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Acidobacteria are active and abundant members of diverse atmospheric H2-oxidizing communities detected in temperate soils

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  • 1.

    Conrad R. Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiol Rev. 1996;60:609–40.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 2.

    Rhee TS, Brenninkmeijer CAM, Röckmann T. The overwhelming role of soils in the global atmospheric hydrogen cycle. Atmos Chem Phys. 2006;6:1611–25.

    CAS  Article  Google Scholar 

  • 3.

    Downey NVS, Randerson JT, Eiler JM. Molecular hydrogen uptake by soils in forest, desert, and marsh ecosystems in California. J Geophys Res. 2008;113:G03037.

    Article  Google Scholar 

  • 4.

    Schmitt S, Hanselmann A, Wollschläger U, Hammer S, Levin I. Investigation of parameters controlling the soil sink of atmospheric molecular hydrogen. Tellus B Chem Phys Meter. 2009;61:416–23.

    Article  CAS  Google Scholar 

  • 5.

    Novelli PC, Lang PM, Masarie KA, Hurst DF, Myers R, Elkins JW. Molecular hydrogen in the troposphere: Global distribution and budget. J Geophys Res. 1999;104:30427–44.

    CAS  Article  Google Scholar 

  • 6.

    Downey NVS, Randerson JT, Eiler JM. Temperature and moisture dependence of soil H2 uptake measured in the laboratory. Geophys Res Lett. 2006;33:1–5.

    Google Scholar 

  • 7.

    Häring V, Conrad R. Demonstration of two different H2-oxidizing activities in soil using an H2 consumption and a tritium exchange assay. Biol Fertil Soils. 1994;17:125–8.

    Article  Google Scholar 

  • 8.

    Schuler S, Conrad R. Soils contain two different activities for oxidation of hydrogen. FEMS Microbiol Ecol. 1990;73:77–84.

    CAS  Article  Google Scholar 

  • 9.

    Constant P, Chowdhury SP, Hesse L, Pratscher J, Conrad R. Genome data mining and soil survey for the novel group 5 [NiFe]-hydrogenase to explore the diversity and ecological importance of presumptive high-affinity H2-oxidizing bacteria. Appl Environ Microbiol. 2011;77:6027–35.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 10.

    Greening C, Constant P, Hards K, Morales SE, Oakeshott JG, Russell RJ, et al. Atmospheric hydrogen scavenging: from enzymes to ecosystems. Appl Environ Microbiol. 2015;81:1190–9.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 11.

    Maimaiti J, Zhang Y, Yang J, Cen YP, Layzell DB, Peoples M, et al. Isolation and characterization of hydrogen-oxidizing bacteria induced following exposure of soil to hydrogen gas and their impact on plant growth. Environ Microbiol. 2007;9:435–44.

    CAS  PubMed  Article  Google Scholar 

  • 12.

    Constant P, Poissant L, Villemur R. Isolation of Streptomyces sp. PCB7, the first microorganism demonstrating high-affinity uptake of tropospheric H2. ISME J. 2008;2:1066–76.

    CAS  PubMed  Article  Google Scholar 

  • 13.

    Constant P, Hallenbeck PC. Chapter 5 – Hydrogenase. In: Pandey A, Chang JS, Hallenbeck PC, Larroche C, editors. Biohydrogen, 1st edition. Amsterdam: Elsevier; 2013.

  • 14.

    Greening C, Biswas A, Carere CR, Jackson CJ, Taylor MC, Stott MB, et al. Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilized energy source for microbial growth and survival. ISME J. 2016;10:761–77.

    CAS  PubMed  Article  Google Scholar 

  • 15.

    Constant P, Hallenbeck PC. Chapter 3 – Hydrogenase. In . Editors: Pandey A, Mohan SV, Chang JS, Hallenbeck PC, Larroche C, editors. Biohydrogen, 2nd edition. Amsterdam: Elsevier; 2019;49–78.

  • 16.

    Piché-Choquette S, Constant P. Molecular hydrogen, a neglected key driver of soil biogeochemical processes. Appl Environ Microbiol. 2019;85:e02418–18.

    PubMed  PubMed Central  Article  Google Scholar 

  • 17.

    Greening C, Berney M, Hards K, Cook GM, Conrad R. A soil actinobacterium scavenges atmospheric H2 using two membrane-associated, oxygen-dependent [NiFe] hydrogenases. Proc Natl Acad Sci USA. 2014;111:4257–61.

    CAS  PubMed  Article  Google Scholar 

  • 18.

    Constant P, Chowdhury SP, Pratscher J, Conrad R. Streptomycetes contributing to atmospheric molecular hydrogen soil uptake are widespread and encode a putative high‐affinity [NiFe]‐hydrogenase. Environ Microbiol. 2010;12:821–9.

    CAS  PubMed  Article  Google Scholar 

  • 19.

    Meredith LK, Rao D, Bosak T, Klepec-Ceraj V, Tada KR, Hansel CM, et al. Consumption of atmospheric hydrogen during the life cycle of soil‐dwelling actinobacteria. Environ Microbiol Rep. 2014;6:226–38.

    CAS  PubMed  Article  Google Scholar 

  • 20.

    Piché-Choquette S, Khdhiri M, Constant P. Survey of high-affinity H2-oxidizing bacteria in soil reveals their vast diversity yet underrepresentation in genomic databases. Micro Ecol. 2017;74:771–5.

    Article  CAS  Google Scholar 

  • 21.

    Greening C, Carere CR, Rushton-Green R, Harold LK, Hards K, Taylor MC, et al. Persistence of the dominant soil phylum Acidobacteria by trace gas scavenging. Proc Natl Acad Sci USA. 2015;112:10497–502.

    CAS  PubMed  Article  Google Scholar 

  • 22.

    Islam ZF, Cordero PRF, Feng J, Chen YJ, Bay SK, Jirapanjawat T, et al. Two Chloroflexi classes independently evolved the ability to persist on atmospheric hydrogen and carbon monoxide. ISME J. 2019;13:1801–13.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 23.

    Mohammadi S, Pol A, van Alen TA, Jetten MSM, Op den Camp HJM. Methylacidiphilum fumariolicum SolV, a thermoacidophilic ‘Knallgas’ methanotroph with both an oxygen-sensitive and -insensitive hydrogenase. ISME J. 2017;11:945–58.

    CAS  PubMed  Article  Google Scholar 

  • 24.

    Janssen PH. Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol. 2006;72:1719–28.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 25.

    Barns SM, Cain EC, Sommerville L, Kuske CR. Acidobacteria phylum sequences in uranium-contaminated subsurface sediments greatly expand the known diversity within the phylum. Appl Environ Microbiol. 2007;73:3113–6.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 26.

    Dedysh SN, Yilmaz P. Refining the taxonomic structure of the phylum Acidobacteria. Int J Syst Evol Microbiol. 2018;68:3796–806.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 27.

    Kielak AM, Barreto CC, Kowalchuk GA, van Veen JA, Kuramae EE. The ecology of acidobacteria: moving beyond genes and genomes. Front Microbiol. 2016;7:744.

    PubMed  PubMed Central  Google Scholar 

  • 28.

    Myers MR, King GM. Isolation and characterization of Acidobacterium ailaaui sp. nov., a novel member of Acidobacteria sub-division I, from a geothermally-heated Hawaiian microbial mat. Int J Syst Evol Microbiol. 2016;66:5328–35.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 29.

    Eichorst SA, Trojan D, Roux S, Herbold C, Rattei T, Woebken D. Genomic insights into the Acidobacteria reveal strategies for their success in terrestrial environments. Environ Microbiol. 2018;20:1041–63.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 30.

    Gödde R, Meuser K, Conrad R. Hydrogen consumption and carbon monoxide production in soils with different properties. Biol Fertil Soils. 2000;32:129–34.

    Article  Google Scholar 

  • 31.

    Meredith LK, Commane R, Keenan TF, Klosterman ST, Munger JW, Templer PH, et al. Ecosystem fluxes of hydrogen in a mid‐latitude forest driven by soil microorganisms and plants. Glob Change Biol. 2017;23:906–19.

    Article  Google Scholar 

  • 32.

    Turlapati SA, Minocha R, Bhiravarasa PS, Tisa LS, Thomas WK, Minocha SC. Chronic N-amended soils exhibit an altered bacterial community structure in Harvard Forest, MA, USA. FEMS Microbiol Ecol. 2012;83:478–93.

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • 33.

    Søndergaard D, Pedersen CNS, Greening C. HydDB: A web tool for hydrogenase classification and analysis. Sci Rep. 2016;6:1–8.

    Article  CAS  Google Scholar 

  • 34.

    Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 35.

    Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform. 2019;20:1160–6.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 36.

    Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25:1972–3.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 37.

    Eddy SR. A new generation of homology search tools based on probabilistic inference. Genome Inf. 2009;23:205–11.

    Google Scholar 

  • 38.

    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.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 39.

    Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 40.

    Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol. 2009;26:1641–50.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 41.

    Kaiser C, Koranda M, Kitzler B, Fuchslueger L, Schnecker J, Schweiger P, et al. Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil. N. Phytol. 2010;187:843–58.

    CAS  Article  Google Scholar 

  • 42.

    Spohn M, Pötsch EM, Eichorst SA, Woebken D, Wanek W, Richter A. Soil microbial carbon use efficiency and biomass turnover in a long-term fertilization experiment in a temperate grassland. Soil Biol Biochem. 2016;97:168–75.

    CAS  Article  Google Scholar 

  • 43.

    Šťovíček A, Kim M, Or D, Gillor O. Microbial community response to hydration-desiccation cycles in desert soil. Sci Rep. 2017;7:1–19.

    Article  CAS  Google Scholar 

  • 44.

    Angel R. Total nucleic acid extraction from soil. Protocol Exchange. 2012; https://doi.org/10.1038/protex.2012.046.

  • 45.

    Rose TM, Schultz ER, Henikoff JG, Pietrokovski S, McCallum CM, Henikoff S. Consensus-degenerate hybrid oligonucleotide primers for amplification of distantly related sequences. Nucl Acids Res. 1998;26:1628–35.

    CAS  PubMed  Article  Google Scholar 

  • 46.

    Herbold CW, Pelikan C, Kuzyk O, Hausmann B, Angel R, Berry D, et al. A flexible and economical barcoding approach for highly multiplexed amplicon sequencing of diverse target genes. Front Microbiol. 2015;6:731.

    PubMed  PubMed Central  Article  Google Scholar 

  • 47.

    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-Source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537–41.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 48.

    Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584.

    PubMed  PubMed Central  Article  Google Scholar 

  • 49.

    Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90 K prokaryotic genomes reveals clear species boundaries. Nat Commun. 2018;9:5114.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 50.

    Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12:59–60.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 51.

    McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8:e61217.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 52.

    Constant P, Chowdhury SP, Hesse L, Conrad R. Co-localization of atmospheric H2 oxidation activity and high affinity H2-oxidizing bacteria in non-axenic soil and sterile soil amended with Streptomyces sp. PCB7. Soil Biol Biochem. 2011;43:1888–93.

    CAS  Article  Google Scholar 

  • 53.

    Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–3.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 54.

    Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 2011;39:W29–37.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 55.

    Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33:1870–4.

    CAS  PubMed  Article  Google Scholar 

  • 56.

    Eichorst SA, Kuske CR, Schmidt TM. Influence of plant polymers on the distribution and cultivation of bacteria in the phylum Acidobacteria. Appl Environ Microbiol. 2011;77:586–96.

    CAS  PubMed  Article  Google Scholar 

  • 57.

    Koch IH, Gich F, Dunfield PF, Overmann J. Edaphobacter modestus gen. nov., sp. nov. and Edaphobacter aggregans sp. nov., two novel acidobacteria isolated from alpine and forest soils. Int J Syst Evol Microbiol. 2008;58:1114–22.

    CAS  PubMed  Article  Google Scholar 

  • 58.

    Eichorst SA, Breznak JA, Schmidt TM. Isolation and characterization of soil bacteria that define Terriglobus gen. nov., in the phylum Acidobacteria. Appl Environ Microbiol. 2007;73:2708–17.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 59.

    Ritz C, Baty F, Streibig JC, Gerhard D. Dose-response analysis using R. PLoS ONE. 2015;10:e0146021.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 60.

    Joseph SJ, Hugenholtz P, Sangwan P, Osborne CA, Janssen PH. Laboratory cultivation of widespread and previously uncultured soil bacteria. Appl Environ Microbiol. 2003;69:7210–5.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 61.

    Männistö MK, Rawat S, Starovoytov V, Haggblom MM. Granulicella arctica sp. nov., Granulicella mallensis sp. nov., Granulicella tundricola sp. nov. and Granulicella sapmiensis sp. nov., novel acidobacteria from tundra soil. Int J Syst Evol Microbiol. 2012;62:2097–106.

    PubMed  Article  CAS  Google Scholar 

  • 62.

    Crowe MA, Power JF, Morgan XC, Dunfield PF, Lagutin K, Rijpstra WIC, et al. Pyrinomonas methylaliphatogenes gen. nov., sp. nov., a novel group 4 thermophilic member of the phylum Acidobacteria from geothermal soils. Int J Syst Evol Microbiol. 2014;64:220–7.

    CAS  PubMed  Article  Google Scholar 

  • 63.

    Belova SE, Ravin NV, Pankratov TA, Rakitin AL, Ivanova AA, Beletsky AV, et al. Hydrolytic capabilities as a key to environmental success: chitinolytic and cellulolytic acidobacteria from acidic sub-arctic soils and boreal peatlands. Front Microbiol. 2018;9:1–14.

    Article  Google Scholar 

  • 64.

    Fierer N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol. 2017;15:579–90.

    CAS  PubMed  Article  Google Scholar 

  • 65.

    Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM, Wu M, et al. Three genomes in the phylum Acidobacteria provide insight into their lifestyles in soils. Appl Environ Microbiol. 2009;75:2046–56.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 66.

    Schäfer C, Bommer M, Hennig SE, Jeoung JH, Dobbek H, Lenz O. Structure of an actinobacterial-type [NiFe]-hydrogenase reveals insight into O2-tolerant H2 oxidation. Structure. 2016;24:285–92.

    PubMed  Article  CAS  Google Scholar 

  • 67.

    Liot Q, Constant P. Breathing air to save energy–new insights into the ecophysiological role of high-affinity [NiFe]-hydrogenase in Streptomyces avermitilis. Microbiologyopen. 2016;5:47–59.

    CAS  PubMed  Article  Google Scholar 

  • 68.

    Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N. A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J. 2009;3:442–53.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 69.

    Whitman WB, Coleman DC, Wiebe WJ. Prokaryotes: the unseen majority. Proc Natl Acad Sci USA. 1998;95:6578–83.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 70.

    Kolter R, Siegele DA, Tormo A. The stationary phase of the bacterial life cycle. Ann Rev Microbiol. 1993;47:855–74.

    CAS  Article  Google Scholar 

  • 71.

    Lennon JTJ, Jones SES. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev. 2011;9:119–30.

    CAS  Google Scholar 

  • 72.

    Jones SE, Lennon JT. Dormancy contributes to the maintenance of microbial diversity. Proc Natl Acad Sci USA. 2010;107:5881–6.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 73.

    Morita RY. Is H2 the universal energy source for long-term survival? Micro Ecol. 1999;38:307–20.

    CAS  Article  Google Scholar 

  • 74.

    Cordero PRF, Bayly K, Man Leung P, Huang C, Islam ZF, Schittenhelm RB, et al. Atmospheric carbon monoxide oxidation is a widespread mechanism supporting microbial survival. ISME J. 2019;13:2868–81.

    CAS  PubMed  PubMed Central  Article  Google Scholar 


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