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

Abstract

Phaeobacter gallaeciensis, a member of the abundant marine Roseobacter clade, is known to be an effective colonizer of biotic and abiotic marine surfaces. Production of the antibiotic tropodithietic acid (TDA) makes P. gallaeciensis a strong antagonist of many bacteria, including fish and mollusc pathogens. In addition to TDA, several other secondary metabolites are produced, allowing the mutualistic bacterium to also act as an opportunistic pathogen. Here we provide the manually annotated genome sequences of the P. gallaeciensis strains DSM 17395 and 2.10, isolated at the Atlantic coast of north western Spain and near Sydney, Australia, respectively. Despite their isolation sites from the two different hemispheres, the genome comparison demonstrated a surprisingly high level of synteny (only 3% nucleotide dissimilarity and 88% and 93% shared genes). Minor differences in the genomes result from horizontal gene transfer and phage infection. Comparison of the P. gallaeciensis genomes with those of other roseobacters revealed unique genomic traits, including the production of iron-scavenging siderophores. Experiments supported the predicted capacity of both strains to grow on various algal osmolytes. Transposon mutagenesis was used to expand the current knowledge on the TDA biosynthesis pathway in strain DSM 17395. This first comparative genomic analysis of finished genomes of two closely related strains belonging to one species of the Roseobacter clade revealed features that provide competitive advantages and facilitate surface attachment and interaction with eukaryotic hosts.

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

“…TDA, which is believed to be the prime agent of Roseobacter antibacterial activity Bruhn et al, 2006), was detected in all R. mobilis by liquid chromatography-tandem mass spectrometry and correlates with the presence of the central genes required for the biosynthesis of TDA, tdaBCDE, in all strains (Supplementary Table S8). In F1926, tdaBCDE are located on a plasmid, the 147 kb plasmid, as has been demonstrated for other TDA producers (Thole et al, 2012). No TDA, or only traces, was detected in MB cultures from non-inhibitory strains or under conditions that abolished activity, such as aeration of the R. mobilis strains.…”

“…The element herein referred to as Roseobacter phage RDJL Φ 1 (Supplementary Table S9) (Huang et al, 2011) due to PHAST annotation (Zhou et al, 2011) has also been described as gene transfer agent (Zhao et al, 2009;Thole et al, 2012). Gene transfer agents have first been described in Rhodobacteraceae (Marrs, 1974) and are widespread within the family (Biers et al, 2008;Huang et al, 2011;Thole et al, 2012).…”

“…Gene transfer agents have first been described in Rhodobacteraceae (Marrs, 1974) and are widespread within the family (Biers et al, 2008;Huang et al, 2011;Thole et al, 2012). This specific gene transfer agent has been found in all to-date sequenced Roseobacter genome sequences, but strain HTCC1062 (Zhao et al, 2009).…”

“…In contrast, we repeatedly have isolated P. inhibens from surface biofilms in Danish harbor areas . It is, therefore, tempting to speculate that R. mobilis is the open-water counterpart to the coastal, macrosurface-attached P. inhibens (Supplementary Table S1 and Supplementary material S8 in (Thole et al, 2012)). In the TARA data set (Global Ocean Microbial Reference Gene Catalog), Ruegeria sp.…”

Molecular and phenotypic analyses reveal the non-identity of the Phaeobacter gallaeciensis type strain deposits CIP 105210T and DSM 17395

“…P. gallaeciensis DSM 24588 (52.10; Thole et al, 2012) Profiles of the extrachromosomal elements. To analyse the plasmid content of the Phaeobacter strains, their high-molecular-mass total genomic DNA was prepared within agarose plugs as previously described and subjected to pulsed-field gel electrophoresis (PFGE; Pradella et al, 2010).…”