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Phaeobacter Gallaeciensis Genomes from Globally Opposite Locations Reveal High Similarity of Adaptation to Surface Life

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Phaeobacter Gallaeciensis Genomes from Globally Opposite Locations Reveal High Similarity of Adaptation to Surface Life The ISME Journal (2012) 6, 2229–2244 & 2012 International Society for Microbial Ecology All rights reserved 1751-7362/12 www.nature.com/ismej ORIGINAL ARTICLE Phaeobacter gallaeciensis genomes from globally opposite locations reveal high similarity of adaptation to surface life Sebastian Thole1, Daniela Kalhoefer1, Sonja Voget2, Martine Berger1, Tim Engelhardt1, Heiko Liesegang2, Antje Wollherr2, Staffan Kjelleberg3,4,RolfDaniel2, Meinhard Simon1, Torsten Thomas3 and Thorsten Brinkhoff1 1Institute for Chemistry and Biology of the Marine Environment, University of Oldenburg, Oldenburg, Germany; 2 Department of Genomic and Applied Microbiology and Go¨ttingen Genomics Laboratory, Institute of Microbiolgy and Genetics, University of Go¨ttingen, Go¨ttingen, Germany; 3 Centre of Marine Bio-Innovation and School of Biotechnology and Biomolecular Sciences, The University of New South Wales, Sydney, New South Wales, Australia and 4Singapore Centre on Environmental Life Sciences Engineering, Nanyang Technological University, Singapore, Singapore 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. The ISME Journal (2012) 6, 2229–2244; doi:10.1038/ismej.2012.62; published online 21 June 2012 Subject Category: integrated genomics and post-genomics approaches in microbial ecology Keywords: antibiotic; comparative genomics; prophages; Roseobacter clade; siderophores; symbiosis Introduction estuary, close relatives of P. gallaeciensis are among the most abundant bacterial groups (Sekiguchi et al., Phaeobacter gallaeciensis belongs to the Roseobac- 2002). Phaeobacter spp. are effective surface colo- ter clade (Martens et al., 2006), and members of this nizers and antagonistic against other bacteria due to genus are present in various marine habitats in the antibiotic tropodithietic acid (TDA), which is temperate regions (Pommier et al., 2005). Phaeobac- produced by several strains affiliated with the ter were found in turbot larva rearings (Hjelm et al., genera Phaeobacter, Ruegeria and Pseudovibiro 2004), cutaneous mucus of seahorses (Balca´zar et al., (Porsby et al., 2008; Gram et al., 2010). Because of 2010) and on cephalopods (Grigioni et al., 2000; the competitive success of Phaeobacter spp. against Barbieri et al., 2001). In the Chinese Changjiang fish and mollusc pathogens, ongoing research focuses on these organisms as probiotic agents in Correspondence: T Thomas, Centre of Marine Bio-Innovation and aquaculture (Rao et al., 2007; Porsby et al., 2008; School of Biotechnology and Biomolecular Sciences, The Prado et al., 2009). Most recently, it was shown University of New South Wales, Sydney, New South Wales 2052 that P. gallaeciensis also produces algicides upon Australia. sensing the lignin-derived breakdown product E-mail: [email protected] Received 16 December 2011; revised 7 May 2012; accepted 14 p-coumaric acid from a co-cultivated microalga May 2012; published online 21 June 2012 (Seyedsayamdost et al., 2011). Thus, the mutualistic P. gallaeciensis genomes from globally opposite locations S Thole et al 2230 relation between this bacterium and its host can Materials and methods switch to parasitism. In addition, other secondary metabolites, like acylated homoserine lactones Genome sequencing, assembly, finishing and (Bruhn et al., 2005; Berger et al., 2011), are produced annotation by Phaeobacter species and it was shown that The genomes of the P. gallaeciensis strains DSM 17395 and 2.10 (DSM 24588) were sequenced as P. gallaeciensis BS107 harbors a hybrid polyketide parts of the Microbial Genome Sequencing Project synthase/non-ribosomal peptide synthetase (NRPS) (http://camera.calit2.net/microgenome/). Gap clo- cluster (Martens et al., 2007). However, none of the sure and sequence editing were performed using above-mentioned traits is unique to Phaeobacter the Staden software package (Staden, 1996). For strains, hence, limiting the knowledge of features further details see Supplementary Material S1. The delineating P. gallaeciensis from other roseobacters. sequences have been deposited in GenBank under the The P. gallaeciensis strains DSM 17395 and 2.10 accession numbers CP002976, CP002977, CP002978, were isolated from geographically very distant CP002979 (strain DSM 17395) and CP002972, locations at the Atlantic coast of north western Spain (strain DSM 17395; scallop larvae hatchery; CP002973, CP002974, CP002975 (strain 2.10). Prediction of potential protein coding open read- Ruiz-Ponte et al., 1998) and Sydney, Australia ing frames (ORFs) was conducted using YACOP (strain 2.10; surface of the alga Ulva lactuca; Rao et al., 2005). Despite the great distance between (Tech and Merkl, 2003). ORF calling was verified manually and expert annotation was performed the isolation sites, the organisms are very closely with the ERGO software package (Overbeek et al., related and indistinguishable by their 16S rRNA 2003) (Supplementary Material S1). gene sequence. For more than 20 years, bacteria affiliated with the marine Roseobacter clade have been intensively Sequence analyses and comparative genomics studied because of their abundance in diverse The BiBag software tool—combining reciprocal marine habitats as well as their physiological and BLAST analyses and global sequence alignments— metabolic versatility. In addition, as part of the was applied to compare the genomes of the two Marine Microbiology Initiative (http://camera. P. gallaeciensis strains (DSM 17395 and 2.10), as calit2.net/microgenome/) and other sequencing pro- well as 35 other roseobacters (Supplementary jects, the complete genomes of 40 members of this Material S1). Whole-genome alignments were prominent bacterial cluster were sequenced performed with the MAUVE software (Darling (Brinkhoff et al., 2008). Comparative analyses based et al., 2004) and circular plots were generated with on the (mostly unfinished) genomes of these isolates DNAPlotter (Carver et al., 2009). Functional classes emphasized the heterogeneity of this bacterial clade were assigned to the ORFs according to the cluster of and demonstrated the difficulty to classify and orthologous groups classification (Tatusov et al., organize roseobacters in terms of ecological 1997). Prediction of horizontally acquired genes was or biogeochemical functions (Newton et al., 2010). performed using the programs IslandViewer and In contrast, comparative analyses encompassing COLOMBO (Waack et al., 2006; Langille and more closely related organisms have proven to be a Brinkman, 2009). Because different results were valuable approach to assess patterns of differentia- obtained with the two programs, predicted alien tion and adaptive strategies (Rocap et al., 2003; Pena genes and genomic islands (GEIs) were manually et al., 2010; Kalhoefer et al., 2011). Our study thus checked for elements commonly associated with focused on the genome comparison of two strains of GEIs like transposases, integrases, tRNAs and GC- the same species to gain insights into the genomic content deviations. The metabolic pathways were and phenotypic diversity below the species level reconstructed using the Pathway-tools software (Schloter et al., 2000). (Karp et al., 2002) from the Biocyc Database Here we report the complete genome sequences collection (Karp et al., 2005). The pathways were and comparative analysis of the manually annotated checked and curated manually, if required. genomes of the P. gallaeciensis strains DSM 17395 The recently published genome of P. gallaeciensis and 2.10. Differences between the genomes ANG1 (Collins and Nyholm, 2011) could not be were examined and Phaeobacter-specific coding included in the analysis of unique gene content as it sequences were compared with other Roseobacter is in draft stage (135 contigs). Furthermore, the 16S clade members. Additional genomic traits were rRNA gene of strain ANG1 is more similar to that of deduced from the genomes and tested in vitro. This Phaeobacter daeponensis strain TF-218 (99%) than to study compares, for the first time, two finished those of
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