Abstract
The Marine Roseobacter Clade (MRC) is a numerically and biogeochemically significant component of the bacterioplankton. Annotation of multiple MRC genomes has revealed that an abundance of carbon monoxide dehydrogenase (CODH) cox genes are present, subsequently implying a role for the MRC in marine CO cycling. The cox genes fall into two distinct forms based on sequence analysis of the coxL gene; forms I and II. The two forms are unevenly distributed across the MRC genomes. Most (18/29) of the MRC genomes contain only the putative form II coxL gene. Only 10 of the 29 MRC genomes analysed have both the putative form II and the definitive form I coxL. None have only the form I coxL. Genes previously shown to be required for post-translational maturation of the form I CODH enzyme are absent from the MRC genomes containing only form II. Subsequent analyses of a subset of nine MRC strains revealed that only MRC strains with both coxL forms are able to oxidise CO.
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References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ . (1990). Basic local alignment search tool. J Mol Biol 215: 403–410.
Brinkhoff T, Giebel HA, Simon M . (2008). Diversity, ecology, and genomics of the Roseobacter clade: a short overview. Arch Microbiol 189: 531–539.
Cunliffe M, Schafer H, Harrison E, Cleave S, Upstill-Goddard RC, Murrell JC . (2008). Phylogenetic and functional gene analysis of the bacterial and archaeal communities associated with the surface microlayer of an estuary. ISME J 2: 776–789.
Daniel LS, Solomon S . (1998). On the climate forcing of carbon monoxide. J Geophys Res 103: 13249–13260.
Dunfield KE, King GM . (2004). Molecular analysis of carbon monoxide-oxidizing bacteria associated with recent Hawaiian volcanic deposits. Appl Environ Microbiol 70: 4242–4248.
Dunfield KE, King GM . (2005). Analysis of the distribution and diversity in recent Hawaiian volcanic deposits of a putative carbon monoxide dehydrogenase large subunit gene. Environ Microbiol 7: 1405–1412.
Fuhrmann S, Ferner M, Jeffke T, Henne A, Gottschalk G, Meyer O . (2003). Complete nucleotide sequence of the circular megaplasmid pHCG3 of Oligotropha carboxidovorans: function in the chemolithoautotrophic utilization of CO, H2 and CO2 . Gene 32: 67–75.
Giovannoni S, Rappé M . (2000). Evolution, diversity and molecular ecology of marine prokaryotes. In: Kirchman DL (ed). Microbial Ecology of the Oceans. Wiley-Liss: New Jersey, USA.
González JM, Kiene RP, Moran MA . (1999). Transformation of sulfur compounds by an abundant lineage of marine bacteria in the α-subclass of the class Proteobacteria. Appl Environ Microbiol 65: 3810–3819.
Hansel CM, Francis CA . (2006). Coupled photochemical and enzymatic Mn(II) oxidation pathways of a planktonic Roseobacter-like bacterium. Appl Environ Microbiol 72: 3543–3549.
King GM . (2003). Molecular and culture-based analyses of aerobic carbon monoxide oxidizer diversity. Appl Environ Microbiol 69: 7257–7265.
King GM, Weber CF . (2007). Distribution, diversity and ecology of aerobic CO-oxidizing bacteria. Nat Rev Microbiol 5: 107–118.
Lorite MJ, Tachil J, Sanjuin J, Meyer O, Bedmar EJ . (2000). Carbon monoxide dehydrogenase activity in Bradyrhizobium japonicum. Appl Environ Microbiol 66: 1871–1876.
Meyer O, Schlegel HG . (1983). Biology of aerobic carbon monoxide-oxidizing bacteria. Annu Rev Microbiol 37: 277–310.
Moran MA, Belas R, Schell MA . (2007). Ecological genomics of marine Roseobacters. Appl Environ Microbiol 73: 4559–4569.
Moran MA, Buchan A, Gonzalez JM, Heidelberg JF, Whitman WB, Kiene RP et al. (2004). Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature 432: 910–913.
Moran MA, Miller WL . (2007). Resourceful heterotrophs make the most of light in the coastal ocean. Nat Rev Microbiol 5: 792–800.
Newton RJ, Griffin LE, Bowles KM, Meile C, Gifford S, Givens CE et al. (2010). Genome characteristics of a generalist marine bacterial lineage. ISME J 4: 784–798.
Pelzmann A, Ferner M, Gnida M, Meyer-Klaucke W, Maisel T, Meyer O . (2009). The CoxD protein of Oligotropha carboxidovorans is a predicted AAA+ ATPase chaperone involved in the biogenesis of the CO dehydrogenase [CuSMoO2] cluster. J Biol Chem 284: 9578–9586.
Schafer H, McDonald IR, Nightingale PD, Murrell JC . (2005). Evidence for the presence of a CmuA methyl transferase pathway in novel marine methyl halide-oxidizing bacteria. Environ Microbiol 7: 839–852.
Tamura K, Dudley J, Nei M, Kumar S . (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596–1599.
Tolli JD, Taylor CD . (2005). Biological CO oxidation in the Sargasso Sea and in Vineyard Sound, Massachusetts. Limnol Oceanogr 50: 1205–1212.
Wagner-Döbler I, Biebl H . (2006). Environmental biology of the marine Roseobacter lineage. Annu Rev Microbiol 60: 255–280.
Weber CF, King GM . (2007). Physiological, ecological and phylogenetic characterization of Stappia, a marine CO-oxidizing bacterial genus. Appl Environ Microbiol 73: 1266–1276.
Yurkov VV, Beatty JT . (1998). Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 62: 695–724.
Zafiriou OC, Andrews SS, Wang W . (2003). Concordant estimates of oceanic carbon monoxide source and sink processes in the Pacific yield a balanced global ‘blue-water’ CO budget. Global Biogeochem Cy 17: 15-11-15-13.
Zuo Y, Jones RD . (1995). Formation of carbon monoxide by photolysis of dissolved marine organic material and its significance in the carbon cycling of the oceans. Naturwiss 82: 472–474.
Acknowledgements
This study relied on the genome sequences made publically available by the Gordon and Betty Moore Foundation (http://www.moore.org) through RoseoBase (www.roseobase.org). I particularly thank Shalabh Sharma and Mary Ann Moran at the Department of Marine Sciences, University of Georgia, Athens, USA for providing the 16S rRNA gene sequences used in Figure 1.
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Cunliffe, M. Correlating carbon monoxide oxidation with cox genes in the abundant Marine Roseobacter Clade. ISME J 5, 685–691 (2011). https://doi.org/10.1038/ismej.2010.170
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DOI: https://doi.org/10.1038/ismej.2010.170
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