Phylogenetically and physiologically diverse methanogenic archaea inhabit the Indian hot spring environments.
Archaea
Diversity
Ecology
Phylogeny
Taxonomy
Journal
Archives of microbiology
ISSN: 1432-072X
Titre abrégé: Arch Microbiol
Pays: Germany
ID NLM: 0410427
Informations de publication
Date de publication:
14 Sep 2023
14 Sep 2023
Historique:
received:
24
03
2023
accepted:
15
08
2023
revised:
10
08
2023
medline:
15
9
2023
pubmed:
14
9
2023
entrez:
14
9
2023
Statut:
epublish
Résumé
Mesophilic and thermophilic methanogens belonging to the hydrogenotrophic, methylotrophic, and acetotrophic groups were isolated from Indian hot spring environments using BY and BCYT growth media. Following initial Hinf I-based PCR-RFLP screening, 70 methanogens were sequenced to ascertain their identity. These methanogens were phylogenetically and physiologically diverse and represented different taxa distributed across three physiological groups, i.e., hydrogenotrophs (53), methylotrophs (14) and acetotrophs (3). Overall, methanogens representing three families, five genera, and ten species, including two putative novel species, were recognized. The highest number and diversity of methanogens was observed at 40 ℃, dominated by Methanobacterium (10; 3 species), Methanosarcina (9; 3 species), Methanothermobacter (7; 2 species), Methanomethylovorans (5; 1 species) and Methanoculleus (3; 1 species). Both putative novel methanogen species were isolated at 40 ℃ and belonged to the genera Methanosarcina and Methanobacterium. At 55 ℃, limited diversity was observed, and resulted in the isolation of only two genera of methanogens, i.e., Methanothermobacter (28; 2 species) and Methanosarcina (4; 1 species). At 70 ℃, only members of the genus Methanothermobacter (5; 2 species) were isolated, whereas no methanogen could be cultured at 85 ℃. Ours is the first study that documents the extensive range of cultivable methanogenic archaea inhabiting hot springs across various geothermal provinces of India.
Identifiants
pubmed: 37707605
doi: 10.1007/s00203-023-03661-2
pii: 10.1007/s00203-023-03661-2
doi:
Substances chimiques
Culture Media
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
332Subventions
Organisme : University Grants Commission
ID : Ref. No. 23/06/2013(i)EU-V
Organisme : Science and Engineering Research Board
ID : YSS/2015/000718
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Aller JY, Kemp PF (2008) Are Archaea inherently less diverse than Bacteria in the same environments? FEMS Microbiol Ecol. https://doi.org/10.1111/j.1574-6941.2008.00498.x
doi: 10.1111/j.1574-6941.2008.00498.x
pubmed: 18479447
Berghuis BA, Yu B, Schulz F, Blainey PC, Woyke T, Quake SR (2019) Hydrogenotrophic methanogenesis in archaeal phylum Verstraetearchaeota reveals the shared ancestry of all methanogens. PNAS 116(11):5037–5044. https://doi.org/10.1073/pnas.1815631116
doi: 10.1073/pnas.1815631116
pubmed: 30814220
pmcid: 6421429
Boone DR (2015a) Methanobacterium. Bergey’s manual of systematics of archaea and bacteria, pp 1–8. https://doi.org/10.1002/9781118960608.gbm00495
Boone DR (2015b) Methanothermobacter. Bergey’s manual of systematics of archaea and bacteria, pp 1–8. https://doi.org/10.1002/9781118960608.gbm00498
Boone DR, Whitman WB, Koga Y (2015a) Methanobacteriaceae. Bergey’s manual of systematics of archaea and bacteria, vol 11, p 1. https://doi.org/10.1002/9781118960608.fbm00097
Boone DR, Whitman WB, Koga Y (2015b) Methanomicrobiaceae. Bergey’s manual of systematics of archaea and bacteria, pp 1–2. https://doi.org/10.1002/9781118960608.fbm00102
Boone DR, Whitman WB, Koga Y (2015c) Methanosarcinaceae. Bergey’s manual of systematics of archaea and bacteria, vol 448, pp 1–2. https://doi.org/10.1002/9781118960608.fbm00105
Brody JR, Kern SE (2004) Sodium boric acid: a Tris-free, cooler conductive medium for DNA electrophoresis. Biotechniques 36(2):214–216. https://doi.org/10.2144/04362BM02
doi: 10.2144/04362BM02
pubmed: 14989083
Cheng L, Qiu TL, Yin XB, Wu XL, Hu GQ, Deng Y, Zhang H (2007) Methermicoccus shengliensis gen. nov., sp. nov., a thermophilic, methylotrophc methanogen isolated from oil-production water, and proposal of Methermicoccaceae fam. nov. Int J Syst Evol Microbiol 57(12):2964–2969. https://doi.org/10.1099/IJS.0.65049-0
doi: 10.1099/IJS.0.65049-0
pubmed: 18048758
Cheng L, Wu K, Zhou L, Tahon G, Liu L, Li J, Zhang J, Zheng F, Deng C, Han W, Bai LP (2023) Isolation of a methyl-reducing methanogen outside the Euryarchaeota. Res Square. https://doi.org/10.21203/RS.3.RS-2501667/V1
Demirel B, Scherer P (2008) The roles of acetotrophic and hydrogenotrophic methanogens during anaerobic conversion of biomass to methane: a review. Rev Environ Sci Biotechnol 7(2):173–190. https://doi.org/10.1007/S11157-008-9131-1/METRICS
doi: 10.1007/S11157-008-9131-1/METRICS
Deppenmeier U, Müller V (2008) Life close to the thermodynamic limit: how methanogenic archaea conserve energy. Bioenerg Energy Conserv Convers. https://doi.org/10.1007/400_2006_026
doi: 10.1007/400_2006_026
Doyle J (1991) DNA protocols for plants. In: Molecular techniques in taxonomy, pp 283–293. https://doi.org/10.1007/978-3-642-83962-7_18
Enzmann F, Mayer F, Rother M, Holtmann D (2018) Methanogens: biochemical background and biotechnological applications. AMB Express 8(1):1–22. https://doi.org/10.1186/S13568-017-0531-X
doi: 10.1186/S13568-017-0531-X
pubmed: 29302756
pmcid: 5754280
Evans PN, Parks DH, Chadwick GL, Robbins SJ, Orphan VJ, Golding SD, Tyson GW (2015) Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350(6259):434–438. https://doi.org/10.1126/SCIENCE.AAC7745
doi: 10.1126/SCIENCE.AAC7745
pubmed: 26494757
Ferry JG (2011) Fundamentals of methanogenic pathways that are key to the biomethanation of complex biomass. Curr Opin Biotechnol 22(3):351–357. https://doi.org/10.1016/j.copbio.2011.04.011
doi: 10.1016/j.copbio.2011.04.011
pubmed: 21555213
pmcid: 3606815
Flemming HC, Wuertz S (2019) Bacteria and archaea on Earth and their abundance in biofilms. Nat Rev Microbiol 17(4):247–260. https://doi.org/10.1038/s41579-019-0158-9
doi: 10.1038/s41579-019-0158-9
pubmed: 30760902
Franzmann PD, Liu Y, Balkwill DL, Aldrich HC, Conway De Macario E, Boone DR (1997) Methanogenium frigidum sp. nov., a psychrophilic, H2-using methanogen from Ace Lake, Antarctica. Int J Syst Bacteriol 47(4):1068–1072. https://doi.org/10.1099/00207713-47-4-1068/
doi: 10.1099/00207713-47-4-1068/
pubmed: 9336907
Garcia JL, Patel BKC, Ollivier B (2000) Taxonomic, phylogenetic, and ecological diversity of methanogenic archaea. Anaerobe 6(4):205–226. https://doi.org/10.1006/ANAE.2000.0345
doi: 10.1006/ANAE.2000.0345
pubmed: 16887666
Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41(8):95–98
Hatzenpichler R (2023) Cultivation and visualization of a methanogen of the phylum Thermoproteota. Res Square. https://doi.org/10.21203/rs.3.rs-2500102/v1
Hays LE, Graham HV, Des Marais DJ, Hausrath EM, Horgan B, McCollom TM, Parenteau MN, Potter-McIntyre SL, Williams AJ, Lynch KL (2017) Biosignature preservation and detection in mars analog environments. Astrobiology 17(4):363–400. https://doi.org/10.1089/AST.2016.1627
doi: 10.1089/AST.2016.1627
pubmed: 28177270
pmcid: 5478115
Hoehler T, Gunsalus RP, McInerney MJ (2010) Environmental constraints that limit methanogenesis. In: Handbook of hydrocarbon and lipid microbiology, pp 635–654. https://doi.org/10.1007/978-3-540-77587-4_51
Ishii S, Kosaka T, Hori K, Hotta Y, Watanabe K (2005) Coaggregation facilitates interspecies hydrogen transfer between Pelotomaculum thermopropionicum and Methanothermobacter thermautotrophicus. Appl Environ Microbiol 71(12):7838–7845. https://doi.org/10.1128/AEM.71.12.7838-7845.2005
doi: 10.1128/AEM.71.12.7838-7845.2005
pubmed: 16332758
pmcid: 1317437
Jabłoński S, Rodowicz P, Łukaszewicz M (2015) Methanogenic archaea database containing physiological and biochemical characteristics. Int J Syst Evolut Microbiol 65(Pt_4):1360–1368. https://doi.org/10.1099/IJS.0.000065/
doi: 10.1099/IJS.0.000065/
Jardine JL, Stoychev S, Mavumengwana V, Ubomba-Jaswa E (2018) Screening of potential bioremediation enzymes from hot spring bacteria using conventional plate assays and liquid chromatography - Tandem mass spectrometry (Lc-Ms/Ms). J Environ Manage 223:787–796. https://doi.org/10.1016/J.JENVMAN.2018.06.089
doi: 10.1016/J.JENVMAN.2018.06.089
pubmed: 29986326
Jarman SN (2006) Cleaver: software for identifying taxon specific restriction endonuclease recognition sites. Bioinformatics (oxford, England) 22(17):2160–2161. https://doi.org/10.1093/BIOINFORMATICS/BTL330
doi: 10.1093/BIOINFORMATICS/BTL330
pubmed: 16787976
Jiang B, Parshina SN, van Doesburg W, Lomans BP, Stams AJM (2005) Methanomethylovorans thermophila sp. nov., a thermophilic, methylotrophic methanogen from an anaerobic reactor fed with methanol. Int J Syst Evolut Microbiol 55(6):2465–2470. https://doi.org/10.1099/IJS.0.63818-0
doi: 10.1099/IJS.0.63818-0
Joblin, K. N. (2005). Methanogenic archaea. In: Methods in gut microbial ecology for ruminants, pp 47–53. https://doi.org/10.1007/1-4020-3791-0_4
Joshi A, Lanjekar V, Dhakephalkar PK, Dagar SS (2018) Cultivation of multiple genera of hydrogenotrophic methanogens from different environmental niches. Anaerobe 50:64–68. https://doi.org/10.1016/J.ANAEROBE.2018.02.001
doi: 10.1016/J.ANAEROBE.2018.02.001
pubmed: 29432849
Khelaifia S, Raoult D, Drancourt M (2013) A versatile medium for cultivating methanogenic archaea. PLoS ONE. https://doi.org/10.1371/JOURNAL.PONE.0061563
doi: 10.1371/JOURNAL.PONE.0061563
pubmed: 23658767
pmcid: 3734326
Kim S, Rhee S (2019) Methanomethylovorans. Bergey’s manual of systematics of archaea and bacteria, pp 1–5. https://doi.org/10.1002/9781118960608.gbm01602
Kristjansson JK (1989) Thermophilic organisms as sources of thermostable enzymes. Trends Biotechnol 7(12):349–353. https://doi.org/10.1016/0167-7799(89)90035-8
doi: 10.1016/0167-7799(89)90035-8
Kumar S, Dagar SS, Agrawal RK, Puniya AK (2018) Comparative diversity analysis of ruminal methanogens in Murrah buffaloes (Bubalus bubalis) in four states of North India. Anaerobe 52:59–63. https://doi.org/10.1016/J.ANAEROBE.2018.05.012
doi: 10.1016/J.ANAEROBE.2018.05.012
pubmed: 29859302
Lai M (2019) Methanoculleus. Bergey’s manual of systematics of archaea and bacteria, pp 1–8. https://doi.org/10.1002/9781118960608.gbm00505.pub2
Liu Y, Whitman WB (2008) Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Ann N Y Acad Sci 1125(1):171–189. https://doi.org/10.1196/ANNALS.1419.019
doi: 10.1196/ANNALS.1419.019
pubmed: 18378594
Maestrojuan GM, Boone DR (1991) Characterization of Methanosarcina barkeri MS(T) and 227, Methanosarcina mazei S-6(T), and Methanosarcina vacuolata Z-761(T). Int J Syst Bacteriol 41(2):267–274. https://doi.org/10.1099/00207713-41-2-267
doi: 10.1099/00207713-41-2-267
Michał B, Gagat P, Jabłoński S, Chilimoniuk J, Gaworski M, Mackiewicz P, Marcin Ł (2018) PhyMet 2: a database and toolkit for phylogenetic and metabolic analyses of methanogens. Environ Microbiol Rep 10(3):378–382. https://doi.org/10.1111/1758-2229.12648
doi: 10.1111/1758-2229.12648
pubmed: 29624889
Miller TL, Wolin MJ (1974) A serum bottle modification of the hungate technique for cultivating obligate anaerobes. Appl Microbiol 27(5):985–987. https://doi.org/10.1128/AM.27.5.985-987.1974
doi: 10.1128/AM.27.5.985-987.1974
pubmed: 4598231
pmcid: 380188
Mohammad BT, Al Daghistani HI, Jaouani A, Abdel-Latif S, Kennes C (2017) Isolation and characterization of thermophilic bacteria From jordanian hot springs: Bacillus licheniformis and Thermomonas hydrothermalis isolates as potential producers of thermostable enzymes. Int J Microbiol. https://doi.org/10.1155/2017/6943952
doi: 10.1155/2017/6943952
pubmed: 29163641
pmcid: 5661075
Narsing Rao MP, Liu L, Jiao J-Y, Xiao M, Li W-J (2018) ‘Hot psrings’ in extremophiles in Eurasian ecosystems: ecology, diversity, and applications. Springer, Singapore, pp 29–55. https://doi.org/10.1007/978-981-13-0329-6_2
Pachauri R, Allen M, Barros V, Broome J (2014) Climate change 2014: synthesis report. Contribution of Working Groups I, II and III to the fifth assessment report of the Intergovernmental Panel on Climate. https://epic.awi.de/id/eprint/37530/
Pak KR, Bartha R (1998) Mercury methylation by interspecies hydrogen and acetate transfer between sulfidogens and methanogens. Appl Environ Microbiol 64(6):1987–1990. https://doi.org/10.1128/AEM.64.6.1987-1990.1998/
doi: 10.1128/AEM.64.6.1987-1990.1998/
pubmed: 9603804
pmcid: 106268
Poddar A, Das SK (2018) Microbiological studies of hot springs in India: a review. Arch Microbiol 200(1):1–18. https://doi.org/10.1007/S00203-017-1429-3/METRICS
doi: 10.1007/S00203-017-1429-3/METRICS
pubmed: 28887679
Pore SD, Engineer A, Dagar SS, Dhakephalkar PK (2019) Meta-omics based analyses of microbiome involved in biomethanation of rice straw in a thermophilic anaerobic bioreactor under optimized conditions. Bioresour Technol 279:25–33. https://doi.org/10.1016/J.BIORTECH.2019.01.099
doi: 10.1016/J.BIORTECH.2019.01.099
pubmed: 30710817
Ruhl IA, Sheremet A, Smirnova AV, Sharp CE, Grasby SE, Strous M, Dunfield PF (2022). Microbial functional diversity correlates with species diversity along a temperature gradient. ASM MSystems. https://doi.org/10.1128/msystems.00991-21
Saleem F, Bouatra S, Guo AC, Psychogios N, Mandal R, Dunn SM, Ametaj BN, Wishart DS (2013) The bovine ruminal fluid metabolome. Metabolomics 9(2):360–378. https://doi.org/10.1007/S11306-012-0458-9/METRICS
doi: 10.1007/S11306-012-0458-9/METRICS
Sharp CE, Brady AL, Sharp GH, Grasby SE, Stott MB, Dunfield PF (2014) Humboldt’s spa: microbial diversity is controlled by temperature in geothermal environments. ISME J 8(6):1166–1174. https://doi.org/10.1038/ismej.2013.237
doi: 10.1038/ismej.2013.237
pubmed: 24430481
pmcid: 4030231
Shu WS, Huang LN (2021) Microbial diversity in extreme environments. Nat Rev Microbiol 20(4):219–235. https://doi.org/10.1038/s41579-021-00648-y
doi: 10.1038/s41579-021-00648-y
pubmed: 34754082
Sigee DC (2005) Freshwater microbiology: biodiversity and dynamic interactions of microorganisms in the freshwater environment. Wiley. https://doi.org/10.1021/np058255j
Singh Bisht S, Nath Das N, Tripathy NK (2011) Indian hot-water springs: a bird’s eye view. J Energy Environ Carbon Credits 1(1):1–15
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. https://doi.org/10.1093/oxfordjournals.molbev.a040023
doi: 10.1093/oxfordjournals.molbev.a040023
pubmed: 8336541
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38(7):3022–3027. https://doi.org/10.1093/MOLBEV/MSAB120
doi: 10.1093/MOLBEV/MSAB120
pubmed: 33892491
pmcid: 8233496
Thauer RK, Kaster AK, Seedorf H, Buckel W, Hedderich R (2008) Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 6(8):579–591. https://doi.org/10.1038/nrmicro1931
doi: 10.1038/nrmicro1931
pubmed: 18587410
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673
doi: 10.1093/nar/22.22.4673
pubmed: 7984417
pmcid: 308517
Tirawongsaroj P, Sriprang R, Harnpicharnchai P, Thongaram T, Champreda V, Tanapongpipat S, Pootanakit K, Eurwilaichitr L (2008) Novel thermophilic and thermostable lipolytic enzymes from a Thailand hot spring metagenomic library. J Biotechnol 133(1):42–49. https://doi.org/10.1016/J.JBIOTEC.2007.08.046
doi: 10.1016/J.JBIOTEC.2007.08.046
pubmed: 17983680
Touzel JP, Albagnac G (1983) Isolation and characterization of Methanococcus mazei strain MC
doi: 10.1111/j.1574-6968.1983.tb00295.x
Vanwonterghem I, Evans PN, Parks DH, Jensen PD, Woodcroft BJ, Hugenholtz P, Tyson GW (2016) Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota. Nat Microbiol. https://doi.org/10.1038/NMICROBIOL.2016.170
doi: 10.1038/NMICROBIOL.2016.170
pubmed: 27694807
Wagner D (2020) Methanosarcina. Bergey’s manual of systematics of archaea and bacteria, vol 1987, pp 1–23. https://doi.org/10.1002/9781118960608.gbm00519.pub2
Wasserfallen, A., Nölling, J., Pfister, P., Reeve, J., & De Macario, E. C. (2000). Phylogenetic analysis of 18 thermophilic Methanobacterium isolates supports the proposals to create a new genus, Methanothermobacter gen. nov., and to reclassify several isolates in three species, Methanothermobacter thermautotrophicus comb. nov., Methanothermobacter wolfeii comb. nov., and Methanothermobacter marburgensis sp. nov. Int J Syst Evolut Microbiol 50(1):43–53. https://doi.org/10.1099/00207713-50-1-43
Whitman WB, Bowen TL, Boone DR (2014) The methanogenic bacteria. The prokaryotes: other major lineages of bacteria and the archaea, 9783642389542, pp 123–163. https://doi.org/10.1007/978-3-642-38954-2_407
Wright ADG, Pimm C (2003) Improved strategy for presumptive identification of methanogens using 16S riboprinting. J Microbiol Methods 55(2):337–349. https://doi.org/10.1016/S0167-7012(03)00169-6
doi: 10.1016/S0167-7012(03)00169-6
pubmed: 14529955
Yadav P, Korpole S, Prasad GS, Sahni G, Maharjan J, Sreerama L, Bhattarai T (2018) Morphological, enzymatic screening, and phylogenetic analysis of thermophilic bacilli isolated from five hot springs of Myagdi, Nepal. J Appl Biol Biotechnol. https://doi.org/10.7324/JABB.2018.60301
doi: 10.7324/JABB.2018.60301
Zabranska J, Pokorna D (2018) Bioconversion of carbon dioxide to methane using hydrogen and hydrogenotrophic methanogens. Biotechnol Adv 36(3):707–720. https://doi.org/10.1016/J.BIOTECHADV.2017.12.003
doi: 10.1016/J.BIOTECHADV.2017.12.003
pubmed: 29248685
Zhou Z, Pan J, Wang F, Gu JD, Li M (2018) Bathyarchaeota: globally distributed metabolic generalists in anoxic environments. FEMS Microbiol Rev 42(5):639–655. https://doi.org/10.1093/FEMSRE/FUY023
doi: 10.1093/FEMSRE/FUY023
pubmed: 29790926
Zinder SH, Sowers KR, Ferry JG (1985) Methanosarcina thermophila sp. nov., a thermophilic, acetotrophic, methane-producing bacterium. Int J Syst Bacteriol 35(4):522–523. https://doi.org/10.1099/00207713-35-4-522
doi: 10.1099/00207713-35-4-522