Abstract
Aerobic hydrogen-oxidizing bacteria (HOB) is a group of active, abundant, and diverse microorganisms with representatives in nearly all phyla, distributed in soil exposed to atmospheric or elevated hydrogen. In this review, first, we discuss the fundamental physiology, isolation, and identification techniques for HOB. On this basis, the hydrogenase genetic organization and metabolic strategy of Cupriavidus necator, Mycobacterium smegmatis as representative HOB are summarized. Availability of hydrogen, oxygen, nutrients, and environmental variables such as temperature and moisture are key ecological factors influencing H2 oxidation activity, hydrogenase groups, and microbial composition. Finally, we systematically illustrate the ecological roles of HOB and the interactions between HOB and other soil microbiota, particularly rhizobia in agricultural soils and Cyanobacteria in deserts. Intensive studies should focus on the cell functioning regulated by hydrogenases and on the full play of ecological roles by competitive HOB consortiums in soil niches, which is expected to facilitate the biogeochemical process of carbon dioxide fixation and energy utilization.
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Abdellatif L, Ben-Mahmoud OM, Yang C et al (2017) The H2-oxidizing rhizobacteria associated with field-grown lentil promote the growth of lentil inoculated with Hup+ rhizobium through multiple modes of action. J Plant Growth Regul 36:348–361. https://doi.org/10.1007/s00344-016-9645-7
Abiraami TV, Singh S, Nain L (2020) Soil metaproteomics as a tool for monitoring functional microbial communities: promises and challenges. Rev Environ Sci Biotechnol 19:73–102. https://doi.org/10.1007/s11157-019-09519-8
Aragno M, Schlegel HG (1981) The hydrogen-oxidizing bacteria. In: Starr MP, Stolp H, Trüper HG et al (eds) The prokaryotes: a handbook on habitats, isolation, and identification of bacteria. Springer, Berlin, pp 865–893
Baginsky C, Brito B, Imperial J et al (2005) Symbiotic hydrogenase activity in Bradyrhizobium sp. (Vigna) increases nitrogen content in Vigna unguiculata plants. Appl Environ Microbiol 71:7536–7538. https://doi.org/10.1128/AEM.71.11.7536-7538.2005
Bahl J, Lau MCY, Smith GJD et al (2011) Ancient origins determine global biogeography of hot and cold desert cyanobacteria. Nat Commun 2:163. https://doi.org/10.1038/ncomms1167
Bay S, Ferrari B, Greening C et al (2018) Life without water: how do bacteria generate biomass in desert ecosystems? Microbiol Aust 39:28–32. https://doi.org/10.1071/MA18008
Bay SK, Dong X, Bradley JA et al (2021) Trace gas oxidizers are widespread and active members of soil microbial communities. Nat Microbiol 6:246–256. https://doi.org/10.1038/s41564-020-00811-w
Berney M, Cook GM (2010) Unique flexibility in energy metabolism allows mycobacteria to combat starvation and hypoxia. PLoS ONE 5:e8614. https://doi.org/10.1371/journal.pone.0008614
Berney M, Greening C, Hards K et al (2014) Three different [NiFe] hydrogenases confer metabolic flexibility in the obligate aerobe Mycobacterium smegmatis. Environ Microbiol 16:318–330. https://doi.org/10.1111/1462-2920.12320
Bernhard M, Buhrke T, Bleijlevens B et al (2001) The H2 sensor of Ralstonia eutropha: biochemical characteristics, spectroscopic properties, and its interaction with a histidine protein kinase *. J Biol Chem 276:15592–15597. https://doi.org/10.1074/jbc.M009802200
Bowien B, Schlegel HG (1981) Physiology and biochemistry of aerobic hydrogen-oxidizing bacteria. Annu Rev Microbiol 35:405–452. https://doi.org/10.1146/annurev.mi.35.100181.002201
Brito B, Martínez M, Fernández D et al (1997) Hydrogenase genes from Rhizobium leguminosarum bv. viciae are controlled by the nitrogen fixation regulatory protein NifA. Proc Natl Acad Sci 94:6019–6024. https://doi.org/10.1073/pnas.94.12.6019
Brito B, Palacios JM, Imperial J, Ruiz-Argüeso T (2002) Engineering the Rhizobium leguminosarum bv. viciae hydrogenase system for expression in free-living microaerobic cells and increased symbiotic Hydrogenase activity. Appl Environ Microbiol 68:2461–2467. https://doi.org/10.1128/AEM.68.5.2461-2467.2002
Bruslind L (2019a) Chemolithotrophy & Nitrogen Metabolism
Bruslind L (2019b) General Microbiology. Oregon State University
Buhrke T, Lenz O, Krauss N, Friedrich B (2005) Oxygen tolerance of the H2-sensing [NiFe] hydrogenase from Ralstonia eutropha H16 is based on limited access of oxygen to the active site*. J Biol Chem 280:23791–23796. https://doi.org/10.1074/jbc.M503260200
Buhrke T, Lenz O, Porthun A, Friedrich B (2004) The H2-sensing complex of Ralstonia eutropha: interaction between a regulatory [NiFe] hydrogenase and a histidine protein kinase. Mol Microbiol 51:1677–1689. https://doi.org/10.1111/j.1365-2958.2003.03933.x
Burgdorf T, Lenz O, Buhrke T et al (2005a) [NiFe]-hydrogenases of Ralstonia eutropha H16: modular enzymes for oxygen-tolerant biological hydrogen oxidation. J Mol Microbiol Biotechnol 10:181–196. https://doi.org/10.1159/000091564
Burgdorf T, Löscher S, Liebisch P et al (2005b) Structural and oxidation-state changes at its nonstandard Ni−Fe site during activation of the NAD-reducing hydrogenase from Ralstonia eutropha detected by X-ray absorption, EPR, and FTIR spectroscopy. J Am Chem Soc 127:576–592. https://doi.org/10.1021/ja0461926
Caruso T, Chan Y, Lacap DC et al (2011) Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale. ISME J 5:1406–1413. https://doi.org/10.1038/ismej.2011.21
Chiri E, Nauer PA, Lappan R et al (2021) Termite gas emissions select for hydrogenotrophic microbial communities in termite mounds. Proc Natl Acad Sci U S A 118:e2102625118. https://doi.org/10.1073/pnas.2102625118
Chowdhury SP, Conrad R (2010) Thermal deactivation of high-affinity H2 uptake activity in soils. Soil Biol Biochem 42:1574–1580. https://doi.org/10.1016/j.soilbio.2010.05.027
Ciani M, Lippolis A, Fava F et al (2021) Microbes: food for the future. Foods 10:971. https://doi.org/10.3390/foods10050971
Clark AE, Kaleta EJ, Arora A, Wolk DM (2013) Matrix-assisted laser desorption ionization-time of flight mass spectrometry: a fundamental shift in the routine practice of clinical microbiology. Clin Microbiol Rev 26:547–603. https://doi.org/10.1128/CMR.00072-12
Conrad R (1996) Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiol Rev 60:609–640. https://doi.org/10.1128/mr.60.4.609-640.1996
Conrad R, Seiler W (1980) Contribution of hydrogen production by biological nitrogen fixation to the global hydrogen budget. J Geophys Res Oceans 85:5493–5498. https://doi.org/10.1029/JC085iC10p05493
Constant P, Chowdhury SP, Hesse L et al (2011a) Genome data mining and soil survey for the novel group 5 [NiFe]-hydrogenase to explore the diversity and ecological importance of presumptive high-affinity H 2-oxidizing bacteria. Appl Environ Microbiol 77:6027–6035. https://doi.org/10.1128/AEM.00673-11
Constant P, Chowdhury SP, Hesse L, Conrad R (2011b) 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 43:1888–1893. https://doi.org/10.1016/j.soilbio.2011.05.009
Constant P, Chowdhury SP, Pratscher J, Conrad R (2010) Streptomycetes contributing to atmospheric molecular hydrogen soil uptake are widespread and encode a putative high-affinity [NiFe]-hydrogenase. Environ Microbiol 12:821–829. https://doi.org/10.1111/j.1462-2920.2009.02130.x
Constant P, Poissant L, Villemur R (2008) Isolation of Streptomyces sp. PCB7, the first microorganism demonstrating high-affinity uptake of tropospheric H2. ISME J 2:1066–1076. https://doi.org/10.1038/ismej.2008.59
Constant P, Poissant L, Villemur R (2009) Tropospheric H2 budget and the response of its soil uptake under the changing environment. Sci Total Environ 407:1809–1823. https://doi.org/10.1016/j.scitotenv.2008.10.064
Cordero PRF, Grinter R, Hards K et al (2019) Two uptake hydrogenases differentially interact with the aerobic respiratory chain during mycobacterial growth and persistence. J Biol Chem 294:18980–18991. https://doi.org/10.1074/jbc.RA119.011076
Dong Z, Layzell DB (2001) H2 oxidation, O2 uptake and CO2 fixation in hydrogen treated soils. Plant Soil 229:1–12. https://doi.org/10.1023/A:1004810017490
Dong Z, Wu L, Kettlewell B et al (2003) Hydrogen fertilization of soils – is this a benefit of legumes in rotation? Plant Cell Environ 26:1875–1879. https://doi.org/10.1046/j.1365-3040.2003.01103.x
Durmowicz MC, Maier RJ (1997) Roles of HoxX and HoxA in biosynthesis of hydrogenase in Bradyrhizobium japonicum. J Bacteriol 179:3676–3682. https://doi.org/10.1128/jb.179.11.3676-3682.1997
Edao Y, Iwai Y (2020) Investigation on characteristic of tritium oxidation by natural soils. Fusion Sci Technol 76:135–140. https://doi.org/10.1080/15361055.2019.1704572
Ehsani E, Dumolin C, Arends JBA et al (2019) Enriched hydrogen-oxidizing microbiomes show a high diversity of co-existing hydrogen-oxidizing bacteria. Appl Microbiol Biotechnol 103:8241–8253
Fierer N, Leff JW, Adams BJ et al (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc Natl Acad Sci 109:21390–21395. https://doi.org/10.1073/pnas.1215210110
Friedrich B, Fritsch J, Lenz O (2011) Oxygen-tolerant hydrogenases in hydrogen-based technologies. Curr Opin Biotechnol 22:358–364. https://doi.org/10.1016/j.copbio.2011.01.006
Friedrich B, Schwartz E (1993) Molecular biology of hydrogen utilization in aerobic chemolithotrophs. Annu Rev Microbiol 47:351–383. https://doi.org/10.1146/annurev.mi.47.100193.002031
Friedrich CG, Friedrich B, Bowien B (1981) Formation of enzymes of autotrophic metabolism during heterotrophic growth of Alcaligenes eutrophus. Microbiology 122:69–78. https://doi.org/10.1099/00221287-122-1-69
Frielingsdorf S, Fritsch J, Schmidt A et al (2014) Reversible [4Fe-3S] cluster morphing in an O2-tolerant [NiFe] hydrogenase. Nat Chem Biol 10:378–385. https://doi.org/10.1038/nchembio.1500
Fritsch J, Lenz O, Friedrich B (2013) Structure, function and biosynthesis of O2-tolerant hydrogenases. Nat Rev Microbiol 11:106–114. https://doi.org/10.1038/nrmicro2940
Fritsch J, Scheerer P, Frielingsdorf S et al (2011) The crystal structure of an oxygen-tolerant hydrogenase uncovers a novel iron-sulphur centre. Nature 479:249–252. https://doi.org/10.1038/nature10505
Fu C, Olson JW, Maier RJ (1995) HypB protein of Bradyrhizobium japonicum is a metal-binding GTPase capable of binding 18 divalent nickel ions per dimer. Proc Natl Acad Sci 92:2333–2337. https://doi.org/10.1073/pnas.92.6.2333
Gödde M, Meuser K, Conrad R (2000) Hydrogen consumption and carbon monoxide production in soils with different properties. Biol Fertil Soils 32:129–134. https://doi.org/10.1007/s003740000226
Giguere AT, Eichorst SA, Meier DV et al (2021) Acidobacteria are active and abundant members of diverse atmospheric H2-oxidizing communities detected in temperate soils. ISME J 15:363–376. https://doi.org/10.1038/s41396-020-00750-8
Golding A-L, Dong Z (2010) Hydrogen production by nitrogenase as a potential crop rotation benefit. Environ Chem Lett 8:101–121. https://doi.org/10.1007/s10311-010-0278-y
Golding A-L, Zou Y, Yang X et al (2012) Plant growth promoting H2-oxidizing bacteria as seed inoculants for cereal crops. Agric Sci 3:510–516. https://doi.org/10.4236/as.2012.34060
Goris T, Wait AF, Saggu M et al (2011) A unique iron-sulfur cluster is crucial for oxygen tolerance of a [NiFe]-hydrogenase. Nat Chem Biol 7:310–318. https://doi.org/10.1038/nchembio.555
Greening C, Berney M, Hards K et al (2014a) A soil actinobacterium scavenges atmospheric H2 using two membrane-associated, oxygen-dependent [NiFe] hydrogenases. Proc Natl Acad Sci 111:4257–4261. https://doi.org/10.1073/pnas.1320586111
Greening C, Biswas A, Carere CR et al (2016) Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival. ISME J 10:761–777. https://doi.org/10.1038/ismej.2015.153
Greening C, Carere CR, Rushton-Green R et al (2015a) Persistence of the dominant soil phylum Acidobacteria by trace gas scavenging. Proc Natl Acad Sci 112:10497–10502. https://doi.org/10.1073/pnas.1508385112
Greening C, Constant P, Hards K et al (2015b) Atmospheric hydrogen scavenging: from enzymes to ecosystems. Appl Environ Microbiol 81:1190–1199. https://doi.org/10.1128/AEM.03364-14
Greening C, Cook GM (2014) Integration of hydrogenase expression and hydrogen sensing in bacterial cell physiology. Curr Opin Microbiol 18:30–38. https://doi.org/10.1016/j.mib.2014.02.001
Greening C, Grinter R (2022) Microbial oxidation of atmospheric trace gases. Nat Rev Microbiol. https://doi.org/10.1038/s41579-022-00724-x
Greening C, Islam ZF, Bay SK (2021) Hydrogen is a major lifeline for aerobic bacteria. Trends Microbiol 30:330–337. https://doi.org/10.1016/j.tim.2021.08.004
Greening C, Villas-Bôas SG, Robson JR et al (2014b) The growth and survival of mycobacterium smegmatis is enhanced by co-metabolism of atmospheric H2. PLoS ONE 9:e103034. https://doi.org/10.1371/journal.pone.0103034
Großkopf T, Soyer OS (2014) Synthetic microbial communities. Curr Opin Microbiol 18:72–77. https://doi.org/10.1016/j.mib.2014.02.002
Grostern A, Alvarez-Cohen L (2013) RubisCO-based CO2 fixation and C1 metabolism in the actinobacterium Pseudonocardia dioxanivorans CB1190. Environ Microbiol 15:3040–3053. https://doi.org/10.1111/1462-2920.12144
Schlegel HG, Gottschalk G, Von Bartha R (1961) Formation and Utilization of Poly-β-Hydroxybutyric Acid by Knallgas Bacteria (Hydrogenomonas). Nature 191:463–465. https://doi.org/10.1038/191463a0
Han Q, Ma Q, Chen Y et al (2020) Variation in rhizosphere microbial communities and its association with the symbiotic efficiency of rhizobia in soybean. ISME J 14:1915–1928. https://doi.org/10.1038/s41396-020-0648-9
Häring V, Conrad R (1994) Demonstration of two different H2-oxidizing activities in soil using an H2 consumption and a tritium exchange assay. Biol Fertil Soils 17:125–128. https://doi.org/10.1007/BF00337744
Hartman K, Tringe SG (2019) Interactions between plants and soil shaping the root microbiome under abiotic stress. Biochem J 476:2705–2724. https://doi.org/10.1042/BCJ20180615
Hogendoorn C, Pol A, Picone N et al (2020) Hydrogen and carbon monoxide-utilizing kyrpidia spormannii species from Pantelleria island. Italy Front Microbiol 11:951. https://doi.org/10.3389/fmicb.2020.00951
Hu X, Kerckhof F-M, Ghesquière J et al (2020) Microbial protein out of thin air: fixation of nitrogen gas by an autotrophic hydrogen-oxidizing bacterial enrichment. Environ Sci Technol 54:3609–3617. https://doi.org/10.1021/acs.est.9b06755
Irvine P, Smith M, Dong Z (2004) Hydrogen fertilizer: Bacteria or fungi? Acta Hortic 631:239–242
Islam S, Akanda AM, Prova A et al (2016) Isolation and identification of plant growth promoting Rhizobacteria from cucumber rhizosphere and their effect on plant growth promotion and disease suppression. Front Microbiol. https://doi.org/10.3389/fmicb.2015.01360
Islam ZF, Cordero PRF, Feng J et al (2019a) Two Chloroflexi classes independently evolved the ability to persist on atmospheric hydrogen and carbon monoxide. ISME J 13:1801–1813. https://doi.org/10.1038/s41396-019-0393-0
Islam ZF, Cordero PRF, Greening C (2019b) Putative iron-sulfur proteins are required for hydrogen consumption and enhance survival of mycobacteria. Front Microbiol 10:2749. https://doi.org/10.3389/fmicb.2019.02749
Islam ZF, Welsh C, Bayly K et al (2020) A widely distributed hydrogenase oxidises atmospheric H2 during bacterial growth. ISME J 14:2649–2658. https://doi.org/10.1038/s41396-020-0713-4
Jabborova D, Kannepalli A, Davranov K et al (2021) Co-inoculation of rhizobacteria promotes growth, yield, and nutrient contents in soybean and improves soil enzymes and nutrients under drought conditions. Sci Rep 11:22081. https://doi.org/10.1038/s41598-021-01337-9
Jannasch HW, Mottl MJ (1985) Geomicrobiology of deep-sea hydrothermal vents. Science 229:717–725. https://doi.org/10.1126/science.229.4715.717
Ji M, Greening C, Vanwonterghem I et al (2017) Atmospheric trace gases support primary production in Antarctic desert surface soil. Nature 552:400–403. https://doi.org/10.1038/nature25014
Maimaiti J, Zhang Y, Yang J et al (2007) Isolation and characterization of hydrogen-oxidizing bacteria induced following exposure of soil to hydrogen gas and their impact on plant growth. Environ Microbiol 9:435–444. https://doi.org/10.1111/j.1462-2920.2006.01155.x
Jiang C, Sheng X, Qian M, Wang Q (2008) Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal-polluted soil. Chemosphere 72:157–164. https://doi.org/10.1016/j.chemosphere.2008.02.006
Jordaan K, Lappan R, Dong X et al (2020) Hydrogen-oxidizing bacteria are abundant in desert soils and strongly stimulated by hydration. mSystems 5:e01131-20. https://doi.org/10.1128/mSystems.01131-20
Khdhiri M, Piché-Choquette S, Tremblay J et al (2018) Meta-omics survey of [NiFe]-hydrogenase genes fails to capture drastic variations in H2-oxidation activity measured in three soils exposed to H2. Soil Biol Biochem 125:239–243. https://doi.org/10.1016/j.soilbio.2018.07.020
Klüber HD, Lechner S, Conrad R (1995) Characterization of populations of aerobic hydrogen-oxidizing soil bacteria. FEMS Microbiol Ecol 16:167–175. https://doi.org/10.1111/j.1574-6941.1995.tb00280.x
Lechner S, Conrad R (1997) Detection in soil of aerobic hydrogen-oxidizing bacteria related to Alcaligenes eutrophus by PCR and hybridization assays targeting the gene of the membrane-bound (NiFe) hydrogenase. FEMS Microbiol Ecol 22:193–206. https://doi.org/10.1111/j.1574-6941.1997.tb00371.x
Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9:119–130. https://doi.org/10.1038/nrmicro2504
Lenz O, Friedrich B (1998) A novel multicomponent regulatory system mediates H2 sensing in Alcaligenes eutrophus. Proc Natl Acad Sci 95:12474–12479. https://doi.org/10.1073/pnas.95.21.12474
Lenz O, Ludwig M, Schubert T et al (2010) H2 Conversion in the presence of O2 as performed by the membrane-bound [NiFe]-hydrogenase of Ralstonia eutropha. ChemPhysChem 11:1107–1119. https://doi.org/10.1002/cphc.200901002
Leung PM, Bay SK, Meier DV et al (2020) Energetic basis of microbial growth and persistence in desert ecosystems. mSystems 5:e00495-19. https://doi.org/10.1128/mSystems.00495-19
Leung PM, Daebeler A, Chiri E et al (2022) A nitrite-oxidising bacterium constitutively consumes atmospheric hydrogen. ISME J. https://doi.org/10.1038/s41396-022-01265-0
Li H, Zhao Q, Huang H (2019) Current states and challenges of salt-affected soil remediation by cyanobacteria. Sci Total Environ 669:258–272. https://doi.org/10.1016/j.scitotenv.2019.03.104
Li Z, Liu X, Liu R et al (2018) Insight into bacterial community diversity and monthly fluctuations of medicago sativa rhizosphere soil in response to hydrogen gas using illumina high-throughput sequencing. Curr Microbiol 75:1626–1633. https://doi.org/10.1007/s00284-018-1569-y
Lin K-H, Liao B-Y, Chang H-W et al (2015) Metabolic characteristics of dominant microbes and key rare species from an acidic hot spring in Taiwan revealed by metagenomics. BMC Genomics 16:1029. https://doi.org/10.1186/s12864-015-2230-9
Lin L, Huang H, Zhang X et al (2022) Hydrogen-oxidizing bacteria and their applications in resource recovery and pollutant removal. Sci Total Environ 835:155559. https://doi.org/10.1016/j.scitotenv.2022.155559
Liot Q, Constant P (2016) Breathing air to save energy – new insights into the ecophysiological role of high-affinity [NiFe]-hydrogenase in Streptomyces avermitilis. MicrobiologyOpen 5:47–59. https://doi.org/10.1002/mbo3.310
Lu Y, Koo J (2019) O2 sensitivity and H2 production activity of hydrogenases—A review. Biotechnol Bioeng 116:3124–3135. https://doi.org/10.1002/bit.27136
Lubitz W, Ogata H, Rüdiger O, Reijerse E (2014) Hydrogenases. Chem Rev 114:4081–4148. https://doi.org/10.1021/cr4005814
Ludwig M, Cracknell JA, Vincent KA et al (2009) Oxygen-tolerant H2 oxidation by membrane-bound [NiFe] hydrogenases of ralstonia species: coping with low level H2 in air. J Biol Chem 284:465–477. https://doi.org/10.1074/jbc.M803676200
Lupacchini S, Appel J, Stauder R et al (2021) Rewiring cyanobacterial photosynthesis by the implementation of an oxygen-tolerant hydrogenase. Metab Eng 68:199–209. https://doi.org/10.1016/j.ymben.2021.10.006
Lynch RC, Darcy JL, Kane NC et al (2014) Metagenomic evidence for metabolism of trace atmospheric gases by high-elevation desert Actinobacteria. Front Microbiol 5:698. https://doi.org/10.3389/fmicb.2014.00698
Madigan M, Martinko J (1997) Brock biology of micro-organisms. Prenticehall Inc, Hoboken
Maier RJ, Triplett EW (1996) Toward more productive, efficient, and competitive nitrogen-fixing symbiotic bacteria. Crit Rev Plant Sci 15:191–234. https://doi.org/10.1080/07352689609701941
Matassa S, Boon N, Verstraete W (2015) Resource recovery from used water: the manufacturing abilities of hydrogen-oxidizing bacteria. Water Res 68:467–478. https://doi.org/10.1016/j.watres.2014.10.028
Matassa S, Verstraete W, Pikaar I, Boon N (2016) Autotrophic nitrogen assimilation and carbon capture for microbial protein production by a novel enrichment of hydrogen-oxidizing bacteria. Water Res 101:137–146. https://doi.org/10.1016/j.watres.2016.05.077
Meredith LK, Commane R, Keenan TF et al (2017) Ecosystem fluxes of hydrogen in a mid-latitude forest driven by soil microorganisms and plants. Glob Change Biol 23:906–919. https://doi.org/10.1111/gcb.13463
Mohammadi S, Pol A, van Alen TA et al (2017) Methylacidiphilum fumariolicum SolV, a thermoacidophilic ‘Knallgas’ methanotroph with both an oxygen-sensitive and -insensitive hydrogenase. ISME J 11:945–958. https://doi.org/10.1038/ismej.2016.171
Noar JD, Bruno-Bárcena JM (2016) Protons and pleomorphs: aerobic hydrogen production in Azotobacters. World J Microbiol Biotechnol 32:29. https://doi.org/10.1007/s11274-015-1980-5
Olson JW, Maier RJ (2002) Molecular hydrogen as an energy source for helicobacter pylori. Science 298:1788–1790. https://doi.org/10.1126/science.1077123
Ortiz M, Leung PM, Shelley G et al (2021) Multiple energy sources and metabolic strategies sustain microbial diversity in Antarctic desert soils. Proc Natl Acad Sci 118:e2025322118. https://doi.org/10.1073/pnas.2025322118
Osborne CA, Peoples MB, Janssen PH (2010) Detection of a reproducible, single-member shift in soil bacterial communities exposed to low levels of hydrogen. Appl Environ Microbiol 76:1471–1479. https://doi.org/10.1128/AEM.02072-09
Osborne CA, Rees GN, Bernstein Y, Janssen PH (2006) New threshold and confidence estimates for terminal restriction fragment length polymorphism analysis of complex bacterial communities. Appl Environ Microbiol 72:1270–1278. https://doi.org/10.1128/AEM.72.2.1270-1278.2006
Palmer JD, Foster KR (2022) Bacterial species rarely work together. Science 376:581–582. https://doi.org/10.1126/science.abn5093
Palmer T, Berks BC (2012) The twin-arginine translocation (Tat) protein export pathway. Nat Rev Microbiol 10:483–496. https://doi.org/10.1038/nrmicro2814
Pander B, Mortimer Z, Woods C et al (2020) Hydrogen oxidising bacteria for production of single-cell protein and other food and feed ingredients. Eng Biol 4:21–24. https://doi.org/10.1049/enb.2020.0005
Panich J, Fong B, Singer SW (2021) Metabolic engineering of cupriavidus necator H16 for sustainable biofuels from CO2. Trends Biotechnol 39:412–424. https://doi.org/10.1016/j.tibtech.2021.01.001
Parkin A, Sargent F (2012) The hows and whys of aerobic H2 metabolism. Curr Opin Chem Biol 16:26–34. https://doi.org/10.1016/j.cbpa.2012.01.012
Petersen JM, Zielinski FU, Pape T et al (2011) Hydrogen is an energy source for hydrothermal vent symbioses. Nature 476:176–180. https://doi.org/10.1038/nature10325
Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799. https://doi.org/10.1038/nrmicro3109
Piché-Choquette S, Khdhiri M, Constant P (2017) Survey of high-affinity H2-oxidizing bacteria in soil reveals their vast diversity yet underrepresentation in genomic databases. Microb Ecol 74:771–775. https://doi.org/10.1007/s00248-017-1011-1
Piché-Choquette S, Tremblay J, Tringe SG, Constant P (2016) H2-saturation of high affinity H2-oxidizing bacteria alters the ecological niche of soil microorganisms unevenly among taxonomic groups. PeerJ 4:e1782. https://doi.org/10.7717/peerj.1782
Picone N, Blom P, Wallenius AJ et al (2021) Methylacidimicrobium thermophilum AP8, a novel methane- and hydrogen-oxidizing bacterium isolated from volcanic soil on Pantelleria Island. Italy. Front Microbiol 12:637762
Picone N, Hogendoorn C, Cremers G et al (2020) Geothermal gases shape the microbial community of the volcanic soil of Pantelleria. Italy Msystems 5:e00517-e520. https://doi.org/10.1128/mSystems.00517-20
Prashar P, Kapoor N, Sachdeva S (2014) Rhizosphere: its structure, bacterial diversity and significance. Rev Environ Sci Biotechnol 13:63–77. https://doi.org/10.1007/s11157-013-9317-z
Pumphrey GM, Ranchou-Peyruse A, Spain JC (2011) Cultivation-independent detection of autotrophic hydrogen-oxidizing bacteria by DNA stable-isotope probing. Appl Environ Microbiol 77:4931–4938. https://doi.org/10.1128/AEM.00285-11
Purohit K, Becker RR, Evans HJ (1982) D-Ribulose-1,5-bisphosphate carboxylase/oxygenase from chemolithotrophically grown Rhizobium japonicum. Biochim Biophys Acta BBA - Gen Subj 715:230–239. https://doi.org/10.1016/0304-4165(82)90363-4
Ray AE, Zaugg J, Benaud N et al (2022) Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts. ISME J. https://doi.org/10.1038/s41396-022-01298-5
Rhee TS, Brenninkmeijer CAM, Röckmann T (2006) The overwhelming role of soils in the global atmospheric hydrogen cycle. Atmos Chem Phys 6:1611–1625. https://doi.org/10.5194/acp-6-1611-2006
Ruiz-Argüeso T, Palacios JM, Imperial J (2001) Regulation of the hydrogenase system in Rhizobium leguminosarum. Plant Soil 230:49–57. https://doi.org/10.1023/A:1004578324977
Schäfer C, Friedrich B, Lenz O (2013) Novel, oxygen-insensitive group 5 [NiFe]-hydrogenase in Ralstonia eutropha. Appl Environ Microbiol 79:5137–5145. https://doi.org/10.1128/AEM.01576-13
Schimel JP (2018) Life in dry soils: effects of drought on soil microbial communities and processes. Annu Rev Ecol Evol Syst 49:409–432. https://doi.org/10.1146/annurev-ecolsys-110617-062614
Schink B, Schlegel H-G (1978) Hydrogen metabolism in aerobic hydrogen-oxidizing bacteria. Biochimie 60:297–305. https://doi.org/10.1016/S0300-9084(78)80826-8
Schlegel HG, Meyer M (1985) Isolation of hydrogenase regulatory mutants of hydrogen-oxidizing bacteria by a colony-screening method. Arch Microbiol 141:377–383. https://doi.org/10.1007/BF00428853
Schmitz RA, Pol A, Mohammadi SS et al (2020) The thermoacidophilic methanotroph Methylacidiphilum fumariolicum SolV oxidizes subatmospheric H2 with a high-affinity, membrane-associated [NiFe] hydrogenase. ISME J 14:1223–1232. https://doi.org/10.1038/s41396-020-0609-3
Schuler S, Conrad R (1991) Hydrogen oxidation activities in soil as influenced by pH, temperature, moisture, and season. Biol Fertil Soils 12:127–130. https://doi.org/10.1007/BF00341488
Schulze-Makuch D, Wagner D, Kounaves SP et al (2018) Transitory microbial habitat in the hyperarid Atacama desert. Proc Natl Acad Sci 115:2670–2675. https://doi.org/10.1073/pnas.1714341115
Schwartz E, Fritsch J, Friedrich B (2013) H2-metabolizing prokaryotes. In: Rosenberg E, DeLong EF, Lory S et al (eds) The prokaryotes: prokaryotic physiology and biochemistry. Springer, Berlin, pp 119–199
Schwartz E, Voigt B, Zühlke D et al (2009) A proteomic view of the facultatively chemolithoautotrophic lifestyle of Ralstonia eutropha H16. Proteomics 9:5132–5142. https://doi.org/10.1002/pmic.200900333
Shomura Y, Yoon K-S, Nishihara H, Higuchi Y (2011) Structural basis for a [4Fe-3S] cluster in the oxygen-tolerant membrane-bound [NiFe]-hydrogenase. Nature 479:253–256. https://doi.org/10.1038/nature10504
Smith-Downey NV, Randerson JT, Eiler JM (2008) Molecular hydrogen uptake by soils in forest, desert, and marsh ecosystems in California. J Geophys Res Biogeosci. https://doi.org/10.1029/2008JG000701
Søndergaard D, Pedersen CNS, Greening C (2016) HydDB: A web tool for hydrogenase classification and analysis. Sci Rep 6:34212. https://doi.org/10.1038/srep34212
Spear JR, Walker JJ, McCollom TM, Pace NR (2005) Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem. Proc Natl Acad Sci 102:2555–2560. https://doi.org/10.1073/pnas.0409574102
Stein S, Selesi D, Schilling R et al (2005) Microbial activity and bacterial composition of H2-treated soils with net CO2 fixation. Soil Biol Biochem 37:1938–1945. https://doi.org/10.1016/j.soilbio.2005.02.035
Sultana S, Alam S, Karim MM (2021) Screening of siderophore-producing salt-tolerant rhizobacteria suitable for supporting plant growth in saline soils with iron limitation. J Agric Food Res 4:100150. https://doi.org/10.1016/j.jafr.2021.100150
Van Soom C, Rumjanek N, Vanderleyden J, Neves MCP (1993) Hydrogenase in Bradyrhizobium japonicum: genetics, regulation and effect on plant growth. World J Microbiol Biotechnol 9:615–624. https://doi.org/10.1007/BF00369567
Vignais PM, Billoud B (2007) Occurrence, classification, and biological function of hydrogenases: an overview. Chem Rev 107:4206–4272. https://doi.org/10.1021/cr050196r
Wang S, Qiu L, Liu X et al (2018) Electron transport chains in organohalide-respiring bacteria and bioremediation implications. Biotechnol Adv 36:1194–1206. https://doi.org/10.1016/j.biotechadv.2018.03.018
Wang X-B, Schmidt R, Yergeau É, Constant P (2020a) Field H2 infusion alters bacterial and archaeal communities but not fungal communities nor nitrogen cycle gene abundance. Soil Biol Biochem 151:108018. https://doi.org/10.1016/j.soilbio.2020.108018
Wang Y, Liu Y, Wang S et al (2020b) Hydrogen agronomy: research progress and prospects. J Zhejiang Univ-Sci B 21:841–855. https://doi.org/10.1631/jzus.B2000386
Willms IM, Rudolph AY, Göschel I et al (2020) Globally abundant “Candidatus Udaeobacter” benefits from release of antibiotics in soil and potentially performs trace gas scavenging. mSphere 5:e00186-20. https://doi.org/10.1128/mSphere.00186-20
Xu X, Zarecki R, Medina S et al (2019) Modeling microbial communities from atrazine contaminated soils promotes the development of biostimulation solutions. ISME J 13:494–508. https://doi.org/10.1038/s41396-018-0288-5
Xu Y, Teng Y, Dong X et al (2021) Genome-resolved metagenomics reveals how soil bacterial communities respond to elevated H-2 availability. Soil Biol Biochem 163:108464. https://doi.org/10.1016/j.soilbio.2021.108464
Yang Z, Zhang Y, Lv Y et al (2019) H2 Metabolism revealed by metagenomic analysis of subglacial sediment from East Antarctica. J Microbiol 57:1095–1104. https://doi.org/10.1007/s12275-019-9366-2
Yu J (2018) Fixation of carbon dioxide by a hydrogen-oxidizing bacterium for value-added products. World J Microbiol Biotechnol 34:89. https://doi.org/10.1007/s11274-018-2473-0
Yu J, Dow A, Pingali S (2013) The energy efficiency of carbon dioxide fixation by a hydrogen-oxidizing bacterium. Int J Hydrog Energy 38:8683–8690. https://doi.org/10.1016/j.ijhydene.2013.04.153
Zhang Y, He X, Dong Z (2009) Effect of hydrogen on soil bacterial community structure in two soils as determined by terminal restriction fragment length polymorphism. Plant Soil 320:295–305. https://doi.org/10.1007/s11104-009-9894-3
Zimmer D, Schwartz E, Tran-Betcke A et al (1995) Temperature tolerance of hydrogenase expression in Alcaligenes eutrophus is conferred by a single amino acid exchange in the transcriptional activator HoxA. J Bacteriol 177:2373–2380. https://doi.org/10.1128/jb.177.9.2373-2380.1995
Zomer RJ, Trabucco A, Bossio DA, Verchot LV (2008) Climate change mitigation: a spatial analysis of global land suitability for clean development mechanism afforestation and reforestation. Agric Ecosyst Environ 126:67–80. https://doi.org/10.1016/j.agee.2008.01.014
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This work was financially supported by the Shanghai Science & Technology Innovation Project (21DZ1209801) and Tongji University interdisciplinary joint research project (2022-4-ZD-02).
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Fan, X., Zhang, X., Zhao, G. et al. Aerobic hydrogen-oxidizing bacteria in soil: from cells to ecosystems. Rev Environ Sci Biotechnol 21, 877–904 (2022). https://doi.org/10.1007/s11157-022-09633-0
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DOI: https://doi.org/10.1007/s11157-022-09633-0