Persistence of the dominant soil phylum Acidobacteria by trace gas scavenging

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 33, 2015, Pages 10497-10502

  Greening, Chris ^a,b   Carere, Carlo R ^c,d   Rushton Green, Rowena ^a   Harold, Liam K ^a   Hards, Kiel ^a   Taylor, Matthew C ^b   Morales, Sergio E ^a   Stott, Matthew B ^c   Cook, Gregory M ^a,e  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b CSIRO   (Australia)

^c GNS SCIENCE   (New Zealand)

^d SCION   (New Zealand)

^e UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Dormancy; Extremophile; Hydrogen; Hydrogenase; Rare biosphere

Indexed keywords

GLUCOSE; HYDROGEN; NICKEL IRON HYDROGENASE; CARBON; GAS; HYDROGENASE; OXYGEN; SOIL;

ACIDOBACTERIA; AEROBIC BACTERIUM; ARTICLE; ATMOSPHERE; BACTERIAL CELL; BACTERIAL GENE; BACTERIUM CULTURE; BACTERIUM ISOLATION; CARBON SOURCE; CONTROLLED STUDY; ENERGY RESOURCE; ENZYME ACTIVITY; GAS SCAVENGER; GENE EXPRESSION; NEW ZEALAND; NONHUMAN; OPERON; OXIDATION; PHYLUM; PRIORITY JOURNAL; PYRINOMONAS METHYLALIPHATO; RESPIRATORY CHAIN; SOIL MICROFLORA; UPREGULATION; VOLCANO; AMINO ACID SEQUENCE; CHEMISTRY; ELECTRON; ELECTRON TRANSPORT; GAS; GAS CHROMATOGRAPHY; GENE EXPRESSION REGULATION; KINETICS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PHYLOGENY; REPRODUCIBILITY; SEQUENCE HOMOLOGY; SOIL;

ACIDOBACTERIA; ACIDOBACTERIUM; ACTINOBACTERIA; BACTERIA (MICROORGANISMS);

ACIDOBACTERIA; AMINO ACID SEQUENCE; ATMOSPHERE; CARBON; CHROMATOGRAPHY, GAS; ELECTRON TRANSPORT; ELECTRONS; GASES; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN; HYDROGENASE; KINETICS; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; OXYGEN; PHYLOGENY; REPRODUCIBILITY OF RESULTS; SEQUENCE HOMOLOGY, AMINO ACID; SOIL; SOIL MICROBIOLOGY;

EID: 84939864398     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1508385112     Document Type: Article

References (45)

1. Lennon JT, Jones SE (2011) Microbial seed banks: The ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9(2):119-130.
2. Jones SE, Lennon JT (2010) Dormancy contributes to the maintenance of microbial diversity. Proc Natl Acad Sci USA 107(13):5881-5886.
3. Price PB, Sowers T (2004) Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proc Natl Acad Sci USA 101(13):4631-4636.
4. Morita RY (1999) Is H2 the universal energy source for long-term survival? Microb Ecol 38(4):307-320.
5. Alvarez HM, Steinbüchel A (2002) Triacylglycerols in prokaryotic microorganisms. Appl Microbiol Biotechnol 60(4):367-376.
6. González-Pastor JE, Hobbs EC, Losick R (2003) Cannibalism by sporulating bacteria. Science 301(5632):510-513.
7. Greening C, et al. (2015) Atmospheric hydrogen scavenging: From enzymes to ecosystems. Appl Environ Microbiol 81(4):1190-1199.
8. Quiza L, Lalonde I, Guertin C, Constant P (2014) Land-use influences the distribution and activity of high affinity CO-oxidizing bacteria associated to type I-coxL genotype in soil. Front Microbiol 5:271.
9. Greening C, Cook GM (2014) Integration of hydrogenase expression and hydrogen sensing in bacterial cell physiology. Curr Opin Microbiol 18:30-38.
10. Bergmann GT, et al. (2011) The under-recognized dominance of Verrucomicrobia in soil bacterial communities. Soil Biol Biochem 43(7):1450-1455.
11. Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72(3):1719-1728.
12. Quaiser A, et al. (2003) Acidobacteria form a coherent but highly diverse group within the bacterial domain: Evidence from environmental genomics. Mol Microbiol 50(2):563-575.
13. Barns SM, Takala SL, Kuske CR (1999) Wide distribution and diversity of members of the bacterial kingdom Acidobacterium in the environment. Appl Environ Microbiol 65(4):1731-1737.
14. Stott MB, et al. (2008) Isolation of novel bacteria, including a candidate division, from geothermal soils in New Zealand. Environ Microbiol 10(8):2030-2041.
15. Sait M, Hugenholtz P, Janssen PH (2002) Cultivation of globally distributed soil bacteria from phylogenetic lineages previously only detected in cultivation-independent surveys. Environ Microbiol 4(11):654-666.
16. Janssen PH, Yates PS, Grinton BE, Taylor PM, Sait M (2002) Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia. Appl Environ Microbiol 68(5):2391-2396.
17. Rappé MS, Giovannoni SJ (2003) The uncultured microbial majority. Annu Rev Microbiol 57(1):369-394.
18. Crowe MA, et al. (2014) Pyrinomonas methylaliphatogenes gen. nov., sp. nov., a novel group 4 thermophilic member of the phylum Acidobacteria from geothermal soils. Int J Syst Evol Microbiol 64(Pt 1):220-227.
19. 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(3):821-829.
20. Constant P, Chowdhury SP, Hesse L, Pratscher J, Conrad R (2011) 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(17):6027-6035.
21. 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(10): 1066-1076.
22. 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(1):318-330.
23. Greening C, Villas-Bôas SG, Robson JR, Berney M, Cook GM (2014) The growth and survival of Mycobacterium smegmatis is enhanced by co-metabolism of atmospheric H2. PLoS One 9(7):e103034.
24. Greening C, Berney M, Hards K, Cook GM, Conrad R (2014) A soil actinobacterium scavenges atmospheric H2 using two membrane-associated, oxygen-dependent [NiFe] hydrogenases. Proc Natl Acad Sci USA 111(11):4257-4261.
25. Vignais PM, Billoud B (2007) Occurrence, classification, and biological function of hydrogenases: An overview. Chem Rev 107(10):4206-4272.
26. Berney M, Cook GM (2010) Unique flexibility in energy metabolism allows mycobacteria to combat starvation and hypoxia. PLoS One 5(1):e8614.
27. Meredith LK, et al. (2014) Consumption of atmospheric hydrogen during the life cycle of soil-dwelling actinobacteria. Environ Microbiol Rep 6(3):226-238.
28. Ehhalt DH, Rohrer F (2009) The tropospheric cycle of H2: A critical review. Tellus B Chem Phys Meterol 61(3):500-535.
29. Schäfer C, Friedrich B, Lenz O (2013) Novel, oxygen-insensitive group 5 [NiFe]-hydrogenase in Ralstonia eutropha. Appl Environ Microbiol 79(17):5137-5145.
30. Ward NL, et al. (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75(7):2046-2056.
31. Eichorst SA, Kuske CR, Schmidt TM (2011) Influence of plant polymers on the distribution and cultivation of bacteria in the phylum Acidobacteria. Appl Environ Microbiol 77(2):586-596.
32. Koch IH, Gich F, Dunfield PF, Overmann J (2008) Edaphobacter modestus gen. nov., sp. nov., and Edaphobacter aggregans sp. nov., acidobacteria isolated from alpine and forest soils. Int J Syst Evol Microbiol 58(Pt 5):1114-1122.
33. Männistö MK, Rawat S, Starovoytov V, Häggblom MM (2012) 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 62(Pt 9):2097-2106.
34. Constant P, Poissant L, Villemur R (2009) Tropospheric H(2) budget and the response of its soil uptake under the changing environment. Sci Total Environ 407(6):1809-1823.
35. 2-oxidizing bacteria predict atmospheric H2 soil uptake activity better than soil microbial community composition. Soil Biol Biochem 85:1-9.
36. 2O, and NO). Microbiol Rev 60(4):609-640.
37. Dunfield PF, Liesack W, Henckel T, Knowles R, Conrad R (1999) High-affinity methane oxidation by a soil enrichment culture containing a type II methanotroph. Appl Environ Microbiol 65(3):1009-1014.
38. Bull ID, Parekh NR, Hall GH, Ineson P, Evershed RP (2000) Detection and classification of atmospheric methane oxidizing bacteria in soil. Nature 405(6783):175-178.
39. King GM, Weber CF (2007) Distribution, diversity and ecology of aerobic CO-oxidizing bacteria. Nat Rev Microbiol 5(2):107-118.
40. Snapper SB, Melton RE, Mustafa S, Kieser T, Jacobs WRJ, Jr (1990) Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol Microbiol 4(11):1911-1919.
41. Aung HL, et al. (2015) Novel regulatory roles of cAMP receptor proteins in fast-growing environmental mycobacteria. Microbiology 161(Pt 3):648-661.
42. Bull TJ, Hermon-Taylor J, Pavlik I, El-Zaatari F, Tizard M (2000) Characterization of IS900 loci in Mycobacterium avium subsp. paratuberculosis and development of multiplex PCR typing. Microbiology 146(Pt 9):2185-2197.
43. nd Ed, pp 57-60.
44. Conrad R, Goodwin S, Zeikus JG (1987) Hydrogen metabolism in a mildly acidic lake sediment (Knaack Lake). FEMS Microbiol Lett 45(4):243-249.
45. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30(12):2725-2729.