Ecological Genomics of Marine Roseobacters

Abstract

Bacterioplankton of the marine Roseobacter clade have genomes that reflect a dynamic environment and diverse interactions with marine plankton. Comparative genome sequence analysis of three cultured representatives suggests that cellular requirements for nitrogen are largely provided by regenerated ammonium and organic compounds (polyamines, allophanate, and urea), while typical sources of carbon include amino acids, glyoxylate, and aromatic metabolites. An unexpectedly large number of genes are predicted to encode proteins involved in the production, degradation, and efflux of toxins and metabolites. A mechanism likely involved in cell-to-cell DNA or protein transfer was also discovered: vir-related genes encoding a type IV secretion system typical of bacterial pathogens. These suggest a potential for interacting with neighboring cells and impacting the routing of organic matter into the microbial loop. Genes shared among the three roseobacters and also common in nine draft Roseobacter genomes include those for carbon monoxide oxidation, dimethylsulfoniopropionate demethylation, and aromatic compound degradation. Genes shared with other cultured marine bacteria include those for utilizing sodium gradients, transport and metabolism of sulfate, and osmoregulation.In surface waters of the open ocean, 1 in 10 bacterial cells is a member of the Roseobacter group (17). In coastal waters, the number of Roseobacter cells increases to 1 in 5 (11, 19). Despite their obvious ecological success, however, roseobacters do not fit the stereotype of a small, metabolically conservative, "oligotrophic" bacterium (8, 18). Instead, they are large (0.08 m 3 ) (38), easily cultured (19), and respond readily to increased substrate availability (7). Analysis of the first Roseobacter genome sequence, that of Silicibacter pomeroyi, revealed a fairly large genome (4.5 Mb) housing abundant and diverse transporters, complex regulatory systems, and multiple pathways for acquiring carbon and energy in seawater. Roseobacters thus appear to be quite versatile from metabolic and ecological standpoints (43), with an assortment of strategies for obtaining carbon and nutrients and, directly or indirectly, affecting the biogeochemical status of seawater.The availability of two additional closed genome sequences of cultured roseobacters provides the opportunity for an ecologically based analysis of the genetic capabilities of this bacterial taxon. The three organisms are assumed to have different niches in the surface ocean based on the conditions of their isolation: S. pomeroyi is a free-living heterotrophic bacterioplankter obtained from coastal seawater (43), congener Silicibacter sp. strain TM1040 (96% 16S rRNA sequence identity to S. pomeroyi [ Fig. 1]) is an associate of the marine dinoflagellate Pfiesteria piscicida (1, 40), and Jannaschia sp. strain CCS1 (with 94% 16S rRNA sequence identity to the two Silicibacter species) represents a recently discovered class of marine aerobic bacteriochlorophyll a-based phototrophs (4). Our comparative an...

Phaeobacter gallaeciensis genomes from globally opposite locations reveal high similarity of adaptation to surface life

“…Only two genomic features likely delineate P. gallaeciensis from other roseobacters. Although these findings support the 'mix and match' hypothesis (Moran et al, 2007) for the heterogeneity of genomic content of roseobacters, they also underline the importance of intra-species comparisons to detect genomic traits that could result in strainlevel specificity.…”

Global occurrence and heterogeneity of the Roseobacter-clade species Ruegeria mobilis

“…In comparison, the closed genomes of R. pomeroyi DSS-3 and Ruegeria sp. TM1040 consist Figure 2 Heatmap of average nucleotide identity (ANI) analysis of Ruegeria mobilis strains, Ruegeria type strains and selected Roseobacter type strains (Richter and Rosselló-Móra, 2009;Pritchard, 2014 (Sule and Belas, 2013) and a 4.1 Mb chromosome plus one megaplasmid (492 kb) with a GC content of 60% and 64.2%, respectively (Moran et al, 2004(Moran et al, , 2007. Two further plasmid sequences are available from Ruegeria sp.…”

“…As they were isolated from a wide variety of ecological niches, they might contribute substantially to the total Roseobacter gene repertoire (Moran et al, 2007). Thereby, R. mobilis stands in contrast to streamlined bacteria such as 'Candidatus Pelagibacter ubique' that has been described as example of a beneficiary in the Black Queen Hypothesis; a theory referring to the selective advantage of gene loss (Jeffrey et al, 2012).…”

The alkaline phosphatase PhoX is more widely distributed in marine bacteria than the classical PhoA

“…We next examined whether phoX is functional in marine isolates using two members of the Roseobacter clade, one of the most abundant bacterial groups in diverse marine habitats (Moran et al, 2007). S. pomeroyi DSS-3 and R. denitrificans both lack PhoA in their genome.…”