Advertisement

Microbial Ecology

, Volume 69, Issue 2, pp 333–345 | Cite as

Community Analysis of Plant Biomass-Degrading Microorganisms from Obsidian Pool, Yellowstone National Park

  • Tatiana A. Vishnivetskaya
  • Scott D. Hamilton-Brehm
  • Mircea Podar
  • Jennifer J. Mosher
  • Anthony V. Palumbo
  • Tommy J. Phelps
  • Martin Keller
  • James G. Elkins
Environmental Microbiology

Abstract

The conversion of lignocellulosic biomass into biofuels can potentially be improved by employing robust microorganisms and enzymes that efficiently deconstruct plant polysaccharides at elevated temperatures. Many of the geothermal features of Yellowstone National Park (YNP) are surrounded by vegetation providing a source of allochthonic material to support heterotrophic microbial communities adapted to utilize plant biomass as a primary carbon and energy source. In this study, a well-known hot spring environment, Obsidian Pool (OBP), was examined for potential biomass-active microorganisms using cultivation-independent and enrichment techniques. Analysis of 33,684 archaeal and 43,784 bacterial quality-filtered 16S rRNA gene pyrosequences revealed that archaeal diversity in the main pool was higher than bacterial; however, in the vegetated area, overall bacterial diversity was significantly higher. Of notable interest was a flooded depression adjacent to OBP supporting a stand of Juncus tweedyi, a heat-tolerant rush commonly found growing near geothermal features in YNP. The microbial community from heated sediments surrounding the plants was enriched in members of the Firmicutes including potentially (hemi)cellulolytic bacteria from the genera Clostridium, Anaerobacter, Caloramator, Caldicellulosiruptor, and Thermoanaerobacter. Enrichment cultures containing model and real biomass substrates were established at a wide range of temperatures (55–85 °C). Microbial activity was observed up to 80 °C on all substrates including Avicel, xylan, switchgrass, and Populus sp. Independent of substrate, Caloramator was enriched at lower (<65 °C) temperatures while highly active cellulolytic bacteria Caldicellulosiruptor were dominant at high (>65 °C) temperatures.

Keywords

Thermophiles Plant biomass utilization Bioenergy Microbial communities Yellowstone National Park Extremophiles. 

Notes

Acknowledgments

We thank the National Park Service and especially Christie Hendrix for coordinating and allowing sampling under permit #YELL-2008-SCI-5714. Heidi Anderson at the Yellowstone Center for Resources helped with plant species identification. We kindly thank Zamin Koo Yang for the assistance with pyrosequencing and Xiangping Yin for ICP analysis. Christopher W. Schadt provided helpful comments on the manuscript. This work was supported by the BioEnergy Science Center (BESC), which is a U.S. Department of Energy Bioenergy Research Center supported by the Office of Biological and Environmental Research in the DOE Office of Science, Oak Ridge National Laboratory. Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the U.S. Department of Energy under contract DE-AC05-00OR22725.

Supplementary material

248_2014_500_MOESM1_ESM.docx (37 kb)
Supplementary Table S1 (DOCX 37 kb)
248_2014_500_MOESM2_ESM.docx (131 kb)
Supplementary Fig. S1 (DOCX 131 kb)
248_2014_500_MOESM3_ESM.docx (239 kb)
Supplementary Fig. S2 (DOCX 239 kb)
248_2014_500_MOESM4_ESM.docx (504 kb)
Supplementary Fig. S3 (DOCX 503 kb)
248_2014_500_MOESM5_ESM.docx (454 kb)
Supplementary Fig. S4 (DOCX 454 kb)
248_2014_500_MOESM6_ESM.docx (296 kb)
Supplementary Fig. S5 (DOCX 295 kb)

References

  1. 1.
    Carroll A, Somerville C (2009) Cellulosic biofuels. Annu Rev Plant Biol 60:165–182. doi: 10.1146/annurev.arplant.043008.092125 PubMedCrossRefGoogle Scholar
  2. 2.
    Bayer E, Shoham Y, Lamed R (2006) Cellulose-decomposing bacteria and their enzyme systems. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 578–617CrossRefGoogle Scholar
  3. 3.
    Reid NM, Addison SL, Macdonald LJ, Lloyd-Jones G (2011) Biodiversity of active and inactive bacteria in the gut flora of wood-feeding huhu beetle larvae (Prionoplus reticularis). Appl Environ Microbiol 77:7000–7006PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Warnecke F, Luginbuhl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT, Cayouette M, McHardy AC, Djordjevic G, Aboushadi N, Sorek R, Tringe SG, Podar M, Martin HG, Kunin V, Dalevi D, Madejska J, Kirton E, Platt D, Szeto E, Salamov A, Barry K, Mikhailova N, Kyrpides NC, Matson EG, Ottesen EA, Zhang XN, Hernandez M, Murillo C, Acosta LG, Rigoutsos I, Tamayo G, Green BD, Chang C, Rubin EM, Mathur EJ, Robertson DE, Hugenholtz P, Leadbetter JR (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–565PubMedCrossRefGoogle Scholar
  5. 5.
    Fouts DE, Szpakowski S, Purushe J, Torralba M, Waterman RC, MacNeil MD, Alexander LJ, Nelson KE (2012) Next generation sequencing to define prokaryotic and fungal diversity in the bovine rumen. PLoS One 7. doi: 10.1371/journal.pone.0048289
  6. 6.
    Hess M, Sczyrba A, Egan R, Kim TW, Chokhawala H, Schroth G, Luo SJ, Clark DS, Chen F, Zhang T, Mackie RI, Pennacchio LA, Tringe SG, Visel A, Woyke T, Wang Z, Rubin EM (2011) Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331:463–467. doi: 10.1126/science.1200387 PubMedCrossRefGoogle Scholar
  7. 7.
    Brulc JM, Antonopoulos DA, Miller MEB, Wilson MK, Yannarell AC, Dinsdale EA, Edwards RE, Frank ED, Emerson JB, Wacklin P, Coutinho PM, Henrissat B, Nelson KE, White BA (2009) Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc Natl Acad Sci U S A 106:1948–1953. doi: 10.1073/pnas.0806191105 PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    Allgaier M, Reddy A, Park JI, Ivanova N, D’Haeseleer P, Lowry S, Sapra R, Hazen TC, Simmons BA, VanderGheynst JS, Hugenholtz P (2010) Targeted discovery of glycoside hydrolases from a switchgrass-adapted compost community. PLoS One 5:e8812. doi: 10.1371/journal.pone.0008812 PubMedCentralPubMedCrossRefGoogle Scholar
  9. 9.
    van der Lelie D, Taghavi S, McCorkle SM, Li LL, Malfatti SA, Monteleone D, Donohoe BS, Ding SY, Adney WS, Himmel ME, Tringe SG (2012) The metagenome of an anaerobic microbial community decomposing poplar wood chips. PLoS One 7. doi: 10.1371/journal.pone.0036740
  10. 10.
    Reddy AP, Allgaier M, Singer SW, Hazen TC, Simmons BA, Hugenholtz P, VanderGheynst JS (2011) Bioenergy feedstock-specific enrichment of microbial populations during high-solids thermophilic deconstruction. Biotechnol Bioeng 108:2088–2098. doi: 10.1002/bit.23176 PubMedCrossRefGoogle Scholar
  11. 11.
    Taylor MP, Eley KL, Martin S, Tuffin MI, Burton SG, Cowan DA (2009) Thermophilic ethanologenesis: future prospects for second-generation bioethanol production. Trends Biotechnol 27:398–405. doi: 10.1016/j.tibtech.2009.03.006 PubMedCrossRefGoogle Scholar
  12. 12.
    Shaw AJ, Podkaminer KK, Desai SG, Bardsley JS, Rogers SR, Thorne PG, Hogsett DA, Lynd LR (2008) Metabolic engineering of a thermophilic bacterium to produce ethanol at high yield. Proc Natl Acad Sci U S A 105:13769–13774. doi: 10.1073/pnas.0801266105 PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Olson DG, McBride JE, Shaw AJ, Lynd LR (2012) Recent progress in consolidated bioprocessing. Curr Opin Biotechnol 23:396–405. doi: 10.1016/j.copbio.2011.11.026 PubMedCrossRefGoogle Scholar
  14. 14.
    Blumer-Schuette SE, Kataeva I, Westpheling J, Adams MW, Kelly RM (2008) Extremely thermophilic microorganisms for biomass conversion: status and prospects. Curr Opin Biotechnol 19:210–217. doi: 10.1016/j.copbio.2008.04.007 PubMedCrossRefGoogle Scholar
  15. 15.
    Yang SJ, Kataeva I, Hamilton-Brehm SD, Engle NL, Tschaplinski TJ, Doeppke C, Davis M, Westpheling J, Adams MWW (2009) Efficient degradation of lignocellulosic plant biomass, without pretreatment, by the thermophilic anaerobe Anaerocellum thermophilum DSM 6725. Appl Environ Microbiol 75:4762–4769PubMedCentralPubMedCrossRefGoogle Scholar
  16. 16.
    Cha M, Chung D, Elkins JG, Guss AM, Westpheling J (2013) Metabolic engineering of Caldicellulosiruptor bescii yields increased hydrogen production from lignocellulosic biomass. Biotechnol Biofuels 6:85. doi: 10.1186/1754-6834-6-85 PubMedCentralPubMedCrossRefGoogle Scholar
  17. 17.
    Svetlitchnyi VA, Kensch O, Falkenhan DA, Korseska SG, Lippert N, Prinz M, Sassi J, Schickor A, Curvers S (2013) Single-step ethanol production from lignocellulose using novel extremely thermophilic bacteria. Biotechnol Biofuels 6:31. doi: 10.1186/1754-6834-6-31 PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Yao S, Mikkelsen MJ (2010) Metabolic engineering to improve ethanol production in Thermoanaerobacter mathranii. Appl Microbiol Biotechnol 88:199–208. doi: 10.1007/s00253-010-2703-3 PubMedCrossRefGoogle Scholar
  19. 19.
    Peacock JP, Cole JK, Murugapiran SK, Dodsworth JA, Fisher JC, Moser DP, Hedlund BP (2013) Pyrosequencing reveals high-temperature cellulolytic microbial consortia in Great Boiling Spring after in situ lignocellulose enrichment. PLoS One 8:e59927. doi: 10.1371/journal.pone.0059927
  20. 20.
    Hugenholtz P, Pitulle C, Hershberger KL, Pace NR (1998) Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180:366–376PubMedCentralPubMedGoogle Scholar
  21. 21.
    Kashefi K, Holmes DE, Reysenbach AL, Lovley DR (2002) Use of Fe(III) as an electron acceptor to recover previously uncultured hyperthermophiles: isolation and characterization of Geothermobacterium ferrireducens gen. nov., sp. nov. Appl Environ Microbiol 68:1735–1742PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Dunfield PF, Tamas I, Lee KC, Morgan XC, McDonald IR, Stott MB (2012) Electing a candidate: a speculative history of the bacterial phylum OP10. Environ Microbiol 14:3069–3080. doi: 10.1111/j.1462-2920.2012.02742.x PubMedCrossRefGoogle Scholar
  23. 23.
    Hamilton-Brehm SD, Gibson RA, Green SJ, Hopmans EC, Schouten S, van der Meer MT, Shields JP, Damste JS, Elkins JG (2013) Thermodesulfobacterium geofontis sp. nov., a hyperthermophilic, sulfate-reducing bacterium isolated from Obsidian Pool, Yellowstone National Park. Extremophiles 17:251–263. doi: 10.1007/s00792-013-0512-1 PubMedCrossRefGoogle Scholar
  24. 24.
    Hamilton-Brehm SD, Mosher JJ, Vishnivetskaya T, Podar M, Carroll S, Allman S, Phelps TJ, Keller M, Elkins JG (2010) Caldicellulosiruptor obsidiansis sp. nov., an anaerobic, extremely thermophilic, cellulolytic bacterium isolated from Obsidian Pool, Yellowstone National Park. Appl Environ Microbiol 76:1014–1020. doi: 10.1128/aem.01903-09 PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Barns SM, Fundyga RE, Jeffries MW, Pace NR (1994) Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. Proc Natl Acad Sci U S A 91:1609–1613PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Elkins JG, Podar M, Graham DE, Makarova KS, Wolf Y, Randau L, Hedlund BP, Brochier-Armanet C, Kunin V, Anderson I, Lapidus A, Goltsman E, Barry K, Koonin EV, Hugenholtz P, Kyrpides N, Wanner G, Richardson P, Keller M, Stetter KO (2008) A korarchaeal genome reveals insights into the evolution of the Archaea. Proc Natl Acad Sci U S A 105:8102–8107. doi: 10.1073/pnas.0801980105 PubMedCentralPubMedCrossRefGoogle Scholar
  27. 27.
    Podar M, Makarova KS, Graham DE, Wolf YI, Koonin EV, Reysenbach AL (2013) Insights into archaeal evolution and symbiosis from the genomes of a nanoarchaeon and its inferred crenarchaeal host from Obsidian Pool, Yellowstone National Park. Biol Direct 8:9. doi: 10.1186/1745-6150-8-9 PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Vishnivetskaya TA, Raman B, Phelps TJ, Podar M, Elkins JG (2012) Cellulolytic microorganisms from thermal environments. In: Anitori RP (ed) Extremophiles: microbiology and biotechnology. Caister Academic Press, Norfolk, pp 131–158Google Scholar
  29. 29.
    Wang ZW, Hamilton-Brehm SD, Lochner A, Elkins JG, Morrell-Falvey JL (2011) Mathematical modeling of hydrolysate diffusion and utilization in cellulolytic biofilms of the extreme thermophile Caldicellulosiruptor obsidiansis. Bioresour Technol 102:3155–3162. doi: 10.1016/j.biortech.2010.10.104 PubMedCrossRefGoogle Scholar
  30. 30.
    Lochner A, Giannone RJ, Keller M, Antranikian G, Graham DE, Hettich RL (2011) Label-free quantitative proteomics for the extremely thermophilic bacterium Caldicellulosiruptor obsidiansis reveal distinct abundance patterns upon growth on cellobiose, crystalline cellulose, and switchgrass. J Proteome Res 10:5302–5314. doi: 10.1021/pr200536j PubMedCrossRefGoogle Scholar
  31. 31.
    Lochner A, Giannone RJ, Rodriguez M Jr, Shah MB, Mielenz JR, Keller M, Antranikian G, Graham DE, Hettich RL (2011) Use of label-free quantitative proteomics to distinguish the secreted cellulolytic systems of Caldicellulosiruptor bescii and Caldicellulosiruptor obsidiansis. Appl Environ Microbiol 77:4042–4054. doi: 10.1128/AEM.02811-10 PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Blumer-Schuette SE, Giannone RJ, Zurawski JV, Ozdemir I, Ma Q, Yin Y, Xu Y, Kataeva I, Poole FL 2nd, Adams MW, Hamilton-Brehm SD, Elkins JG, Larimer FW, Land ML, Hauser LJ, Cottingham RW, Hettich RL, Kelly RM (2012) Caldicellulosiruptor core and pangenomes reveal determinants for noncellulosomal thermophilic deconstruction of plant biomass. J Bacteriol 194:4015–4028. doi: 10.1128/JB.00266-12 PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Spear JR, Walker JJ, McCollom TM, Pace NR (2005) Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem. Proc Natl Acad Sci U S A 102:2555–2560. doi: 10.1073/pnas.0409574102 PubMedCentralPubMedCrossRefGoogle Scholar
  34. 34.
    Shock EL, Holland M, Meyer-Dombard DAR, Amend JP (2005) Geochemical sources of energy for microbial metabolism in hydrothermal ecosystems: Obsidian Pool, Yellowstone National Park, USA. In: Inskeep W, McDermott T (eds) Geothermal biology and geochemistry in Yellowstone National Park. Thermal Biology Institute, Montana State University, Bozeman, pp 95–112Google Scholar
  35. 35.
    Miller TL, Wolin MJ (1974) A serum bottle modification of the Hungate technique for cultivating obligate anaerobes. Appl Microbiol 27:985–987PubMedCentralPubMedGoogle Scholar
  36. 36.
    Raes J, Korbel JO, Lercher MJ, von Mering C, Bork P (2007) Prediction of effective genome size in metagenomic samples. Genome Biol 8:R10. doi: 10.1186/gb-2007-8-1-r10 PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Angly FE, Willner D, Prieto-Davà A, Edwards RA, Schmieder R, Vega-Thurber R, Antonopoulos DA, Barott K, Cottrell MT, Desnues C, Dinsdale EA, Furlan M, Haynes M, Henn MR, Hu Y, Kirchman DL, McDole T, McPherson JD, Meyer F, Miller RM, Mundt E, Naviaux RK, Rodriguez-Mueller B, Stevens R, Wegley L, Zhang L, Zhu B, Rohwer F (2009) The GAAS metagenomic tool and its estimations of viral and microbial average genome size in four major biomes. PLoS Comput Biol 5:e1000593PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Ellenbroek FM, Cappenberg TE (1991) DNA-synthesis and tritiated-thymidine incorporation by heterotrophic fresh-water bacteria in continuous culture. Appl Environ Microbiol 57:1675–1682PubMedCentralPubMedGoogle Scholar
  39. 39.
    Mackelprang R, Waldrop MP, DeAngelis KM, David MM, Chavarria KL, Blazewicz SJ, Rubin EM, Jansson JK (2011) Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw. Nature 480:368–371PubMedCrossRefGoogle Scholar
  40. 40.
    Porat I, Vishnivetskaya TA, Mosher JJ, Brandt CC, Yang ZK, Brooks SC, Liang L, Drake MM, Podar M, Brown SD, Palumbo AV (2009) Characterization of archaeal community in contaminated and uncontaminated surface stream sediments. Microb Ecol 60:784–795. doi: 10.1007/s00248-010-9734-2 CrossRefGoogle Scholar
  41. 41.
    Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145. doi: 10.1093/nar/gkn879 PubMedCentralPubMedCrossRefGoogle Scholar
  42. 42.
    Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methe B, DeSantis TZ, Petrosino JF, Knight R, Birren BW (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504. doi: 10.1101/gr.112730.110 PubMedCentralPubMedCrossRefGoogle Scholar
  43. 43.
    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267PubMedCentralPubMedCrossRefGoogle Scholar
  44. 44.
    Claesson MJ, O’Sullivan O, Wang Q, Nikkila J, Marchesi JR, Smidt H, de Vos WM, Ross RP, O’Toole PW (2009) Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLoS One 4:e6669. doi: 10.1371/journal.pone.0006669 PubMedCentralPubMedCrossRefGoogle Scholar
  45. 45.
    Meyer F, Paarmann D, D’Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA (2008) The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9. doi: 10.1186/1471-2105-9-386
  46. 46.
    Parks DH, Beiko RG (2010) Identifying biologically relevant differences between metagenomic communities. Bioinformatics 26:715–721. doi: 10.1093/bioinformatics/btq041 PubMedCrossRefGoogle Scholar
  47. 47.
    Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48:443–453PubMedCrossRefGoogle Scholar
  48. 48.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi: 10.1128/aem.01541-09 PubMedCentralPubMedCrossRefGoogle Scholar
  49. 49.
    Lozupone C, Hamady M, Knight R (2006) UniFrac - an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinforma 7:371–385. doi: 10.1186/1471-2105-7-371 CrossRefGoogle Scholar
  50. 50.
    Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. doi: 10.1128/aem.71.12.8228-8235.2005 PubMedCentralPubMedCrossRefGoogle Scholar
  51. 51.
    Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  52. 52.
    Fournier RO (1989) Geochemistry and dynamics of the Yellowstone National Park hydrothermal system. Annu Rev Earth Planet Sci 17:13–53. doi: 10.1146/annurev.earth.17.1.13 CrossRefGoogle Scholar
  53. 53.
    Kennedy BM, Lynch MA, Reynolds JH, Smith SP (1985) Intensive sampling of noble-gases in fluids at Yellowstone. 1. Early overview of the data - regional patterns. Geochim Cosmochim Acta 49:1251–1261. doi: 10.1016/0016-7037(85)90014-6 CrossRefGoogle Scholar
  54. 54.
    White DE (1981) Active geothermal systems and hydrothermal ore deposits. Economic geology 75th anniversary volumeGoogle Scholar
  55. 55.
    Meyer-Dombard DR, Shock EL, Amend JP (2005) Archaeal and bacterial communities in geochemically diverse hot springs of Yellowstone National Park, USA. Geobiology 3:211–227. doi: 10.1111/j.1472-4669.2005.00052.x CrossRefGoogle Scholar
  56. 56.
    Cole JK, Peacock JP, Dodsworth JA, Williams AJ, Thompson DB, Dong HL, Wu G, Hedlund BP (2013) Sediment microbial communities in Great Boiling Spring are controlled by temperature and distinct from water communities. ISME J 7:718–729. doi: 10.1038/ismej.2012.157 PubMedCentralPubMedCrossRefGoogle Scholar
  57. 57.
    Stout RG, Al-Niemi TS (2002) Heat-tolerant flowering plants of active geothermal areas in Yellowstone National Park. Ann Bot 90:259–267PubMedCentralPubMedCrossRefGoogle Scholar
  58. 58.
    Ogg CD, Patel BKC (2009) Caloramator australicus sp nov., a thermophilic, anaerobic bacterium from the Great Artesian Basin of Australia. Int J Syst Evol Microbiol 59:95–101. doi: 10.1099/ijs.0.000802-0 PubMedCrossRefGoogle Scholar
  59. 59.
    Orlygsson J, Sigurbjornsdottir MA, Bakken HE (2010) Bioprospecting thermophilic ethanol and hydrogen producing bacteria from hot springs in Iceland. Icel Agric Sci 23:73–85Google Scholar
  60. 60.
    Vanfossen AL, Verhaart MR, Kengen SM, Kelly RM (2009) Carbohydrate utilization patterns for the extremely thermophilic bacterium Caldicellulosiruptor saccharolyticus reveal broad growth substrate preferences. Appl Environ Microbiol 75:7718–7724PubMedCentralPubMedCrossRefGoogle Scholar
  61. 61.
    Blumer-Schuette SE, Giannone RJ, Zurawski JV, Ozdemir I, Ma Q, Yin YB, Xu Y, Kataeva I, Poole FL, Adams MWW, Hamilton-Brehm SD, Elkins JG, Larimer FW, Land ML, Hauser LJ, Cottingham RW, Hettich RL, Kelly RM (2012) Caldicellulosiruptor core and pangenomes reveal determinants for noncellulosomal thermophilic deconstruction of plant biomass. J Bacteriol 194:4015–4028. doi: 10.1128/jb.00266-12 PubMedCentralPubMedCrossRefGoogle Scholar
  62. 62.
    Yang S-J, Kataeva I, Wiegel J, Yin Y, Dam P, Xu Y, Westpheling J, Adams MWW (2009) eclassification of ‘Anaerocellum thermophilum’ as Caldicellulosiruptor bescii strain DSM 6725T sp. nov. Int J Syst Evol Microbiol. doi: 10.1099/ijs.0.017731-0, ijs.0.017731-017730Google Scholar
  63. 63.
    Mathrani IM, Ahring BK (1992) Thermophilic and alkalophilic xylanases from several Dictyoglomus isolates. Appl Microbiol Biotechnol 38:23–27CrossRefGoogle Scholar
  64. 64.
    Mathrani IM, Ahring BK (1991) Isolation and characterization of a strictly xylan-degrading Dictyoglomus from a man-made, thermophilic anaerobic environment. Arch Microbiol 157:13–17CrossRefGoogle Scholar
  65. 65.
    Podosokorskaya OA, Merkel AY, Kolganova TV, Chernyh NA, Miroshnichenko ML, Bonch-Osmolovskaya EA, Kublanov IV (2011) Fervidobacterium reparium sp. nov., a thermophilic anaerobic cellulolytic bacterium isolated from a hot spring. Int J Syst Evol Microbiol. doi: 10.1099/ijs.0.026070-0 Google Scholar

Copyright information

© Springer Science+Business Media New York (outside the USA) 2014

Authors and Affiliations

  • Tatiana A. Vishnivetskaya
    • 1
    • 2
  • Scott D. Hamilton-Brehm
    • 1
    • 3
  • Mircea Podar
    • 1
  • Jennifer J. Mosher
    • 1
    • 4
  • Anthony V. Palumbo
    • 1
  • Tommy J. Phelps
    • 1
  • Martin Keller
    • 1
  • James G. Elkins
    • 1
  1. 1.BioEnergy Science Center, Biosciences DivisionOak Ridge National LaboratoryOak RidgeUSA
  2. 2.Center for Environmental BiotechnologyUniversity of TennesseeKnoxvilleUSA
  3. 3.Division of Earth and Ecosystem SciencesDesert Research InstituteLas VegasUSA
  4. 4.Department of Biological SciencesMarshall UniversityHuntingtonUSA

Personalised recommendations