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An Updated genome annotation for the model marine bacterium Ruegeria pomeroyi DSS-3
Standards in Genomic Sciences volume 9, Article number: 11 (2014)
The Erratum to this article has been published in Standards in Genomic Sciences 2015 10:112
When the genome of Ruegeria pomeroyi DSS-3 was published in 2004, it represented the first sequence from a heterotrophic marine bacterium. Over the last ten years, the strain has become a valuable model for understanding the cycling of sulfur and carbon in the ocean. To ensure that this genome remains useful, we have updated 69 genes to incorporate functional annotations based on new experimental data, and improved the identification of 120 protein-coding regions based on proteomic and transcriptomic data. We review the progress made in understanding the biology of R. pomeroyi DSS-3 and list the changes made to the genome.
Ruegeria pomeroyi DSS-3 is an important model organism in studies of the physiology and ecology of marine bacteria . It is a genetically tractable strain that has been essential for elucidating bacterial roles in the marine sulfur and carbon cycles [2, 3] and the biology and genomics of the marine Roseobacter clade , a group that makes up 5–20% of bacteria in ocean surface waters [5, 6]. Here we update the R. pomeroyi DSS-3 genome with 189 changes collected from the work of several research groups over the last ten years.
Genome sequencing information
The R. pomeroyi DSS-3 genome has been instrumental in expanding knowledge of the marine sulfur cycle, particularly the role of marine bacteria in controlling the flux of volatile sulfur to the atmosphere [3, 22] and the bacterial transformations of dimethylsulfoniopropionate (DMSP) [3, 23], dimethylsulfide, and sulfonates [24, 25]. Since 2006, many of the genes mediating the uptake and metabolism of DMSP have been identified from the R. pomeroyi DSS-3 genome. These include the demethylation pathway genes dmdABCD[2, 22] and the cleavage pathway genes dddD, dddP, dddQ, dddW, acuK, acuN, dddA and dddC[23, 26, 27]. Although many genes were identified first in R. pomeroyi DSS-3, these are now known to be widespread in ocean surface waters and harbored by a number of other major marine bacterial taxa . R. pomeroyi DSS-3 also transforms sulfonates and has served as a model for identifying genes required for the degradation of 2,3-dihydroxypropane-1-sufonate (hpsNOP) , L-cysteate (cuyARZ) , taurine (tauXY) and n-acetyltaurine (naaST) [24, 31, 32], 3-sulfolactate (slcD, suyAB) [29, 33] and isethionate (iseJ) .
Members of the marine Roseobacter lineage are capable of oxidizing sulfite and thiosulfate [34, 35], and the genome sequence of R. pomeroyi DSS-3 revealed the sox gene cluster that mediates these processes [1, 4]. Recently, the reverse dissimilatory sulfite reductase gene cluster was found in sediment-dwelling roseobacters, and homologs to the sulfite reductase genes from this pathway (soeABC) were identified in the R. pomeroyi DSS-3 genome . R. Pomeroyi DSS-3 was initially studied as a member of an ecologically important bacterial taxon that appeared unusually amenable to cultivation , but has now played a major role in improving our understanding of global sulfur transformations.
Studies of the R. pomeroyi DSS-3 genome have also provided a better understanding of the genes involved in processing organic nitrogen compounds, such as taurine and N-acetyltaurine [24, 31, 32]. The bacterium can catabolize lysine by using the saccharopine pathway, which is used by many plants and animals, or by using the lysine dehydrogenase pathway. Under high salt conditions, it preferentially uses the latter pathway, leading to biosynthesis of the osmolyte aminoadipate. The function of several genes in both lysine pathways has recently been experimentally verified .
R. pomeroyi DSS-3 genome hosts at least 28 tripartite ATP-independent periplasmic (TRAP) transporters . While the substrates for many of these transporters are not yet known, the TRAP transporters responsible for the uptake of 2,3-dihydroxypropane-1-sufonate (hpsKLM) , isethionate (iseKLM) , and ectoine and hydroxyectoine have been characterized (uehABC) [38, 39]. Ectoine and hydroxyectoine are used as compatible solutes by some bacteria and phytoplankton, although R. pomeroyi DSS-3 can also assimilate carbon and nitrogen from them . Several genes involved in ectoine metabolism (doe, eut, ueh) have been found in the R. pomeroyi DSS-3 genome based on homology with genes in Halomonas elongata DSM 2581 T .
Progress has been made in understanding the mechanisms of metal uptake in R. pomeroyi DSS-3. The manganese uptake regulator mur has been experimentally validated, as have the ABC transporter genes for manganese metabolism (sitABCD) . In total, 69 annotation changes were made based on new experimental data identifying genes responsible for carbon, nitrogen, sulfur, and metal uptake and metabolism .
Proteomics  and mRNA sequencing have resulted in 120 protein coding regions being identified, removed or corrected in the updated genome. A detailed proteomic study of R. pomeroyi DSS-3 under diverse growth conditions resulted in the identification of 26 novel open reading frames (ORFs) and 5 sequencing errors . The function of most of the new genes is not known and 16 of the expressed polypeptides do not have known homologs. The 26 ORFs missed in the original annotation is a significant number but less than the 1% error rate predicted for Glimmer 2 . The proteomic analysis was also able to correct the start sites of 64 genes , enhancing the information that had been obtained only from the DNA sequence . Many of the ORFs identified by proteomics were independently confirmed using strand-specific messenger RNA sequences from continuous cultures  and the gene calling software Glimmer 3 . This method also identified several genes that were originally annotated in the wrong orientation, including a novel bacterial collagen gene (SPO1999).
A list of genome updates based on these biochemical, genetic, and -omics approaches is provided in Table 4, and full details in Additional file 1: Table S1. The updated annotations have been incorporated into the official genome record at the National Center for Biotechnology Information (Bethesda, MD, USA) under accession numbers CP000031.2 and CP000032.1 and Roseobase (http://roseobase.org).
Ten years after the publication of the Ruegeria pomeroyi DSS-3 genome sequence, advances in knowledge of gene function and structural genome features motivated an annotation update. As an ecologically-relevant heterotrophic marine bacterium that is amenable to laboratory studies and genetic manipulation, R. pomeroyi is serving as a valuable model organism for investigations of the ecology, biochemistry, and biogeochemistry of ocean microbes.
Moran MA, Buchan A, González JM, Heidelberg JF, Whitman WB, Kiene RP, Henriksen JR, King GM, Belas R, Fuqua C, Brinkac L, Lewis M, Shivani J, Weaver B, Pai G, Eisen JA, Rahe E, Sheldon WM, Ye W, Miller TR, Carlton J, Rasko DA, Paulsen IT, Ren Q, Daugherty SC, Deboy RT, Dodson RJ, Durkin AS, Madupu R, Nelson WC, et al.: Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature 2004, 432: 910–3. PubMed http://dx.doi.org/10.1038/nature03170 10.1038/nature03170
Reisch CR, Stoudemayer MJ, Varaljay VA, Amster IJ, Moran MA, Whitman WB: Novel pathway for assimilation of dimethylsulphoniopropionate widespread in marine bacteria. Nature 2011, 473: 208–11. PubMed http://dx.doi.org/10.1038/nature10078 10.1038/nature10078
Moran MA, Reisch CR, Kiene RP, Whitman WB: Genomic insights into bacterial DMSP transformations. Annu Rev Mar Sci 2012, 4: 523–42. PubMed http://dx.doi.org/10.1146/annurev-marine-120710–100827 10.1146/annurev-marine-120710-100827
Newton RJ, Griffin LE, Bowles KM, Meile C, Gifford S, Givens CE, Howard EC, King E, Oakley CA, Reisch CR, Rinta-Kanto JM, Sharma S, Sun S, Varaljay V, Vila-Costa M, Westrich JR, Moran MA: Genome characteristics of a generalist marine bacterial lineage. ISME J 2010, 4: 784–98. PubMed http://dx.doi.org/10.1038/ismej.2009.150 10.1038/ismej.2009.150
González JM, Moran MA: Numerical dominance of a group of marine bacteria in the alpha-subclass of the class Proteobacteria in coastal seawater. Appl Environ Microbiol 1997, 63: 4237–42. PubMed
Buchan A, González JM, Moran MA: Overview of the marine roseobacter lineage. Appl Environ Microbiol 2005, 71: 5665–77. PubMed http://dx.doi.org/10.1128/AEM.71.10.5665–5677.2005 10.1128/AEM.71.10.5665-5677.2005
Yi H, Lim YW, Chun J: Taxonomic evaluation of the genera Ruegeria and Silicibacter : a proposal to transfer the genus Silicibacter Petursdottir and Kristjansson 1999 to the genus Ruegeria Uchino et al. 1999. Int J Syst Evol Microbiol 2007, 57: 815–9. PubMed http://dx.doi.org/10.1099/ijs.0.64568–0 10.1099/ijs.0.64568-0
González JM, Covert JS, Whitman WB, Henriksen JR, Mayer F, Scharf B, Schmitt R, Buchan A, Fuhrman JA, Kiene RP, Moran MA: Silicibacter pomeroyi sp. nov. and Roseovarius nubinhibens sp. nov., dimethylsulfoniopropionate-demethylating bacteria from marine environments. Int J Syst Evol Microbiol 2003, 53: 1261–9. PubMed http://dx.doi.org/10.1099/ijs.0.02491–0 10.1099/ijs.0.02491-0
Field D, Garrity G, Gray T, Morrison N, Selengut J, Sterk P, Tatusova T, Thomson N, Allen MJ, Angiuoli SV, Stevens R, Swift P, Taylor C, Tateno Y, Tett A, Turner S, Ussery D, Vaughan B, Ward N, Whetzel T, San GI, Wilson G, Wipat A: The minimum information about a genome sequence (MIGS) specification. Nat Biotechnol 2008, 26: 541–7. PubMed http://dx.doi.org/10.1038/nbt1360 10.1038/nbt1360
Woese CR, Kandler O, Wheelis ML: Towards a natural system of organisms: proposal for the domains Archaea , Bacteria, and Eucarya. Proc Natl Acad Sci USA 1990, 87: 4576–9. PubMed http://dx.doi.org/10.1073/pnas.87.12.4576 10.1073/pnas.87.12.4576
Garrity GM, Bell JA, Lilburn TPhylum XIV: Proteobacteria phyl. nov. In Bergey's Manual of Systematic Bacteriology. Volume 2. 2nd edition. Edited by: Garrity GM, Brenner DJ, Krieg NR, Staley JT. New York: Part B, Springer; 2005:1.
Validation List No. 107: List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 2006, 56: 1–6. PubMed http://dx.doi.org/10.1099/ijs.0.64188–0
Garrity GM, Bell JA, Class LT I: Alphaproteobacteria class. nov. In Bergey's Manual of Systematic Bacteriology. Volume 2. 2nd edition. Edited by: Garrity GM, Brenner DJ, Krieg NR, Staley JT. New York: Part C, Springer; 2005:1.
Garrity GM, Bell JA, Order LT III: Rhodobacterales ord. nov. In Bergey's Manual of Systematic Bacteriology. Volume 2. 2nd edition. Edited by: Garrity GM, Brenner DJ, Krieg NR, Staley JT. New York: Part C, Springer; 2005:161.
Garrity GM, Bell JA, Family LT I: Rhodobacteraceae fam. nov. In Bergey's Manual of Systematic Bacteriology. Volume 2. 2nd edition. Edited by: Garrity GM, Brenner DJ, Krieg NR, Staley JT. New York: Part C, Springer; 2005:161.
Validation List no. 68: Validation of publication of new names and new combinations previously effectively published outside the IJSB. Int J Syst Bacteriol 1999, 49: 1–3. http://dx.doi.org/10.1099/00207713–49–1-1
Uchino Y, Hirata A, Yokota A, Sugiyama J: Reclassification of marine Agrobacterium species: Proposals of Stappia stellulata gen. nov., comb. nov., Stappia aggregata sp. nov., nom. rev., Ruegeria atlantica gen. nov., comb. nov., Ruegeria gelatinovora comb. nov., Ruegeria algicola comb. nov., and Ahrensia kieliense gen. nov., sp. nov., nom. rev. J Gen Appl Microbiol 1998, 44: 201–10. PubMed http://dx.doi.org/10.2323/jgam.44.201 10.2323/jgam.44.201
Martens T, Heidorn T, Pukall R, Simon M, Tindall BJ, Brinkhoff T: Reclassification of Roseobacter gallaeciensis Ruiz-Ponte et al. 1998 as Phaeobacter gallaeciensis gen. nov., comb. nov., description of Phaeobacter inhibens sp. nov., reclassification of Ruegeria algicola (Lafay et al. 1995) Uchino et al. 1999 as Marinovum algicola gen. nov., comb. nov., and emended descriptions of the genera Roseobacter, Ruegeria and Leisingera . Int J Syst Evol Microbiol 2006, 56: 1293–304. PubMed http://dx.doi.org/10.1099/ijs.0.63724–0 10.1099/ijs.0.63724-0
Vandecandelaere I, Nercessian O, Segaert E, Achouak W, Faimali M, Vandamme P: Ruegeria scottomollicae sp. nov., isolated from a marine electroactive biofilm. Int J Syst Evol Microbiol 2008, 58: 2726–33. PubMed http://dx.doi.org/10.1099/ijs.0.65843–0 10.1099/ijs.0.65843-0
Delcher AL: Improved microbial gene identification with GLIMMER. Nucleic Acids Res 1999, 27: 4636–41. PubMed http://dx.doi.org/10.1093/nar/27.23.4636 10.1093/nar/27.23.4636
Eisen JA, Nelson KE, Paulsen IT, Heidelberg JF, Wu M, Dodson RJ, Deboy R, Gwinn ML, Nelson WC, Haft DH, Hickey EK, Peterson JD, Durkin AS, Kolonay JL, Yang F, Holt I, Umayam LA, Mason T, Brenner M, Shea TP, Parksey D, Nierman WC, Feldblyum TV, Hansen CL, Craven MB, Radune D, Vamathevan J, Khouri H, White O, Gruber TM, et al.: The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium. Proc Natl Acad Sci USA 2002, 99: 9509–14. PubMed http://dx.doi.org/10.1073/pnas.132181499 10.1073/pnas.132181499
Howard EC, Henriksen JR, Buchan A, Reisch CR, Bürgmann H, Welsh R, Ye W, González JM, Mace K, Joye SB, Kiene RP, Whitman WB, Moran MA: Bacterial taxa that limit sulfur flux from the ocean. Science 2006, 314: 649–52. PubMed http://dx.doi.org/10.1126/science.1130657 10.1126/science.1130657
Todd JD, Curson ARJ, Kirkwood M, Sullivan MJ, Green RT, Johnston AWB: DddQ, a novel, cupin-containing, dimethylsulfoniopropionate lyase in marine roseobacters and in uncultured marine bacteria. Environ Microbiol 2011, 13: 427–38. PubMed http://dx.doi.org/10.1111/j.1462–2920.2010.02348.x 10.1111/j.1462-2920.2010.02348.x
Gorzynska AK, Denger K, Cook AM, Smits THM: Inducible transcription of genes involved in taurine uptake and dissimilation by Silicibacter pomeroyi DSS-3. Arch Microbiol 2006, 185: 402–6. PubMed http://dx.doi.org/10.1007/s00203–006–0106–8 10.1007/s00203-006-0106-8
Weinitschke S, Sharma PI, Stingl U, Cook AM, Smits THM: Gene clusters involved in isethionate degradation by terrestrial and marine bacteria. Appl Environ Microbiol 2010, 76: 618–21. PubMed http://dx.doi.org/10.1128/AEM.01818–09 10.1128/AEM.01818-09
Todd JD, Kirkwood M, Newton-Payne S, Johnston AWB: DddW, a third DMSP lyase in a model Roseobacter marine bacterium, Ruegeria pomeroyi DSS-3. ISME J 2012, 6: 223–6. PubMed http://dx.doi.org/10.1038/ismej.2011.79 10.1038/ismej.2011.79
Todd JD, Curson ARJ, Sullivan MJ, Kirkwood M, Johnston AWB: The Ruegeria pomeroyi acuI gene has a role in DMSP catabolism and resembles yhdH of E. coli and other bacteria in conferring resistance to acrylate. PLoS ONE 2012, 7: e35947. PubMed http://dx.doi.org/10.1371/journal.pone.0035947 10.1371/journal.pone.0035947
Varaljay VA, Howard EC, Sun S, Moran MA: Deep sequencing of a dimethylsulfoniopropionate-degrading gene ( dmdA ) by using PCR primer pairs designed on the basis of marine metagenomic data. Appl Environ Microbiol 2010, 76: 609–17. PubMed http://dx.doi.org/10.1128/AEM.01258–09 10.1128/AEM.01258-09
Mayer J, Huhn T, Habeck M, Denger K, Hollemeyer K, Cook AM: 2,3-Dihydroxypropane-1-sulfonate degraded by Cupriavidus pinatubonensis JMP134: purification of dihydroxypropanesulfonate 3-dehydrogenase. Microbiology 2010, 156: 1556–64. PubMed http://dx.doi.org/10.1099/mic.0.037580–0 10.1099/mic.0.037580-0
Denger K, Smits THM, Cook AM: L-cysteate sulpho-lyase, a widespread pyridoxal 5’-phosphate-coupled desulphonative enzyme purified from Silicibacter pomeroyi DSS-3. Biochem J 2006, 394: 657–64. PubMed http://dx.doi.org/10.1042/BJ20051311 10.1042/BJ20051311
Denger K, Lehmann S, Cook AM: Molecular genetics and biochemistry of N-acetyltaurine degradation by Cupriavidus necator H16. Microbiology 2011, 157: 2983–91. PubMed http://dx.doi.org/10.1099/mic.0.048462–0 10.1099/mic.0.048462-0
Cook AM, Denger K: Metabolism of taurine in microorganisms: a primer in molecular biodiversity? Adv Exp Med Biol 2006, 583: 3–13. PubMed http://dx.doi.org/10.1007/978–0-387–33504–9_1 10.1007/978-0-387-33504-9_1
Denger K, Mayer J, Buhmann M, Weinitschke S, Smits THM, Cook AM: Bifurcated degradative pathway of 3-sulfolactate in Roseovarius nubinhibens ISM via sulfoacetaldehyde acetyltransferase and (S)-cysteate sulfolyase. J Bacteriol 2009, 191: 5648–56. PubMed http://dx.doi.org/10.1128/JB.00569–09 10.1128/JB.00569-09
González JM, Kiene RP, Moran MA: Transformation of sulfur compounds by an abundant lineage of marine bacteria in the alpha-subclass of the class Proteobacteria . Appl Environ Microbiol 1999, 65: 3810–9. PubMed
Moran MA, González JM, Kiene RP: Linking a bacterial taxon to sulfur cycling in the sea: Studies of the marine Roseobacter group. Geomicrobiol J 2003, 20: 375–88. http://dx.doi.org/10.1080/01490450303901 10.1080/01490450303901
Lehmann S: Sulfite dehydrogenases in organotrophic bacteria: enzymes, genes and regulation. University of Konstanz: Doctoral Dissertation; 2013:142.
Neshich IA, Kiyota E, Arruda P: Genome-wide analysis of lysine catabolism in bacteria reveals new connections with osmotic stress resistance. ISME J 2013, 7: 2400–10. PubMed http://dx.doi.org/10.1038/ismej.2013.123 10.1038/ismej.2013.123
Mulligan C, Fischer M, Thomas GH: Tripartite ATP-independent periplasmic (TRAP) transporters in Bacteria and Archaea . FEMS Microbiol Rev 2011, 35: 68–86. PubMed http://dx.doi.org/10.1111/j.1574–6976.2010.00236.x 10.1111/j.1574-6976.2010.00236.x
Lecher J, Pittelkow M, Zobel S, Bursy J, Bönig T, Smits SH, Schmitt L, Bremer E: The crystal structure of UehA in complex with ectoine-A comparison with other TRAP-T binding proteins. J Mol Biol 2009, 389: 58–73. PubMed http://dx.doi.org/10.1016/j.jmb.2009.03.077 10.1016/j.jmb.2009.03.077
Schwibbert K, Marin-Sanguino A, Bagyan I, Heidrich G, Lentzen G, Seitz H, Rampp M, Schuster SC, Klenk HP, Pfeiffer F, Oesterhelt D, Kunte HJ: A blueprint of ectoine metabolism from the genome of the industrial producer Halomonas elongata DSM 2581 T. Environ Microbiol 2011, 13: 1973–94. PubMed http://dx.doi.org/10.1111/j.1462–2920.2010.02336.x 10.1111/j.1462-2920.2010.02336.x
Green RT, Todd JD, Johnston AWB: Manganese uptake in marine bacteria; the novel MntX transporter is widespread in Roseobacters, Vibrios, Alteromonadales and the SAR11 and SAR116 clades. ISME J 2013, 7: 581–91. PubMed http://dx.doi.org/10.1038/ismej.2012.140 10.1038/ismej.2012.140
Christie-Oleza JA, Miotello G, Armengaud J: High-throughput proteogenomics of Ruegeria pomeroyi : seeding a better genomic annotation for the whole marine Roseobacter clade. BMC Genomics 2012, 13: 73. PubMed http://dx.doi.org/10.1186/1471–2164–13–73 10.1186/1471-2164-13-73
Chan LK, Newton RJ, Sharma S, Smith CB, Rayapati P, Limardo AJ, Meile C, Moran MA: Transcriptional changes underlying elemental stoichiometry shifts in a marine heterotrophic bacterium. Front Microbiol 2012, 3: 159. PubMed http://dx.doi.org/10.3389/fmicb.2012.00159
Delcher AL, Bratke KA, Powers EC, Salzberg SL: Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 2007, 23: 673–9. PubMed http://dx.doi.org/10.1093/bioinformatics/btm009 10.1093/bioinformatics/btm009
This work was supported by NSF grant MCB-1158037 and the Gordon and Betty Moore Foundation. We are grateful to A. Cook and K. Denger for adopting R. pomeroyi DSS-3 in their sulfonate research, and A. Burns for reviewing the mRNA data.
The authors declare that they have no competing interests.
ARR conceived of the study, carried out the bioinformatics analyses, and wrote the manuscript. CBS carried out the bioinformatics analyses and wrote the manuscript. MAM conceived of the study and wrote the manuscript. All authors read and approved the final manuscript.
An erratum to this article is available at http://dx.doi.org/10.1186/s40793-015-0107-9.
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Rivers, A.R., Smith, C.B. & Moran, M.A. An Updated genome annotation for the model marine bacterium Ruegeria pomeroyi DSS-3. Stand in Genomic Sci 9, 11 (2014) doi:10.1186/1944-3277-9-11