Abstract
The marine γ-proteobacterium Oceanimonas doudoroffii was shown to have at least three different enzymes, each of which can cleave dimethylsulfoniopropionate (DMSP), an abundant compatible solute made by different classes of marine phytoplankton. These various DMSP lyases have similarities, but also some differences to those that had been identified in other bacteria. This was demonstrated by cloning each of the corresponding genes and transferring them into other species of bacteria in which backgrounds they conferred the ability to catabolise DMSP, releasing dimethyl sulfide (DMS) as one of the products (Ddd+ phenotype; DMSP-dependent DMS). One of these genes resembled dddD, which was in a cluster with other ddd genes variously involved in subsequent steps of DMSP catabolism, in DMSP import and in DMSP-dependent transcriptional regulation. The other two gene products both had sequence similarity to the previously identified DddP lyase. However, these two Oceanimonas DddP polypeptides were not particularly similar to each other and were in two different sub-branches compared to those that had been studied in strains of the Roseobacter clade of bacteria. One of these O. doudoroffii enzymes, DddP1, most closely resembled gene products in a disparate group of microbes that included two bacteria, Vibrio orientalis and Puniceispirillum marinum and, more strikingly, some Ascomycete fungi that can catabolise DMSP. Previously, the only bacteria known to have multiple ways to catabolise DMSP were in the Roseobacter clade, which were also the only bacteria that had been shown to have functional DddP DMSP lyases. Thus Oceanimonas doudoroffii is unusual on more than one count and likely acquired its dddD, dddP1 and dddP2 genes by independent horizontal gene transfer events.
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References
Anon (2001) Notification that new names and new combinations have appeared in volume 51 part 1, of the IJSEM. Int J Syst Evol Microbiol 51:269
Baumann L, Baumann P, Mandel M, Allen RD (1972) Taxonomy of aerobic marine eubacteria. J Bacteriol 110:402–429
Beringer JE (1974) R factor transfer in Rhizobium. J Gen Microbiol 84:188–198
Brown GR, Sutcliffe IC, Cummings SP et al (2001) Reclassification of [Pseudomonas] doudoroffii (Baumann et al. 1983) into the genus Oceanomonas gen. nov. as Oceanomonas doudoroffii comb. nov., and description of a phenol-degrading bacterium from estuarine water as Oceanomonas baumannii sp. nov. I. J Syst Evol Microbiol 51:67–72
Curson ARJ, Rogers R, Todd JD, Brearley CA, Johnston AWB (2008) Molecular genetic analysis of a dimethylsulfoniopropionate lyase that liberates the climate-changing gas dimethylsulfide in several marine alpha-proteobacteria and Rhodobacter sphaeroides. Env Microbiol 10:757–767
Curson ARJ, Sullivan MJ, Todd JD, Johnston AWB (2010) Identification of genes for dimethyl sulfide production in bacteria in the gut of Atlantic Herring (Clupea harengus). ISME J 4:144–146
Curson ARJ, Sullivan MJ, Todd JD, Johnston AWB (2011) DddY, a periplasmic dimethylsulfoniopropionate lyase found in taxonomically diverse species of proteobacteria. ISME J 5:1191–1200
de Souza MP, Yoch DC (1995) Comparative physiology of dimethyl sulfide production by dimethylsulfoniopropionate lyase in Pseudomonas doudoroffii and Alcaligenes sp. Strain M3A. Appl Env Microbiol 61:3986–3991
de Souza MP, Yoch DC (1996) N-terminal amino acid sequences and comparison of DMSP lyases from Pseudomonas doudoroffii and Alcaligenes strain M3A. In: Kiene RP, Visscher PT, Keller MD, Kirst GO (eds) Environmental and biological chemistry on dimethylsulfoniopropionate and related sulfonium compounds. Plenum Press, New York, pp 293–304
Dickschat JS, Zell C, Brock NL (2010) Pathways and substrate specificity of DMSP catabolism in marine bacteria of the Roseobacter clade. Chem Biochem 15:417–425
Figurski DH, Helinski DR (1979) Replication of an origin-containing derivative of plasmid RK2 dependant on a plasmid function provided in trans. Proc Nat’l Acad Sci USA 76:1648–1652
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 Env Microbiol 65:3810–3819
González JM, Covert JS, Whitman WB, Henriksen JR, Mayer F, Scharf B, Schmitt R, Buchan A, Fuhrman JA, Kiene RP, Moran MA (2003) Silicibacter pomeroyi sp. nov. and Roseovarius nubinhibens sp. nov., dimethylsulfoniopropionate-demethylating bacteria from marine environments. Int J Syst Evol Microbiol 53:1261–1269
Howard EC, Henriksen JR, Buchan A, Reisch CR, Bürgmann H et al (2006) Bacterial taxa that limit sulfur flux from the ocean. Science 314:649–652
Ivanova EP, Flavier S, Christen R (2004) Phylogenetic relationships among marine Alteromonas-like proteobacteria: emended description of the family Alteromonadaceae and proposal of Pseudoalteromonadaceae fam. nov., Colwelliaceae fam. nov., Shewanellaceae fam. nov., Moritellaceae fam. nov., Ferri. Int J Syst Evol Microbiol 54:1773–1788
Kirkwood M, Le Brun NE, Todd JD, Johnston AWB (2010a) The dddP gene of Roseovarius nubinhibens encodes a novel lyase that cleaves dimethylsulfoniopropionate into acrylate plus dimethyl sulfide. Microbiol 156:1900–1906
Kirkwood M, Todd JD, Rypien KL, Johnston AWB (2010b) The opportunistic coral pathogen Aspergillus sydowii contains dddP and makes dimethyl sulfide from dimethylsulfoniopropionate. ISME J 4:147–150
Ledyard KM, DeLong EF, Dacey JWH (1993) Characterization of a DMSP-degrading bacterial isolate from the Sargasso Sea. Arch Microbiol 160:312–318
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
Oh HM, Kwon KK, Kang I, Kang SG, Lee JH, Kim SJ, Cho JC (2010) Complete genome sequence of “Candidatus Puniceispirillum marinum” IMCC1322, a representative of the SAR116 clade in the alphaproteobacteria. J Bacteriol 192:3240–3241
Raina JB, Dinsdale EA, Willis BL, Bourne DG (2010) Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? Trends Microbiol 18:101–108
Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S et al (2007) The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol 5(3):e77. doi:10.1371/journal.pbio.0050077
Sambrook S, Fritsch EF, Maniatis T (1989) “Molecular cloning: a laboratory manual”. Cold Spring Harbor Laboratory, Cold Spring Harbor
Schäfer H, Myronova N, Boden R (2010) Microbial degradation of dimethylsulfide and related C1-sulfur compounds: organisms and pathways controlling fluxes of sulfur in the biosphere. J Exp Bot 61:315–334
Spaink HP, Okker RJH, Wijffelman CA, Pees E, Lugtenberg BJJ (1987) Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI. Plant Mol Biol 9:27–39
Staskawicz B, Dahlbeck D, Keen N, Napoli C (1987) Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J Bacteriol 169:5789–5794
Studier FW, Moffat BA (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189:113–130
Sullivan MJ, Curson ARJ, Shearer N, Todd JD, Green RT, Johnston AWB (2011) Unusual regulation of a leaderless operon involved in the catabolism of dimethylsulfoniopropionate in Rhodobacter sphaeroides. PLoS One 6(1):e15972
Sun L, Curson ARJ, Todd JD, Johnston AWB (2011) Diversity of DMSP transport in marine bacteria, revealed by genetic analyses. Biogeochemistry. doi:10.1007/s10533-011-9666-z
Todd JD, Rogers R, Li YG, Wexler M, Bond PL et al (2007) Structural and regulatory genes required to make the gas dimethyl sulfide in bacteria. Science 315:666–669
Todd JD, Curson ARJ, Dupont CL, Nicholson P, Johnston AWB (2009) The dddP gene, encoding a novel enzyme that converts dimethylsulfoniopropionate into dimethyl sulfide, is widespread in ocean metagenomes and marine bacteria and also occurs in some ascomycete fungi. Env Microbiol 11:1376–1385
Todd JD, Curson ARJ, Nikolaidou-Katsaridou N, Brearley CA, Watmough NJ, Chan Y, Page PC, Sun L, Johnston AWB (2010) Molecular dissection of bacterial acrylate catabolism–unexpected links with dimethylsulfoniopropionate catabolism and dimethyl sulfide production. Env Microbiol 12:327–343
Todd JD, Curson ARJ, Kirkwood M, Sullivan MJ, Green RT, Johnston AWB (2011a) DddQ, a novel, cupin-containing, dimethylsulfoniopropionate lyase in marine roseobacters and in uncultured marine bacteria. Env Microbiol 13:427–438
Todd JD, Kirkwood M, Newton-Payne S, Johnston AWB (2011b). DddW, a third DMSP lyase in a model Roseobacter marine bacterium, Ruegeria pomeroyi DSS-3. ISME J. doi: 10.1038/ismej.2011.79. [Epub ahead of print]
Wexler M, Yeoman KH, Stevens JB, de Luca NG, Sawers G, Johnston AWB (2001) The Rhizobium leguminosarum tonB gene is required for the uptake of siderophore and haem as sources of iron. Mol Microbiol 41:801–816
Wood WB (1966) Host specificity of DNA produced by Escherichia coli: bacterial mutations affecting the restriction and modification of DNA. J Mol Biol 16:118–133
Yang Y, Yeh L, Cao Y, Baumann L, Baumann P, Tang JS, Beaman B (1983) Characterization of marine luminous bacteria isolated off the coast of China and description of Vibrio orientalis sp. nov. Curr Microbiol 8:95–100
Yoch DC (2002) Dimethylsulfoniopropionate: its sources, role in the marine food web, and biological degradation to dimethylsulfide. Appl Env Microbiol 68:5804–5815
Yoch DC, Ansede JH, Rabinowitz KS (1997) Evidence for intracellular and extracellular dimethylsulfoniopropionate (DMSP) lyases and DMSP uptake sites in two species of marine bacteria. Appl Env Microbiol 63:3182–3188
Young JPW, Crossman LC, Johnston AWB, Thomson NR, Ghazoui ZF, Hull KH et al (2006) The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol 7:R34
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The work was funded by grants from the United Kingdom Biotechnology and Biological Sciences Research Council and the Natural Environment Research Council and a Tyndall Centre Studentship to EKF. We thank Jennifer Sampson and Pamela Wells for technical support.
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Curson, A.R.J., Fowler, E.K., Dickens, S. et al. Multiple DMSP lyases in the γ-proteobacterium Oceanimonas doudoroffii . Biogeochemistry 110, 109–119 (2012). https://doi.org/10.1007/s10533-011-9663-2
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DOI: https://doi.org/10.1007/s10533-011-9663-2