of bats in agriculture. Science 332:41–42

    Article  PubMed  Google Scholar 

  • Branton D, Deamer DW, Marziali A et al (2008) The potential and challenges of nanopore sequencing. Nat Biotechnol 26:1146–1153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brochier-Armanet C, Boussau B, Gribaldo S et al (2008) Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245–252

    Article  CAS  PubMed  Google Scholar 

  • Brochier-Armanet C, Gribaldo S, Forterre P (2012) Spotlight on the Thaumarchaeota. ISME J 6:227–230

    Article  CAS  PubMed  Google Scholar 

  • Burford EP, Kierans M, Gadd GM (2003) Geomycology: fungi in mineral substrata. Mycologist 17:98–107

    Article  Google Scholar 

  • Campbell BJ, Engel AS, Porter ML et al (2006) The versatile epsilon-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4:458–468

    Article  CAS  PubMed  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 30:779–800

    Article  CAS  Google Scholar 

  • Caumartin V (1963) Review of the microbiology of underground environments. NSS Bull 25:1–14

    Google Scholar 

  • 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 6:475–482

    Article  CAS  PubMed  Google Scholar 

  • Chelius MK, Moore JC (2004) Molecular phylogenetic analysis of Archaea and bacteria in Wind Cave, South Dakota. Geomicrobiol J 21:123–134

    Article  CAS  Google Scholar 

  • 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 12:2998–3006

    Article  CAS  PubMed  Google Scholar 

  • Connell L, Staudigel H (2013) Fungal diversity in a dark oligotrophic volcanic ecosystem (DOVE) on Mount Erebus, Antarctica. Biology 2:798–809

    Article  PubMed  PubMed Central  Google Scholar 

  • Cuezva S, Fernandez-Cortes A, Porca E et al (2012) The biogeochemical role of Actinobacteria in Altamira Cave, Spain. FEMS Microbiol Ecol 81:281–290

    Article  CAS  PubMed  Google Scholar 

  • Cunningham KI, Northup DE, Pollastro RM et al (1995) Bacteria, fungi and biokarst in Lechuguilla Cave, Carlsbad Caverns National Park, New Mexico. Environ Geol 25:2–8

    Article  Google Scholar 

  • 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 42:5002–5010

    Article  PubMed  CAS  Google Scholar 

  • 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 110:2336–2341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Derewacz DK, McNees CR, Scalmani G et al (2014) Structure and stereochemical determination of hypogeamicins from a cave-derived Actinomycete. J Nat Prod 77:1759–1763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Desai MS, Assig K, Dattagupta S (2013) Nitrogen fixation in distinct microbial niches within a chemoautotrophy-driven cave ecosystem. ISME J 7:2411–2423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 53:371–383

    Article  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 219–238

    Chapter  Google Scholar 

  • Engel AS (2015) Bringing microbes into focus for speleology: an introduction. In: Engel AS (ed) Microbial life of cave systems. DeGruyter, Germany, pp 1–18

    Chapter  Google Scholar 

  • 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 51:31–53

    Article  CAS  PubMed  Google Scholar 

  • Engel AS, Stern LA, Bennett PC (2004b) Microbial contributions to cave formation: new insights into sulfuric acid speleogenesis. Geology 32:369–372

    Article  CAS  Google Scholar 

  • 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 4:98–110

    Article  PubMed  Google Scholar 

  • Fisher MC, Henk DA, Briggs CJ et al (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–194

    Article  CAS  PubMed  Google Scholar 

  • Fliermans C, Schmidt E (1977) Nitrobacter in Mammoth Cave. Int J Speleol 9:1–19

    Article  Google Scholar 

  • Forde BM, O’Toole PW (2013) Next-generation sequencing technologies and their impact on microbial genomics. Brief Funct Genomics 12:440–453

    Article  CAS  PubMed  Google Scholar 

  • Frick WF, Pollock JF, Hicks AC et al (2010) An emerging disease causes regional population collapse of a common North American bat species. Science 329:670–682

    Article  CAS  Google Scholar 

  • 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 2:6

    Google Scholar 

  • Ganzert L, Bajerski F, Wagner D (2014) Bacterial community composition and diversity of five different permafrost-affected soils of Northeast Greenland. FEMS Microbiol Ecol 89:426–441

    Article  CAS  PubMed  Google Scholar 

  • Gargas A, Trest MT, Christensen M et al (2009) Geomyces destructans sp. nov. associated with bat White-nose Syndrome. Mycotaxon 108:147–154

    Article  Google Scholar 

  • Gerič B, Pipan T, Mulec J (2004) Diversity of culturable bacteria and meiofauna in the epikarst of Škocjanske Jame Caves (Slovenia). Acta Carsol 33:301–309

    Google Scholar 

  • 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 36:123–127

    Article  CAS  PubMed  Google Scholar 

  • Grady F, Garton R, Homes MG (2000) The Pleistocene peccary Platygonus vetus from Poorfarm Cave, Pocahantas County, WV. J Cave Karst Stud 62:41

    Google Scholar 

  • Grunenwald H, Baas B, Caruccio NC et al (2010) Rapid, high-throughput library preparation for next-generation sequencing. Nat Methods 7:8

    Article  CAS  Google Scholar 

  • Handelsman J (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68:669–685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 778

    Google Scholar 

  • Hasenclever HF, Shacklette MH, Young RV et al (1967) The natural occurrence of Histoplasma capsulatum in a cave. 1. Epidemiologic aspects. Am J Epidemiol 86:238–245

    Article  CAS  PubMed  Google Scholar 

  • Hess WH (1900) The origin of nitrates in cavern earths. J Geol 8:129–134

    Article  CAS  Google Scholar 

  • Høeg OA (1946) Cyanophyceae and bacteria in calcareous sediments in the interior of limestone caves in Nord-Rana, Norway. Nytt Mag Naturvidensk 85:99–104

    Google Scholar 

  • 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 39:509–518

    Article  CAS  PubMed  Google Scholar 

  • Ikner LA, Toomey RS, Nolan G et al (2007) Culturable microbial diversity and the impact of tourism in Kartchner Caverns, Arizona. Microb Ecol 53:30–42

    Article  PubMed  Google Scholar 

  • 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 75:218–228

    Article  CAS  Google Scholar 

  • 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 3:4

    Article  Google Scholar 

  • 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 74:278–291

    Article  CAS  Google Scholar 

  • 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 203–224

    Chapter  Google Scholar 

  • Jurado V, Porca E, Cuezva S et al (2010) Fungal outbreak in a show cave. Sci Total Environ 408:3632–3638

    Article  CAS  PubMed  Google Scholar 

  • 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:e1002743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klimchouk AB, Ford DC, Palmer AN et al (2000) Speleogenesis: evolution of Karstic Aquifers. National Speleological Society, Huntsville, AL

    Google Scholar 

  • Könneke M, Bernhard AE, de la Torre JR et al (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546

    Article  PubMed  CAS  Google Scholar 

  • 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–E5

    Google Scholar 

  • 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 7:240

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 211–225

    Google Scholar 

  • Land M, Pukall R, Abt B et al (2009) Complete genome sequence of Beutenbergia cavernae type strain (HKI 0122). Stand Genomic Sci 1:21–28

    Article  PubMed  PubMed Central  Google Scholar 

  • Lander ES (2011) Initial impact of the sequencing of the human genome. Nature 470:187–197

    Article  CAS  PubMed  Google Scholar 

  • 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 75:5111–5120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SD (2008) Jiangella alkaliphila sp. nov., an actinobacterium isolated from a cave. Int J Syst Evol Microbiol 58:1176–1179

    Article  CAS  PubMed  Google Scholar 

  • 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 320–344

    Chapter  Google Scholar 

  • Leinonen R, Sugawara H, Shumway M (2010) The sequence read archive. Nucl Acids Res 39:D19–D21

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lynch MDJ, Neufeld JD (2015) Ecology and exploration of the rare biosphere. Nat Rev Microbiol 13:217–229

    Article  CAS  PubMed  Google Scholar 

  • Martens-Habbena W, Berube PM, Urakawa H et al (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976–979

    Article  CAS  PubMed  Google Scholar 

  • 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 6:610–618

    Article  CAS  PubMed  Google Scholar 

  • McMurray DN, Russel LH (1982) Contribution of bats to the maintenance of Histoplasma capsulatum in a cave microfocus. Am J Trop Med Hyg 31:527–531

    Article  CAS  PubMed  Google Scholar 

  • 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 12:1–14

    Article  CAS  Google Scholar 

  • 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 117:638–649

    Article  PubMed  Google Scholar 

  • Northup DE, Barnes SM, Yu LE et al (2003) Diverse microbial communitiens inhabiting ferromanganese deposits in Lechuguilla and Spider Caves. Environ Microbiol 5:1071–1086

    Article  PubMed  Google Scholar 

  • Ortiz M, Neilson JW, Nelson WM et al (2013) Profiling bacterial diversity and taxonomic composition on speleothem surfaces in Kartchner Caverns, AZ. Microb Ecol 65:371–383

    Article  PubMed  Google Scholar 

  • 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 8:478–491

    Article  CAS  PubMed  Google Scholar 

  • Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276:734–740

    Article  CAS  PubMed  Google Scholar 

  • Pace NR, Stahl DA, Lane DJ et al (1986) The analysis of natural microbial populations by ribosomal RNA sequences. Adv Microb Ecol 9:1–55

    Article  CAS  Google Scholar 

  • Palmer AN (2007) Cave geology. Cave Books, Dayton, OH

    Google Scholar 

  • 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 3:395–411

    Article  CAS  Google Scholar 

  • Peck SB (1986) Bacterial deposition of iron and manganese oxides in North American caves. NSS Bull 48:26–30

    CAS  Google Scholar 

  • 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 106:14796–14801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e19167

    Article  CAS  Google Scholar 

  • Polyak VJ, Güven N (1996) Alunite, natroalunite and hydrated halloysite in Carlsbad Cavern and Lechuguilla Cave, New Mexico. Clays Clay Miner 44:843–850

    Article  CAS  Google Scholar 

  • Polyak VJ, Güven N (2000) Clays in caves of the Guadalupe Mountains, New Mexico. J Cave Karst Stud 62:120–126

    CAS  Google Scholar 

  • Polz MF, Cavanaugh CM (1998) Bias in template-to-product rations in multitemplate PCR. Appl Environ Microbiol 64:3724–3730

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 81:255–266

    Article  CAS  PubMed  Google Scholar 

  • Posada D (2003) Using MODELTEST and PAUP* to select a model of nucleotide substitution. Current Protocols in Bioinformatics Chapter 6:Unit 6.5

    Google Scholar 

  • 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 35:7188–7196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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–D596

    Article  CAS  PubMed  Google Scholar 

  • 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:e86347

    Article  CAS  Google Scholar 

  • 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 167

    Google Scholar 

  • 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 51:318–331

    Article  PubMed  Google Scholar 

  • 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 23:20–29

    Article  Google Scholar 

  • Rhoads A, Au KF (2015) PacBio sequencing and its applications. Genomics Proteom Bioinformatics 13:278–289

    Article  Google Scholar 

  • Rinke C, Schwientek P, Sczyrba A et al (2013) Insights into the phylogeny and coding potential of microbial dark matter. Nature 499:431–437

    Article  CAS  PubMed  Google Scholar 

  • 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 78:1157–1167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanger F, Air GM, Barrell BG et al (1977) Nucleotide sequence of bacteriophage φX174 DNA. Nature 265:687–695

    Article  CAS  PubMed  Google Scholar 

  • Sarbu SM, Kane TC, Kinkle BK (1996) A chemoautotrophically based cave ecosystem. Science 272:1953–1955

    Article  CAS  PubMed  Google Scholar 

  • Sasowsky ID, Palmer MV (1994) Breakthroughs in karst geomicrobiology and redox geochemistry, vol 1. Karst Waters Institute, Charles Town, WV

    Google Scholar 

  • 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:e76376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schabereiter-Gurtner C, Saiz-Jimenez C, Pinar G et al (2002) Altamira cave Paleolithic paintings harbor partly unknown bacterial communities. FEMS Microbiol Lett 211:7–11

    Article  CAS  PubMed  Google Scholar 

  • 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 6:1749–1762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scott W (1909) An ecological study of the plankton of Shawnee Cave, with notes on the cave environment. Biol Bull 17:386–407

    Article  Google Scholar 

  • Shabarova T, Pernthaler J (2010) Karst pools in subsurface environments: collectors of microbial diversity or temporary residence between habitat types. Environ Microbiol 12:1061–1074

    Article  CAS  PubMed  Google Scholar 

  • Shapiro J, Pringle A (2009) Anthropogenic influences on the diversity of fungi isolated from caves in Kentucky and Tennessee. Am Midl Nat 163:76–86

    Article  Google Scholar 

  • Shendure J, Mitra RD, Varma C et al (2004) Advanced sequencing technologies: methods and goals. Nat Rev Genet 5:335–344

    Article  CAS  PubMed  Google Scholar 

  • Snyder LA, Loman N, Pallen MJ et al (2009) Next-generation sequencing—the promise and perils of charting the great microbial unknown. Microb Ecol 57:1–3

    Article  PubMed  Google Scholar 

  • 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 103:12115–12120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stahl DA, Lane DJ, Olsen GJ, Pace NR (1984) Analysis of hydrothermal vent-associated symbionts by ribosomal RNA sequences. Science 224:409–411

    Article  CAS  PubMed  Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sterflinger K (2000) Fungi as geologic agents. Geomicrobiol J 17:97–124

    Article  CAS  Google Scholar 

  • 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 14:969–1027

    Article  CAS  PubMed  Google Scholar 

  • Tan SC, Yiap BC (2009) DNA, RNA, and protein extraction: the past and the present. J Biomed Biotechnol 2009:574398

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tedersoo L, Bahram M, Põlme S et al (2014) Global diversity and geography of soil fungi. Science 346:1256688

    Article  PubMed  CAS  Google Scholar 

  • 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 7:1227–1236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas T, Gilbert JA, Meyer F (2012) Metagenomics—a guide from sampling to data analysis. Microb Inform Exp 2:1–12

    Article  Google Scholar 

  • Tomczyk-Żak K, Zielenkiewicz U (2016) Microbial diversity in caves. Geomicrobiol J 33:20–38

    Article  Google Scholar 

  • Tyson GW, Chapman J, Hugenholtz P et al (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37–43

    Article  CAS  PubMed  Google Scholar 

  • Valentine DL (2007) Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat Rev Microbiol 5:316–323

    Article  CAS  PubMed  Google Scholar 

  • Vanderwolf KJ, Malloch D, McAlpine DF et al (2013) A world review of fungi, yeasts, and slime molds in caves. Int J Speleol 42:9

    Article  Google Scholar 

  • Venter JC, Remington K, Heidelberg JF et al (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74

    Article  CAS  PubMed  Google Scholar 

  • Vlăsceanu L, Popa R, Kinkle BK (1997) Characterization of Thiobacillus thioparus LV43 and its distribution in a chemoautotrophically based groundwater ecosystem. Appl Environ Microbiol 63:3123–3127

    PubMed  PubMed Central  Google Scholar 

  • 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 109:6999–7003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilgenbusch JC, Swofford D (2003) Inferring evolutionary trees with PAUP*. Current Protocols in Bioinformatics Chapter 6:Unit 6.4

    Google Scholar 

  • Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74:5088–5090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 33:1–11

    Article  CAS  Google Scholar 

  • Zhalnina K, Dias R, de Quadros PD et al (2015) Soil pH determines microbial diversity and composition in the Park Grass Experiment. Microb Ecol 69:395–406

    Article  CAS  PubMed  Google Scholar 

  • 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 45:105–112

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Department of Biology, University of Akron, Akron, OH, USA

    Olivia S. Hershey & Hazel A. Barton

Authors
  1. Olivia S. Hershey
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hazel A. Barton
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hazel A. Barton .

Editor information

Editors and Affiliations

  1. Emil Racovitza Institute of Speleology, Romanian Academy, Cluj Napoca, Romania

    Oana Teodora Moldovan

  2. Faculty of Science, P. J. Šafárik University, Košice, Slovakia

    Ľubomír Kováč

  3. Bennelongia Environmental Consultants, Jolimont, Western Australia, Australia

    Stuart Halse

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Hershey, O.S., Barton, H.A. (2018). The Microbial Diversity of Caves. In: Moldovan, O., Kováč, Ľ., Halse, S. (eds) Cave Ecology. Ecological Studies, vol 235. Springer, Cham. https://doi.org/10.1007/978-3-319-98852-8_5

Download citation

Publish with us

Policies and ethics

Search

Navigation