A widely distributed hydrogenase oxidises atmospheric H2 during bacterial growth

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  Google Scholar 

Ehhalt DH, Rohrer F. The tropospheric cycle of H₂: a critical review. Tellus B. 2009;61:500–35.

Google Scholar 

Constant P, Poissant L, Villemur R. Tropospheric H₂ budget and the response of its soil uptake under the changing environment. Sci Total Environ. 2009;407:1809–23.

CAS  PubMed  Google Scholar 

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 utilised energy source for microbial growth and survival. ISME J. 2016;10:761–77.

CAS  PubMed  Google Scholar 

Kanno M, Constant P, Tamaki H, Kamagata Y. Detection and isolation of plant-associated bacteria scavenging atmospheric molecular hydrogen. Environ Microbiol. 2015;18:2495–506.

Google Scholar 

Kessler AJ, Chen Y-J, Waite DW, Hutchinson T, Koh S, Popa ME, et al. Bacterial fermentation and respiration processes are uncoupled in permeable sediments. Nat Microbiol. 2019;4:1014–23.

CAS  PubMed  Google Scholar 

Khdhiri M, Hesse L, Popa ME, Quiza L, Lalonde I, Meredith LK, et al. Soil carbon content and relative abundance of high affinity H₂-oxidizing bacteria predict atmospheric H₂ soil uptake activity better than soil microbial community composition. Soil Biol Biochem. 2015;85:1–9.

CAS  Google Scholar 

Lynch RC, Darcy JL, Kane NC, Nemergut DR, Schmidt SK. Metagenomic evidence for metabolism of trace atmospheric gases by high-elevation desert actinobacteria. Front Microbiol. 2014;5:698.

PubMed  PubMed Central  Google Scholar 

Ji M, Greening C, Vanwonterghem I, Carere CR, Bay SK, Steen JA, et al. Atmospheric trace gases support primary production in Antarctic desert surface soil. Nature. 2017;552:400–3.

CAS  PubMed  Google Scholar 

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  Google Scholar 

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  Google Scholar 

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  Google Scholar 

Schäfer C, Friedrich B, Lenz O. Novel, oxygen-insensitive group 5 [NiFe]-hydrogenase in Ralstonia eutropha. Appl Environ Microbiol. 2013;79:5137–45.

PubMed  PubMed Central  Google Scholar 

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  Google Scholar 

Meredith LK, Rao D, Bosak T, Klepac-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  Google Scholar 

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  Google Scholar 

Myers MR, King GM. Isolation and characterization of Acidobacterium ailaaui sp. nov., a novel member of Acidobacteria subdivision 1, from a geothermally heated Hawaiian microbial mat. Int J Syst Evol Microbiol. 2016;66:5328–35.

CAS  PubMed  Google Scholar 

Islam ZF, Cordero PRF, Feng J, Chen Y-J, Bay S, Gleadow RM, 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  Google Scholar 

Schmitz RA, Pol A, Mohammadi SS, Hogendoorn C, van Gelder AH, Jetten MSM, et al. The thermoacidophilic methanotroph Methylacidiphilum fumariolicum SolV oxidizes subatmospheric H₂ with a high-affinity, membrane-associated [NiFe] hydrogenase. ISME J 2020;14:1223–32.

CAS  PubMed  PubMed Central  Google Scholar 

Berney M, Cook GM. Unique flexibility in energy metabolism allows mycobacteria to combat starvation and hypoxia. PLoS One. 2010;5:e8614.

PubMed  PubMed Central  Google Scholar 

Berney M, Greening C, Conrad R, Jacobs WR, Cook GM. An obligately aerobic soil bacterium activates fermentative hydrogen production to survive reductive stress during hypoxia. Proc Natl Acad Sci USA. 2014;111:11479–84.

CAS  PubMed  Google Scholar 

Cordero PRF, Grinter R, Hards K, Cryle MJ, Warr CG, Cook GM, et al. Two uptake hydrogenases differentially interact with the aerobic respiratory chain during mycobacterial growth and persistence. J Biol Chem. 2019;294:18980–91.

CAS  PubMed  Google Scholar 

Greening C, Villas-Bôas SG, Robson JR, Berney M, Cook GM. The growth and survival of Mycobacterium smegmatis is enhanced by co-metabolism of atmospheric H₂. PLoS One. 2014;9:e103034.

PubMed  PubMed Central  Google Scholar 

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  Google Scholar 

Søndergaard D, Pedersen CNS, Greening C. HydDB: a web tool for hydrogenase classification and analysis. Sci Rep. 2016;6:34212.

PubMed  PubMed Central  Google Scholar 

Papen H, Kentemich T, Schmülling T, Bothe H. Hydrogenase activities in cyanobacteria. Biochimie. 1986;68:121–32.

CAS  PubMed  Google Scholar 

Houchins JP, Burris RH. Occurrence and localization of two distinct hydrogenases in the heterocystous cyanobacterium Anabaena sp. Strain 7120. J Bacteriol. 1981;146:209–14.

CAS  PubMed  PubMed Central  Google Scholar 

Tamagnini P, Axelsson R, Lindberg P, Oxelfelt F, Wünschiers R, Lindblad P. Hydrogenases and hydrogen metabolism of cyanobacteria. Microbiol Mol Biol Rev. 2002;66:1–20.

CAS  PubMed  PubMed Central  Google Scholar 

Bothe H, Schmitz O, Yates MG, Newton WE. Nitrogen fixation and hydrogen metabolism in cyanobacteria. Microbiol Mol Biol Rev. 2010;74:529–51.

CAS  PubMed  PubMed Central  Google Scholar 

Koch H, Galushko A, Albertsen M, Schintlmeister A, Gruber-Dorninger C, Lucker S, et al. Growth of nitrite-oxidizing bacteria by aerobic hydrogen oxidation. Science. 2014;345:1052–4.

CAS  PubMed  Google Scholar 

Drobner E, Huber H, Stetter KO. Thiobacillus ferrooxidans, a facultative hydrogen oxidizer. Appl Environ Microbiol. 1990;56:2922–3.

CAS  PubMed  PubMed Central  Google Scholar 

Berney M, Greening C, Hards K, Collins D, Cook GM. Three different [NiFe] hydrogenases confer metabolic flexibility in the obligate aerobe Mycobacterium smegmatis. Environ Microbiol. 2014;16:318–30.

CAS  PubMed  Google Scholar 

Islam ZF, Cordero PRF, Greening C. Putative iron-sulfur proteins are required for hydrogen consumption and enhance survival of mycobacteria. Front Microbiol. 2019;10:2749.

PubMed  PubMed Central  Google Scholar 

Taylor SW, Fahy E, Zhang B, Glenn GM, Warnock DE, Wiley S, et al. Characterization of the human heart mitochondrial proteome. Nat Biotechnol. 2003;21:281–6.

CAS  PubMed  Google Scholar 

Park D, Kim H, Yoon S. Nitrous oxide reduction by an obligate aerobic bacterium, Gemmatimonas aurantiaca strain T-27. Appl Environ Microbiol. 2017;83:e00502–17.

PubMed  PubMed Central  Google Scholar 

Razzell WE, Trussell PC. Isolation and properties of an iron-oxidizing Thiobacillus. J Bacteriol. 1963;85:595–603.

CAS  PubMed  PubMed Central  Google Scholar 

Valdés J, Pedroso I, Quatrini R, Dodson RJ, Tettelin H, Blake R, et al. Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. BMC Genomics. 2008;9:597.

PubMed  PubMed Central  Google Scholar 

Hanada S, Hiraishi A, Shimada K, Matsuura K. Chloroflexus aggregans sp. nov., a filamentous phototrophic bacterium which forms dense cell aggregates by active gliding movement. Int J Syst Evol Microbiol. 1995;45:676–81.

CAS  Google Scholar 

Otaki H, Everroad RC, Matsuura K, Haruta S. Production and consumption of hydrogen in hot spring microbial mats dominated by a filamentous anoxygenic photosynthetic bacterium. Microbes Environ. 2009;27:293–9.

Google Scholar 

Kawai S, Nishihara A, Matsuura K, Haruta S. Hydrogen-dependent autotrophic growth in phototrophic and chemolithotrophic cultures of thermophilic bacteria, Chloroflexus aggregans and Chloroflexus aurantiacus, isolated from Nakabusa hot springs. FEMS Microbiol Lett. 2019;366:fnz122.

CAS  PubMed  Google Scholar 

Heinhorst S, Baker SH, Johnson DR, Davies PS, Cannon GC, Shively JM. Two copies of form I RuBisCO genes in Acidithiobacillus ferrooxidans ATCC 23270. Curr Microbiol. 2002;45:115–17.

CAS  PubMed  Google Scholar 

Klatt CG, Bryant DA, Ward DM. Comparative genomics provides evidence for the 3-hydroxypropionate autotrophic pathway in filamentous anoxygenic phototrophic bacteria and in hot spring microbial mats. Environ Microbiol. 2007;9:2067–78.

CAS  PubMed  Google Scholar 

Zhang H, Sekiguchi Y, Hanada S, Hugenholtz P, Kim H, Kamagata Y, et al. Gemmatimonas aurantiaca gen. nov., sp. nov., a Gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int J Syst Evol Microbiol. 2003;53:1155–63.

CAS  PubMed  Google Scholar 

Zammit CM, Mutch LA, Watling HR, Watkin ELJ. The recovery of nucleic acid from biomining and acid mine drainage microorganisms. Hydrometallurgy. 2011;108:87–92.

CAS  Google Scholar 

Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, et al. Primer3—new capabilities and interfaces. Nucleic Acids Res. 2012;40:e115.

CAS  PubMed  PubMed Central  Google Scholar 

Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547–9.

CAS  PubMed  PubMed Central  Google Scholar 

Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil P-A, et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol. 2018;36:996–1004.

CAS  PubMed  PubMed Central  Google Scholar 

Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics. 2020;6:1925–7.

Google Scholar 

Kawasumi T, Igarashi Y, Kodama T, Minoda Y. Hydrogenobacter thermophilus gen. nov., sp. nov., an extremely thermophilic, aerobic, hydrogen-oxidizing bacterium. Int J Syst Evol Microbiol. 1984;34:5–10.

CAS  Google Scholar 

Klenk H-P, Lapidus A, Chertkov O, Copeland A, Del Rio TG, Nolan M, et al. Complete genome sequence of the thermophilic, hydrogen-oxidizing Bacillus tusciae type strain (T2 T) and reclassification in the new genus, Kyrpidia gen. nov. as Kyrpidia tusciae comb. nov. and emendation of the family Alicyclobacilla. Stand Genom Sci. 2011;5:121.

CAS  Google Scholar 

Hogendoorn C, Pol A, Picone N, Cremers G, van Alen TA, Gagliano AL, et al. Hydrogen and carbon monoxide-utilizing Kyrpidia spormannii species from Pantelleria Island, Italy. Front Microbiol. 2020;11:951.

PubMed  PubMed Central  Google Scholar 

Hedrich S, Johnson DB. Aerobic and anaerobic oxidation of hydrogen by acidophilic bacteria. FEMS Microbiol Lett. 2013;349:40–45.

CAS  PubMed  Google Scholar 

Grostern A, Alvarez-Cohen L. RubisCO-based CO2 fixation and C1 metabolism in the actinobacterium Pseudonocardia dioxanivorans CB1190. Environ Microbiol. 2013;15:3040–53.

CAS  PubMed  Google Scholar 

Auernik KS, Kelly RM. Physiological versatility of the extremely thermoacidophilic archaeon Metallosphaera sedula supported by transcriptomic analysis of heterotrophic, autotrophic, and mixotrophic growth. Appl Environ Microbiol. 2010;76:931–5.

CAS  PubMed  Google Scholar 

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  Google Scholar 

Tveit AT, Hestnes AG, Robinson SL, Schintlmeister A, Dedysh SN, Jehmlich N, et al. Widespread soil bacterium that oxidizes atmospheric methane. Proc Natl Acad Sci USA. 2019;116:8515–24.

CAS  PubMed  Google Scholar 

Conrad R. Soil microorganisms oxidizing atmospheric trace gases (CH₄, CO, H₂, NO). Indian J Microbiol. 1999;39:193–203.

Google Scholar 

Spear JR, Walker JJ, McCollom TM, Pace NR. Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem. Proc Natl Acad Sci USA. 2005;102:2555–60.

CAS  PubMed  Google Scholar 

Ferrera I, Sanchez O. Insights into microbial diversity in wastewater treatment systems: How far have we come? Biotechnol Adv. 2016;34:790–802.

CAS  PubMed  Google Scholar 

Mielke RE, Pace DL, Porter T, Southam G. A critical stage in the formation of acid mine drainage: Colonization of pyrite by Acidithiobacillus ferrooxidans under pH‐neutral conditions. Geobiology. 2003;1:81–90.

CAS  Google Scholar 

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  Google Scholar 

Cordero PRF, Bayly K, Leung PM, 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  Google Scholar 

Eichner MJ, Basu S, Gledhill M, de Beer D, Shaked Y. Hydrogen dynamics in Trichodesmium colonies and their potential role in mineral iron acquisition. Front Microbiol. 2019;10:1565.

PubMed  PubMed Central  Google Scholar 

Houchins JP, Burris RH. Comparative characterization of two distinct hydrogenases from Anabaena sp. strain 7120. J Bacteriol. 1981;146:215–21.

CAS  PubMed  PubMed Central  Google Scholar 

Greening C, Grinter R, Chiri E. Uncovering the metabolic strategies of the dormant microbial majority: towards integrative approaches. mSystems. 2019;4:e00107–19.

CAS  PubMed  PubMed Central  Google Scholar