Atmospheric hydrogen scavenging: From enzymes to ecosystems

Applied and Environmental Microbiology

Volumn 81, Issue 4, 2015, Pages 1190-1199

  Greening, Chris ^a,b   Constant, Philippe ^c   Hards, Kiel ^b   Morales, Sergio E ^b   Oakeshott, John G ^a   Russell, Robyn J ^a   Taylor, Matthew C ^a   Berney, Michael ^d   Conrad, Ralf ^e   Cookb, Gregory M ^b,f  

^a CSIRO   (Australia)

^b UNIVERSITY OF OTAGO   (New Zealand)

^c INRS INSTITUT ARMAND FRAPPIER   (Canada)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^e MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^f MAURICE WILKINS CENTRE FOR MOLECULAR BIODISCOVERY   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGY; EARTH ATMOSPHERE; ECOLOGY; ENZYMES;

ENERGY GENERATIONS; MOLECULAR HYDROGEN; RECENT PROGRESS; RESPIRATORY CHAINS; SOIL MICROBIAL; STREPTOMYCETES; STRESS TOLERANCE; [NIFE]-HYDROGENASE;

HYDROGEN;

BACTERIUM; ENZYME ACTIVITY; HYDROGEN; MICROBIAL ECOLOGY; SCAVENGING (CHEMISTRY); SOIL MICROORGANISM;

ACTINOBACTERIA; CORYNEBACTERINEAE; STREPTOMYCINEAE;

BACTERIAL PROTEIN; HYDROGEN; HYDROGENASE; NICKEL-IRON HYDROGENASE;

ACTINOBACTERIA; ATMOSPHERE; CHEMISTRY; ECOSYSTEM; ENZYMOLOGY; GENETICS; METABOLISM; MICROBIOLOGY;

ACTINOBACTERIA; AIR MICROBIOLOGY; ATMOSPHERE; BACTERIAL PROTEINS; ECOSYSTEM; HYDROGEN; HYDROGENASE;

EID: 84922022068     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03364-14     Document Type: Short Survey

References (73)

1. Schmidt U. 1974. Molecular hydrogen in the atmosphere. Tellus A 26: 78-90. http://dx.doi.org/10.1111/j.2153-3490.1974.tb01954.x.
2. Conrad R, Seiler W. 1980. Contribution of hydrogen production by biological nitrogen fixation to the global hydrogen budget. J Geophys Res 85:5493-5498. http://dx.doi.org/10.1029/JC085iC10p05493.
3. 2: a critical review. Tellus B 61:500-535. http://dx.doi.org/10.1111/j.1600-0889.2009 .00416.x.
4. Novelli PC, Lang PM, Masarie A, Hurst DF, Elkins W. 1999. Molecular hydrogen in the troposphere: global distribution and budget. J Geophys Res Atmos 104:30427-30444. http://dx.doi.org/10.1029/1999JD900788.
5. 2 budget and the response of its soil uptake under the changing environment. Sci Total Environ 407:1809-1823. http://dx.doi.org/10.1016/j.scitotenv.2008.10.064.
6. Schultz MG, Diehl T, Brasseur GP, Zittel W. 2003. Air pollution and climate-forcing impacts of a global hydrogen economy. Science 302:624- 627. http://dx.doi.org/10.1126/science.1089527.
7. Tromp TK, Shia R-L, Allen M, Eiler JM, Yung YL. 2003. Potential environmental impact of a hydrogen economy on the stratosphere. Science 300:1740-1742. http://dx.doi.org/10.1126/science.1085169.
8. Rhee TS, Brenninkmeijer CAM, Röckmann T. 2006. The overwhelming role of soils in the global atmospheric hydrogen cycle. Atmos Chem Phys 6:1611-1625. http://dx.doi.org/10.5194/acp-6-1611-2006.
9. Yashiro H, Sudo K, Yonemura S, Takigawa M. 2011. The impact of soil uptake on the global distribution of molecular hydrogen: chemical transport model simulation. Atmos Chem Phys 11:6701-6719. http://dx.doi .org/10.5194/acp-11-6701-2011.
10. 2O, and NO). Microbiol Rev 60:609-640.
11. Conrad R, Seiler W. 1979. The role of hydrogen bacteria during the decomposition of hydrogen by soil. FEMS Microbiol Lett 6:143-145. http: //dx.doi.org/10.1111/j.1574-6968.1979.tb04296.x.
12. Conrad R, Aragno M, Seiler W. 1983. The inability of hydrogen bacteria to utilize atmospheric hydrogen is due to threshold and affinity for hydrogen. FEMS Microbiol Lett 18:207-210. http://dx.doi.org/10.1111/j.1574 -6968.1983.tb00479.x.
13. 2 oxidation in respiring and denitrifying Paracoccus denitrificans. FEMS Microbiol Lett 78:259-263. http://dx.doi.org/10.1111/j.1574-6968.1991.tb04452.x.
14. 2. FEMS Microbiol Lett 111:337-341. http://dx.doi.org/10.1111/j.1574-6968.1993.tb06408.x.
15. Maimaiti J, Zhang Y, Yang J, Cen Y-P, Layzell DB, Peoples M, Dong Z. 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. http://dx.doi.org/10.1111/j.1462 -2920.2006.01155.x.
16. 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. http://dx.doi.org/10.1111/j.1462 -2920.2009.02130.x.
17. Vignais PM, Billoud B. 2007. Occurrence, classification, and biological function of hydrogenases: an overview. Chem Rev 107:4206-4272. http: //dx.doi.org/10.1021/cr050196r.
18. Conrad R, Weber M, Seiler W. 1983. Kinetics and electron transport of soil hydrogenases catalyzing the oxidation of atmospheric hydrogen. Soil Biol Biochem 15:167-173. http://dx.doi.org/10.1016/0038-0717 (83)90098-6.
19. Conrad R, Seiler W. 1981. Decomposition of atmospheric hydrogen by soil microorganisms and soil enzymes. Soil Biol Biochem 13:43-49. http: //dx.doi.org/10.1016/0038-0717(81)90101-2.
20. Guo R, Conrad R. 2008. Extraction and characterization of soil hydrogenases oxidizing atmospheric hydrogen. Soil Biol Biochem 40:1149-1154. http://dx.doi.org/10.1016/j.soilbio.2007.12.007.
21. 2-oxidizing bacteria in non-axenic soil and sterile soil amended with Streptomyces sp. PCB7. Soil Biol Biochem 43:1888-1893. http://dx.doi.org/10.1016/j.soilbio.2011 .05.009.
22. 2. ISME J 2:1066 -1076. http://dx.doi.org/10.1038 /ismej.2008.59.
23. 2 using two membraneassociated, oxygen-dependent [NiFe] hydrogenases. Proc Natl Acad Sci U S A 111:4257-4261. http://dx.doi.org/10.1073/pnas.1320586111.
24. Meredith LK, Rao D, Bosak T, Klepac-Ceraj V, Tada KR, Hansel CM, Ono S, Prinn RG. 2014. Consumption of atmospheric hydrogen during the life cycle of soil-dwelling actinobacteria. Environ Microbiol Rep 6:226-238. http://dx.doi.org/10.1111/1758-2229.12116.
25. 2-oxidizing bacteria. Appl Environ Microbiol 77: 6027-6035. http://dx.doi.org/10.1128/AEM.00673-11.
26. Bontemps C, Toussaint M, Revol P, Hotel L, Jeanbille M, Turpault M, Blaudez D, Leblond P, Lorraine D. 2013. Taxonomic and functional diversity of Streptomyces in a forest soil. FEMS Microbiol Lett 342:157- 167. http://dx.doi.org/10.1111/1574-6968.12126.
27. Berney M, Greening C, Hards K, Collins D, Cook GM. 2014. Three different [NiFe] hydrogenases confer metabolic flexibility in the obligate aerobe Mycobacterium smegmatis. Environ Microbiol 16:318-330. http: //dx.doi.org/10.1111/1462-2920.12320.
28. 2-based lithoautotrophy and anaerobiosis. J Mol Biol 332:369 -383. http://dx.doi.org/10.1016 /S0022-2836(03)00894-5.
29. Schäfer C, Friedrich B, Lenz O. 2013. Novel, oxygen-insensitive group 5 [NiFe]-hydrogenase in Ralstonia eutropha. Appl Environ Microbiol 79: 5137-5145. http://dx.doi.org/10.1128/AEM.01576-13.
30. Schäfer C. 2014. Proteinbiochemische, spektroskopische und röntgenkristallographische Untersuchung der Actinobakteriellen [NiFe]- Hydrogenase aus Ralstonia eutropha. Ph.D. thesis. Humboldt-Universität zu Berlin, Berlin, Germany.
31. Lubitz W, Ogata H, Rüdiger O, Reijerse E. 2014. Hydrogenases. Chem Rev 114:4081-4148. http://dx.doi.org/10.1021/cr4005814.
32. Greening CA. 2013. Physiological roles of the three [NiFe]-hydrogenases in Mycobacterium smegmatis. Ph.D. thesis. University of Otago, Dunedin, New Zealand.
33. Lenz O, Schwartz E, Dernedde J. 1994. The Alcaligenes eutrophus H16 hoxX gene participates in hydrogenase regulation. J Bacteriol 176:4385- 4393.
34. Berney M, Cook GM. 2010. Unique flexibility in energy metabolism allows mycobacteria to combat starvation and hypoxia. PLoS One 5:e8614. http://dx.doi.org/10.1371/journal.pone.0008614.
35. 2 in air. J Biol Chem 284:465-477. http://dx.doi.org/10.1074/jbc.M803676200.
36. Fritsch J, Scheerer P, Frielingsdorf S, Kroschinsky S, Friedrich B, Lenz O, Spahn CMT. 2011. The crystal structure of an oxygen-tolerant hydrogenase uncovers a novel iron-sulphur centre. Nature 479:249-252. http: //dx.doi.org/10.1038/nature10505.
37. 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. http://dx.doi.org/10.1038/nature10504.
38. Bowman L, Flanagan L, Fyfe P, Parkin A, Hunter WN, Sargent F. 2014. How the structure of the large subunit controls function in an oxygentolerant [NiFe]-hydrogenase. Biochem J 458:449-458. http://dx.doi.org /10.1042/BJ20131520.
39. Rousset M, Montet Y, Guigliarelli B, Forget N, Asso M, Bertrand P, Fontecilla-Camps JC, Hatchikian EC. 1998. [3Fe-4S] to [4Fe-4S] cluster conversion in Desulfovibrio fructosovorans [NiFe] hydrogenase by sitedirected mutagenesis. Proc Natl Acad SciUSA95:11625-11630. http://dx .doi.org/10.1073/pnas.95.20.11625.
40. 2-sensing [NiFe]-hydrogenase from Ralstonia eutropha H16 is based on limited access of oxygen to the active site. J Biol Chem 280:23791-23796. http://dx.doi.org/10.1074/jbc.M503260200.
41. Cano M, Volbeda A, Guedeney G, Aubert-Jousset E, Richaud P, Peltier G, Cournac L. 2014. Improved oxygen tolerance of the Synechocystis sp. PCC 6803 bidirectional hydrogenase by site-directed mutagenesis of putative residues of the gas diffusion channel. Int J Hydrogen Energy 39: 16872-16884. http://dx.doi.org/10.1016/j.ijhydene.2014.08.030.
42. Schuler S, Conrad R. 1991. Hydrogen oxidation activities in soil as influenced by pH, temperature, moisture, and season. Biol Fertil Soils 12:127- 130. http://dx.doi.org/10.1007/BF00341488.
43. 2 uptake measured in the laboratory. Geophys Res Lett 33:L14813. http://dx.doi.org/10.1029/2006GL026749.
44. 2 uptake activity in soils. Soil Biol Biochem 42:1574-1580. http://dx.doi .org/10.1016/j.soilbio.2010.05.027.
45. Scherr N, Nguyen L. 2009. Mycobacterium versus Streptomyces-we are different, we are the same. Curr Opin Microbiol 12:699-707. http://dx.doi .org/10.1016/j.mib.2009.10.003.
46. 2 consumption and a tritium exchange assay. Biol Fertil Soils 17:125-128. http://dx.doi.org/10.1007/BF00337744.
47. Berney M, Greening C, Conrad R, Jacobs WR, Cook GM. 2014. An obligately aerobic soil bacterium activates fermentative hydrogen production to survive reductive stress during hypoxia. Proc Natl Acad Sci U S A 111:11479-11484. http://dx.doi.org/10.1073/pnas.1407034111.
48. 2. PLoS One 9:e103034. http://dx.doi.org/10 .1371/journal.pone.0103034.
49. 2 cycle. Eur J Inorg Chem 2011:919-921. http://dx.doi.org/10.1002/ejic.201001255.
50. Greening C, Cook GM. 2014. Integration of hydrogenase expression and hydrogen sensing in bacterial cell physiology. Curr Opin Microbiol 18: 30-38. http://dx.doi.org/10.1016/j.mib.2014.02.001.
51. Kumar A, Toledo JC, Patel RP, Lancaster JR, Steyn AJC. 2007. Mycobacterium tuberculosis DosS is a redox sensor and DosT is a hypoxia sensor. Proc Natl Acad Sci U S A 104:11568-11573. http://dx.doi.org/10.1073 /pnas.0705054104.
52. Smith-Downey NV, Randerson JT, Eiler JM. 2008. Molecular hydrogen uptake by soils in forest, desert, and marsh ecosystems in California. J Geophys Res 113:G03037. http://dx.doi.org/10.1029/2008JG000701.
53. King GM. 2003. Contributions of atmospheric CO and hydrogen uptake to microbial dynamics on recent Hawaiian volcanic deposits. Appl Environ Microbiol 69:4067-4075. http://dx.doi.org/10.1128/AEM.69.7.4067 -4075.2003.
54. Constant P, Poissant L, Villemur R. 2008. Annual hydrogen, carbon monoxide and carbon dioxide concentrations and surface to air exchanges in a rural area (Québec, Canada). Atmos Environ 42:5090-5100. http://dx .doi.org/10.1016/j.atmosenv.2008.02.021.
55. King GM, Weber CF, Nanba K, Sato Y, Ohta H. 2008. Atmospheric CO and hydrogen uptake and CO oxidizer phylogeny for Miyake-jima, Japan volcanic deposits. Microbes Environ 23:299-305. http://dx.doi.org/10 .1264/jsme2.ME08528.
56. Conrad R, Seiler W. 1979. Field measurements of hydrogen evolution by nitrogen-fixing legumes. Soil Biol Biochem 11:689-690. http://dx.doi.org /10.1016/0038-0717(79)90041-5.
57. Dong Z, Wu L, Kettlewell B, Caldwell CD, Layzell DB. 2003. Hydrogen fertilization of soils-is this a benefit of legumes in rotation? Plant Cell Environ 26:1875-1879. http://dx.doi.org/10.1046/j.1365-3040.2003.01103.x.
58. Seiler W, Liebl KH, Stöhr WT, Zakosek H. 1977. Zeitschrift fiir Pflanzenernahrung und Bodenkunde. Z Pflanzenernaehr Bodenkd 272:257- 272.
59. 2 uptake. Tellus B 52:347- 362. http://dx.doi.org/10.1034/j.1600-0870.2000.00103.x.
60. 2 fixation. Soil Biol Biochem 37:1938-1945. http://dx.doi.org/10.1016 /j.soilbio.2005.02.035.
61. 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. http://dx.doi .org/10.1128/AEM.02072-09.
62. 2 fixation and C1 metabolism in the actinobacterium Pseudonocardia dioxanivorans CB1190. Environ Microbiol 15:3040-3053. http://dx.doi.org/10.1111 /1462-2920.12144.
63. McLearn N, Dong Z. 2002. Microbial nature of the hydrogen-oxidizing agent in hydrogen-treated soil. Biol Fertil Soils 35:465-469. http://dx.doi .org/10.1007/s00374-002-0495-z.
64. Pumphrey GM, Ranchou-Peyruse A, Spain JC. 2011. Cultivationindependent detection of autotrophic hydrogen-oxidizing bacteria by DNA stable-isotope probing. Appl Environ Microbiol 77:4931-4938. http://dx.doi.org/10.1128/AEM.00285-11.
65. Blagodatskaya E, Kuzyakov Y. 2013. Active microorganisms in soil: critical review of estimation criteria and approaches. Soil Biol Biochem 67: 192-211. http://dx.doi.org/10.1016/j.soilbio.2013.08.024.
66. Lennon JT, Jones SE. 2011. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9:119-130. http://dx.doi.org/10.1038/nrmicro2504.
67. 2, NO). Indian J Microbiol 39:193-203.
68. Janssen PH. 2006. Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719-1728. http://dx.doi.org/10.1128/AEM.72.3.1719-1728.2006.
69. Bergmann GT, Bates ST, Eilers KG, Lauber CL, Caporaso G, Walters WA, Knight R, Fierer N. 2011. The under-recognized dominance of Verrucomicrobia in soil bacterial communities. Soil Biol Biochem 43: 1450-1455. http://dx.doi.org/10.1016/j.soilbio.2011.03.012.
70. Lynch RC, King AJ, Farías ME, Sowell P, Vitry C, Schmidt SK. 2012. The potential for microbial life in the highest-elevation (>6000 m.a.s.l.) mineral soils of the Atacama region. J Geophys Res 117:G02028. http://dx .doi.org/10.1029/2012JG001961.
71. Pointing SB, Chan Y, Lacap DC, Lau MCY, Jurgens JA, Farrell RL. 2009. Highly specialized microbial diversity in hyper-arid polar desert. Proc Natl Acad Sci U S A 106:19964-19969. http://dx.doi.org/10.1073 /pnas.0908274106.
72. 2 under resting and growing conditions. Arch Microbiol 137:26-32. http://dx.doi.org/10.1007/BF00425803.
73. Schuler S, Conrad R. 1990. Soils contain two different activities for oxidation of hydrogen. FEMS Microbiol Lett 73:77-83. http://dx.doi.org/10 .1111/j.1574-6968.1990.tb03927.x.