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An Updated genome annotation for the model marine bacterium Ruegeria pomeroyi DSS-3

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The Erratum to this article has been published in Standards in Genomic Sciences 2015 10:112

Abstract

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.

Introduction

Ruegeria pomeroyi DSS-3 is an important model organism in studies of the physiology and ecology of marine bacteria [1]. 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 [4], 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.

Organism information

Ruegeria pomeroyi DSS-3 (formerly Silicibacter pomeroyi DSS-3 [7]) is a motile gram-negative alphaproteobacterium in the marine Roseobacter lineage [8]. This mesophilic, heterotrophic bacterium was isolated from an estuary in coastal Georgia, U.S.A [9] (Table 1).

Table 1 Classification and general features of Ruegeria pomeroyi DSS-3 according to MIGS recommendations[9]

Genome sequencing information

Genome project history

The genome of R. pomeroyi DSS-3 was sequenced in 2003 by The Institute for Genomic Research (now the J. Craig Venter Institute) using Sanger sequencing (Table 2), and was annotated using Glimmer 2 [20] and the TIGR Assembler [21]. The genome was published in 2004 [1].

Table 2 Project information

Genome properties

The R. pomeroyi DSS-3 genome contains a 4,109,437 bp circular chromosome (5 bp shorter than previously reported [1]) and a 491,611 bp circular megaplasmid, with a G + C content of 64.1 (Table 3). A detailed description of the genome is found in the original article [1].

Table 3 Genome statistics

Reannotation

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 [28]. 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) [29], L-cysteate (cuyARZ) [30], taurine (tauXY) and n-acetyltaurine (naaST) [24, 31, 32], 3-sulfolactate (slcD, suyAB) [29, 33] and isethionate (iseJ) [25].

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 [36]. R. Pomeroyi DSS-3 was initially studied as a member of an ecologically important bacterial taxon that appeared unusually amenable to cultivation [5], 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 [37].

R. pomeroyi DSS-3 genome hosts at least 28 tripartite ATP-independent periplasmic (TRAP) transporters [1]. 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) [29], isethionate (iseKLM) [25], 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 [39]. 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 [40].

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) [41]. In total, 69 annotation changes were made based on new experimental data identifying genes responsible for carbon, nitrogen, sulfur, and metal uptake and metabolism [42].

Proteomics [42] 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 [42]. 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 [20]. The proteomic analysis was also able to correct the start sites of 64 genes [42], enhancing the information that had been obtained only from the DNA sequence [20]. Many of the ORFs identified by proteomics were independently confirmed using strand-specific messenger RNA sequences from continuous cultures [43] and the gene calling software Glimmer 3 [44]. 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).

Table 4 Updates and corrections to the genome sequence

Conclusion

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.

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Acknowledgements

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.

Author information

Correspondence to Mary Ann Moran.

Additional information

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

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.

Electronic supplementary material

Additional file 1: Table S1: Full details of updates and corrections to the Ruegeria pomeroyi DSS-3 genome sequence. (DOCX )

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Keywords

  • Roseobacter
  • DMSP