Extremophilic nitrite-oxidizing Chloroflexi from Yellowstone hot springs.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
02 2020
02 2020
Historique:
received:
26
02
2019
accepted:
06
09
2019
revised:
03
08
2019
pubmed:
19
10
2019
medline:
9
4
2020
entrez:
19
10
2019
Statut:
ppublish
Résumé
Nitrifying microorganisms occur across a wide temperature range from 4 to 84 °C and previous studies in geothermal systems revealed their activity under extreme conditions. Archaea were detected to be responsible for the first step of nitrification, but it is still a challenging issue to clarify the identity of heat-tolerant nitrite oxidizers. In a long-term cultivation approach, we inoculated mineral media containing ammonium and nitrite as substrates with biofilms and sediments of two hot springs in Yellowstone National Park (USA). The nitrifying consortia obtained at 70 °C consisted mostly of novel Chloroflexi as revealed by metagenomic sequencing. Among these, two deep-branching novel Chloroflexi were identified as putative nitrite-oxidizing bacteria (NOB) by the presence of nitrite oxidoreductase encoding genes in their genomes. Stoichiometric oxidation of nitrite to nitrate occurred under lithoautotrophic conditions, but was stimulated by organic matter. Both NOB candidates survived long periods of starvation and the more abundant one formed miniaturized cells and was heat resistant. This detection of novel thermophilic NOB exemplifies our still incomplete knowledge of nitrification, and indicates that nitrite oxidation might be an ancient and wide-spread form of energy conservation.
Identifiants
pubmed: 31624340
doi: 10.1038/s41396-019-0530-9
pii: 10.1038/s41396-019-0530-9
pmc: PMC6976673
doi:
Substances chimiques
Ammonium Compounds
0
Nitrates
0
Nitrites
0
Oxidoreductases
EC 1.-
nitrite dehydrogenase
EC 1.7.3.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
364-379Références
Alawi M, Lipski A, Sanders T, Eva-Maria-Pfeiffer, Spieck E. Cultivation of a novel cold-adapted nitrite oxidizing betaproteobacterium from the Siberian Arctic. ISME J. 2007;1:256–64.
pubmed: 18062041
Reigstad LJ, Richter A, Daims H, Urich T, Schwark L, Schleper C. Nitrification in terrestrial hot springs of Iceland and Kamchatka. FEMS Microbiol Ecol. 2008;64:167–74.
pubmed: 18355293
Spieck E, Bock E. The lithoautotrophic nitrite-oxidizing bacteria. In: Garrity G, Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s manual of systematic bacteriology. Berlin/Heidelberg, Germany: Springer-Verlag; 2005. p. 149–53.
Ehrich S, Behrens D, Lebedeva E, Ludwig W, Bock E. A new obligately chemolithoautotrophic, nitrite-oxidizing bacterium, Nitrospira moscoviensis sp. nov. and its phylogenetic relationship. Arch Microbiol. 1995;164:16–23.
pubmed: 7646315
Lücker S, Nowka B, Rattei T, Spieck E, Daims H. The genome of Nitrospina gracilis illuminates the metabolism and evolution of the major marine nitrite oxidizer. Front Microbiol. 2013;4:3–19.
Sorokin DY, Lücker S, Vejmelkova D, Kostrikina NA, Kleerebezem R, WIC Rijpstra, et al. Nitrification expanded: discovery, physiology and genomics of a nitrite-oxidizing bacterium from the phylum Chloroflexi. ISME J. 2012;6:2245–56.
pubmed: 22763649
pmcid: 3504966
Hedlund B, Thomas S, Dodsworth J, Zhang C. Life in high-temperature environments. In: Yates M, Nakatsu C, Miller R, Pillai S, editors. Manual of environmental microbiology, 4th ed. Washington, DC., USA: ASM Press; 2016. p. 4.3.4-1–4.3.4-15. https://doi.org/10.1128/9781555818821.ch4.3.4 .
Dodsworth J, Hungate B, Hedlund BP. Ammonia oxidation, denitrification and dissimilatory nitrate reduction to ammonium in two US Great Basin hot springs with abundant ammonia-oxidizing archaea. Environ Microbiol. 2011;13:2371–86.
pubmed: 21631688
Inskeep WP, Ackerman GG, Taylor WP, Kozubal M, Korf S, Macur RE. On the energetics of chemolithotropy in nonequilibrium systems: case studies of geothermal springs in Yellowstone National Park. Geobiology. 2005;3:297–317.
Dodsworth JA, McDonald AI, Hedlund BP. Calculation of total free energy yield as an alternative approach for predicting the importance of potential chemolithotrophic reactions in geothermal springs. FEMS Microbiol Ecol. 2012;81:446–54.
pubmed: 22443686
de la Torre JR, Walker CB, Ingalls AE, Könneke M, Stahl DA. Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol. 2008;10:810–8.
pubmed: 18205821
Abby SS, Melcher M, Kerou M, Krupovic M, Stieglmeier M, Rossel C, et al. Candidatus Nitrosocaldus cavascurensis, an ammonia oxidizing, extremely thermophilic archaeon with a highly mobile genome. Front Microbiol. 2018;9:1–19.
Daebeler A, Herbold CW, Vierheilig J, Sedlacek CJ, Pjevac P, Albertsen M, et al. Cultivation and genomic analysis of ‘Candidatus Nitrosocaldus islandicus,’ an obligately thermophilic, ammonia-oxidizing thaumarchaeon from a hot spring biofilm in Graendalur valley, Iceland. Front Microbiol. 2018;9:1–16.
Becraft ED, Dodsworth JA, Murugapiran SK, Ohlsson JI, Briggs BR, Kanbar J, et al. Single-cell-genomics-facilitated read binning of candidate phylum EM19 genomes from geothermal spring metagenomes. Appl Environ Microbiol. 2016;82:992–1003.
pubmed: 26637598
pmcid: 4751853
Lebedeva EV, Off S, Zumbrägel S, Kruse M, Shagzhina A, Lücker S, et al. Isolation and characterization of a moderately thermophilic nitrite-oxidizing bacterium from a geothermal spring. FEMS Microbiol Ecol. 2011;75:195–204.
pubmed: 21138449
Edwards TA, Calica NA, Huang DA, Manoharan N, Hou W, Huang L, et al. Cultivation and characterization of thermophilic Nitrospira species from geothermal springs in the US Great Basin, China, and Armenia. FEMS Microbiol Ecol. 2013;85:283–92.
pubmed: 23528039
Kits KD, Sedlacek CJ, Lebedeva EV, Han P, Bulaev A, Pjevac P, et al. Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle. Nature. 2017;549:269–72.
pubmed: 28847001
pmcid: 5600814
Hugenholtz P, Pitulle C, Hershberger KL, Pace NR. Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol. 1998;180:366–76.
pubmed: 9440526
pmcid: 106892
Meyer-Dombard DR, Shock EL, Amend JP. Archaeal and bacterial communities in geochemically diverse hot springs of Yellowstone National Park, USA. Geobiology. 2005;3:211–27.
Hedlund BP, Murugapiran SK, Alba TW, Levy A, Dodsworth JA, Goertz GB, et al. Uncultivated thermophiles: current status and spotlight on ‘Aigarchaeota’. Curr Opin Microbiol. 2015;25:136–45.
pubmed: 26113243
Kato S, Sakai S, Hirai M, Tasumi E, Nishizawa M, Suzuki K, et al. Long-term cultivation and metagenomics reveal ecophysiology of previously uncultivated Thermophiles involved in biogeochemical nitrogen cycle. Microbes Environ. 2018;33:107–10.
pubmed: 29459499
pmcid: 5877337
Krümmel A, Harms H. Effect of organic matter on growth and cell yield of ammonia-oxidizing bacteria. Arch Microbiol. 1982;133:50–54.
Spieck E, Lipski A. Cultivation, growth physiology, and chemotaxonomy of nitrite-oxidizing bacteria. In: Klotz MG, editor. Methods in enzymology. 1st ed. Oxford, UK: Academic Press/Elsevier Inc.; 2011. p. 109–30.
Widdel F, Bak F. Gram-negative mesophilic sulfate-reducing bacteria. The Prokaryotes. New York, NY, USA: Springer New York; 1992. p. 3352–78.
Amann R, Ludwig W, Schleifer K. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev. 1995;59:143–69.
pubmed: 7535888
pmcid: 239358
Manz W, Amann R, Ludwig W, Wagner M, Schleifer K-H. Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Syst Appl Microbiol. 1992;15:593–600.
Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol. 1990;56:1919–25.
pubmed: 184531
pmcid: 184531
Wallner G, Amann R, Beisker W. Optimizing fluorescent in situ hybridization with rRNA‐targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry. 1993;14:136–43.
pubmed: 7679962
Taylor S, Ninjoor V, Dowd DM, Tappel AL. Cathepsin B2 measurement by sensitive fluorometric ammonia analysis. Anal Biochem. 1974;60:153–62.
pubmed: 4850914
Corbin JL. Liquid chromatographic-fluorescence determination of ammonia from nitrogenase reactions: A 2 min assay. Appl Environ Microbiol. 1984;47:1027–30.
pubmed: 16346533
pmcid: 16346533
Schmidt EL, Belser LW. Autotrophic nitrifying bacteria. In: Weaver RW, Angle JS, Bottomley PJ, editors. Methods of soil analysis. Part 2-microbiological and biochemical properties. Madison, WI, USA: Soil Science Society of America; 1994. p. 159–77.
Sambrook J, Green MR, editors. Extracting DNA from gram-negative bacteria. Molecular cloning: a laboratory manual, 4th ed. New York, NY: Cold Spring Harbor Laboratory Press; 2012 p. 19–20.
Rotthauwe J, Witzel K, Liesack W. The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol. 1997;63:4704–12.
pubmed: 9406389
pmcid: 168793
Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA. 2005;102:14683–8.
pubmed: 16186488
Pester M, Maixner F, Berry D, Rattei T, Koch H, Lücker S, et al. NxrB encoding the beta subunit of nitrite oxidoreductase as functional and phylogenetic marker for nitrite-oxidizing Nitrospira. Environ Microbiol. 2014;16:3055–71.
pubmed: 24118804
Poly F, Wertz S, Brothier E, Degrange V. First exploration of Nitrobacter diversity in soils by a PCR cloning-sequencing approach targeting functional gene nxrA. FEMS Microbiol Ecol. 2008;63:132–40.
pubmed: 18031541
Lane DJ. 16/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M, editors. Nucleic acid techniques in bacterial systematics. Chichester, UK: John Wiley & Sons; 1991. p. 115–71.
Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar A, et al. ARB: a software environment for sequence data. Nucleic Acids Res. 2004;32:1363–71.
pubmed: 14985472
pmcid: 390282
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–D596.
Herlemann DP, Labrenz M, Jürgens K, Bertilsson S, Waniek JJ, Andersson AF. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J. 2011;5:1571–9.
pubmed: 21472016
pmcid: 3176514
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci. 2011;108:4516–22.
pubmed: 20534432
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.
pubmed: 20383131
pmcid: 20383131
Dowd SE, Sun Y, Wolcott RD, Domingo A, Carroll JA. Bacterial tag–encoded FLX amplicon pyrosequencing (bTEFAP) for microbiome studies: Bacterial diversity in the ileum of newly weaned Salmonella-infected pigs. Foodborne Pathog Dis. 2008;5:459–72.
pubmed: 18713063
Bushnell B. BBMap short read aligner. Berkeley, CA.: University of California; 2016. http://sourceforge.net/projects/bbmap .
Nikolenko SI, Korobeynikov AI, Alekseyev MA. BayesHammer: Bayesian clustering for error correction in single-cell sequencing. BMC Genomics. 2013;14:S7.
pubmed: 23368723
pmcid: 23368723
Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. MetaSPAdes: a new versatile metagenomic assembler. Genome Res. 2017;27:824–34.
pubmed: 28298430
pmcid: 5411777
Li H, Durbin R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics. 2010;26:589–95.
pubmed: 20080505
pmcid: 20080505
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078–9.
pubmed: 2723002
pmcid: 2723002
Graham ED, Heidelberg JF, Tully BJ. BinSanity: unsupervised clustering of environmental microbial assemblies using coverage and affinity propagation. PeerJ. 2017;5:e3035.
pubmed: 28289564
pmcid: 5345454
Lu YY, Chen T, Fuhrman JA, Sun F, Sahinalp C. COCACOLA: binning metagenomic contigs using sequence COmposition, read CoverAge, CO-alignment and paired-end read LinkAge. Bioinformatics. 2017;33:791–8.
pubmed: 27256312
Alneberg J, Bjarnason BS, De Bruijn I, Schirmer M, Quick J, Ijaz UZ, et al. Binning metagenomic contigs by coverage and composition. Nat Methods. 2014;11:1144–6.
pubmed: 25218180
Wu YW, Simmons BA, Singer SW. MaxBin 2.0: An automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics. 2015;32:605–7.
pubmed: 26515820
Kang DD, Froula J, Egan R, Wang Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ. 2015;3:e1165.
pubmed: 26336640
pmcid: 4556158
Sieber CMK, Probst AJ, Sharrar A, Thomas BC, Hess M, Tringe SG, et al. Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy. Nat Microbiol. 2018;3:836–43.
pubmed: 29807988
pmcid: 6786971
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.
pubmed: 25977477
pmcid: 4484387
Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–9.
pubmed: 24642063
pmcid: 24642063
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10.
Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 2007;35:W182–W185.
pubmed: 17526522
pmcid: 1933193
Guindon S, Delsuc F, Dufayard JF, Gascuel O. Estimating maximum likelihood phylogenies with PhyML. Methods Mol Biol. 2009;537:113–37.
pubmed: 19378142
Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–4.
pubmed: 12912839
Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–3.
pubmed: 3998144
pmcid: 3998144
Na SI, Kim YO, Yoon SH, Ha Smin, Baek I, Chun J. UBCG: Up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol. 2018;56:281–5.
Olm MR, Brown CT, Brooks B, Banfield JF. DRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. 2017;11:2864–8.
pubmed: 28742071
pmcid: 5702732
Lagkouvardos I, Joseph D, Kapfhammer M, Giritli S, Horn M, Haller D, et al. IMNGS: a comprehensive open resource of processed 16S rRNA microbial profiles for ecology and diversity studies. Sci Rep. 2016;6:33721.
pubmed: 27659943
pmcid: 5034312
Dodsworth JA, Gevorkian J, Despujos F, Cole JK, Murugapiran SK, Ming H, et al. Thermoflexus hugenholtzii gen. nov., sp. nov., a thermophilic, microaerophilic, filamentous bacterium representing a novel class in the Chloroflexi, Thermoflexia classis nov., and description of Thermoflexaceae fam. nov. and Thermoflexales ord. nov. Int J Syst Evol Microbiol. 2014;64:2119–27.
pubmed: 24676733
Jackson TJ, Ramaley RF, Meinschein WG. Thermomicrobium, a new genus of extremely thermophilic bacteria. Int J Syst Bacteriol. 1973;23:28–36.
King CE, King GM. Thermomicrobium carboxidum sp. nov., and Thermorudis peleae gen. nov., sp. nov., carbon monoxide-oxidizing bacteria isolated from geothermally heated biofilms. Int J Syst Evol Microbiol. 2014;64:2586–92.
pubmed: 24814334
Herbold CW, Lee CK, McDonald IR, Cary SC. Evidence of global-scale aeolian dispersal and endemism in isolated geothermal microbial communities of Antarctica. Nat Commun. 2014;5:1–10.
Meincke M, Bock E, Kastrau D, Kroneck PMH. Nitrite oxidoreductase from Nitrobacter hamburgensis: redox centers and their catalytic role. Arch Microbiol. 1992;158:127–31.
Lücker S, Wagner M, Maixner F, Pelletier E, Koch H, Vacherie B, et al. A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc Natl Acad Sci. 2010;107:13479–84.
pubmed: 20624973
Kirstein K, Bock E. Close genetic relationship between Nitrobacter hamburgensis nitrite oxidoreductase and Escherichia coli nitrate reductases. Arch Microbiol. 1993;160:447–53.
pubmed: 8297210
Kitzinger K, Koch H, Lücker S, Sedlacek CJ, Herbold C, Schwarz J, et al. Characterization of the first “Candidatus Nitrotoga” isolate reveals metabolic versatility and separate evolution of widespread nitrite-oxidizing bacteria. mBio. 2018;9:1–16.
Anantharaman K, Brown CT, Hug LA, Sharon I, Castelle CJ, Probst AJ, et al. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat Commun. 2016;7:1–11.
Hedlund BP, Dodsworth JA, Murugapiran SK, Rinke C, Woyke T. Impact of single-cell genomics and metagenomics on the emerging view of extremophile “microbial dark matter”. Extremophiles. 2014;18:865–75.
pubmed: 25113821
Takami H, Noguchi H, Takaki Y, Uchiyama I, Toyoda A, Nishi S, et al. A deeply branching thermophilic bacterium with an ancient acetyl-CoA pathway dominates a subsurface ecosystem. PLoS ONE. 2012;7.
pubmed: 22303444
pmcid: 3267732
Nunoura T, Takaki Y, Kakuta J, Nishi S, Sugahara J, Kazama H, et al. Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res. 2011;39:3204–23.
pubmed: 21169198
Hugenholtz P, Stackebrandt E. Reclassification of Sphaerobacter thermophilus from the subclass Sphaerobacteridae in the phylum Actinobacteria to the class Thermomicrobia (emended description) in the phylum Chloroflexi (emended description). Int J Syst Evol Microbiol. 2004;54:2049–51.
pubmed: 15545432
Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. 2016.
Daims H, Lücker S, Le Paslier D, Wagner M. Diversity, environmental genomics, and ecophysiology of nitrite-oxidizing bacteria. In: Ward BB, Klotz MG, Arp DJ, editors. Nitrification. Washington, DC, USA: ASM Press; 2011. p. 295–322.
Bock E. Growth of Nitrobacter in the presence of organic matter. Arch Microbiol. 1976;108:305–12.
pubmed: 942282
Lipski A, Spieck E, Makolla A, Altendorf K. Fatty acid profiles of nitrite-oxidizing bacteria reflect their phylogenetic heterogeneity. Syst Appl Microbiol. 2001;24:377–84.
pubmed: 11822673
Kim J-G, Park S-J, Sinninghe Damsté JS, Schouten S, Rijpstra WIC, Jung M-Y, et al. Hydrogen peroxide detoxification is a key mechanism for growth of ammonia-oxidizing archaea. Proc Natl Acad Sci. 2016;113:7888–93.
pubmed: 27339136
Nunoura T, Chikaraishi Y, Izaki R, Suwa T, Sato T, Harada T, et al. A primordial and reversible TCA cycle in a facultatively chemolithoautotrophic thermophile. Science. 2018;359:559–63.
pubmed: 29420286
Mall A, Sobotta J, Huber C, Tschirner C, Kowarschik S, Bačnik K, et al. Reversibility of citrate synthase allows autotrophic growth of a thermophilic bacterium. Science. 2018;359:563–7.
pubmed: 29420287
Pati A, la Butti K, Pukall R, Nolan M, del Rio TG, Tice H, et al. Complete genome sequence of Sphaerobacter thermophilus type strain (S 6022 T). Stand Genom Sci. 2010;2:49–56.
Yabe S, Aiba Y, Sakai Y, Hazaka M, Yokota A. A life cycle of branched aerial mycelium- and multiple budding spore-forming bacterium Thermosporothrix hazakensis belonging to the phylum Chloroflexi. J Gen Appl Microbiol. 2010;56:137–41.
pubmed: 20513961
Filippidou S, Junier T, Wunderlin T, Kooli WM, Palmieri I, Al-Dourobi A, et al. Adaptive strategies in a poly-extreme environment: differentiation of vegetative cells in Serratia ureilytica and resistance to extreme conditions. Front Microbiol. 2019;10:1–13.
Suzina NE, Mulyukin AL, Kozlova AN, Shorokhova AP, Dmitriev VV, Barinova ES, et al. Ultrastructure of resting cells of some non-spore-forming bacteria. Microbiology. 2004;73:435–47.
Meyer-Dombard DR, Swingley W, Raymond J, Havig J, Shock EL, Summons RE. Hydrothermal ecotones and streamer biofilm communities in the Lower Geyser Basin, Yellowstone National Park. Environ Microbiol. 2011;13:2216–31.
pubmed: 21453405
Yamada T, Sekiguchi Y. Cultivation of uncultured chloroflexi subphyla: significance and ecophysiology of formerly uncultured chloroflexi ‘subphylum i’ with natural and biotechnological relevance. Microbes Environ. 2009;24:205–16.
pubmed: 21566375
Miller SR, Strong AL, Jones KL, Ungerer MC. Bar-coded pyrosequencing reveals shared bacterial community properties along the temperature gradients of two alkaline hot springs in Yellowstone National Park. Appl Environ Microbiol. 2009;75:4565–72.
pubmed: 19429553
pmcid: 2704827
Watsuji T, Kato T, Ueda K, Beppu T. CO2 supply induces the growth of Symbiobacterium thermophilum, a syntrophic bacterium. Biosci Biotechnol Biochem. 2006;70:753–6.
pubmed: 16557001
Stewart EJ. Growing unculturable bacteria. J Bacteriol. 2012;194:4151–60.
pubmed: 22661685
pmcid: 3416243
Overmann J, Abt B, Sikorski J. Present and future of culturing bacteria. Annu Rev Microbiol. 2017;71:711–30.
pubmed: 28731846
Inskeep W. The YNP metagenome project: environmental parameters responsible for microbial distribution in the Yellowstone geothermal ecosystem. Front Microbiol. 2013;4:1–15.