Complete genome sequence of the Phaeobacter gallaeciensis type strain CIP 105210T (= DSM 26640T = BS107T)
© The Author(s) 2014
Published: 15 June 2014
Phaeobacter gallaeciensis CIP 105210T (= DSM 26640T = BS107T) is the type strain of the species Phaeobacter gallaeciensis. The genus Phaeobacter belongs to the marine Roseobacter group (Rhodobacteraceae, Alphaproteobacteria). Phaeobacter species are effective colonizers of marine surfaces, including frequent associations with eukaryotes. Strain BS107T was isolated from a rearing of the scallop Pecten maximus. Here we describe the features of this organism, together with the complete genome sequence, comprising eight circular replicons with a total of 4,448 genes. In addition to a high number of extrachromosomal replicons, the genome contains six genomic island and three putative prophage regions, as well as a hybrid between a plasmid and a circular phage. Phylogenomic analyses confirm previous results, which indicated that the originally reported P. gallaeciensis type-strain deposit DSM 17395 belongs to P. inhibens and that CIP 105210T (= DSM 26640T) is the sole genome-sequenced representative of P. gallaeciensis.
KeywordsAlphaproteobacteria Roseobacter group Plasmid wealth Replication systems Sister species Phaeobacter inhibens
Strain CIP 105210T (= BS107T = DSM 26640T) is the type strain of Phaeobacter gallaeciensis, the type species of Phaeobacter, a genus of marine species of Rhodobacteraceae (Rhodobacterales, Alphaproteobacteria). BS107T was isolated from the scallop Pecten maximus and was initially described as the type strain of Roseobacter gallaeciensis . After comprehensive reclassifications of Rhodobacteraceae genera, BS107T became the type strain of the species P. gallaeciensis , currently comprising the species P. gallaeciensis, P. inhibens, P. caeruleus, P. daeponensis, P. leonis and P. arcticus. A recent study  revealed the non-identity of the reported identical deposits DSM 17395 and CIP 105210T and confirmed that the strain CIP 105210T represents the original P. gallaeciensis isolate BS107T, which is now deposited in the DSMZ open collection as DSM 26640T. In contrast, strain DSM 17395 was reclassified as a representative of the sister species P. inhibens. Analysis of their similar, but distinct metabolic capacities allowed for a discrimination between the two strains, which were originally reported to represent the same type strain . Thus, in the absence of sequenced genomes, the assignment to species was essentially based on deviating plasmid profiles and molecular analyses (16S rDNA, ITS, DNA-DNA hybridization), which showed convergent results.
The genus Phaeobacer comprises effective surface colonizers. Comparative analyses of strains DSM 17395 and DSM 24588 (= 2.10) revealed a high level of adaptation to life on surfaces . The production of the characteristic antibiotic tropodithietic acid (TDA) correlates with the formation of a brown pigment that is eponymous for Phaeobacter . Current scientific interest in Phaeobacter is based on the role of its strains as probiotic agents in fish aquaculture  and as agents of bleaching diseases in marine red algae , as well as on their potential regulatory activity during phytoplankton blooms  via so-called roseobacticides . Here we present the complete genome sequence of P. gallaeciensis CIP 105210T, together with a summary classification and a set of features, including insights into genome architecture, genomic islands and phages.
Classification and features
16S rRNA gene analysis
A representative genomic 16S rDNA gene sequence of P. gallaeciensis CIP 105210T was compared with the Greengenes database for determining the weighted relative frequencies of taxa and (truncated) keywords as previously described , to infer the taxonomic and environmental affiliation of the strain. The most frequently occurring genera were Ruegeria (30.2%), Phaeobacter (29.4%), Roseobacter (13.9%), Silicibacter (13.7%) and Nautella (3.6%) (698 hits in total). Regarding the 30 hits to sequences from members of the species, the average identity within HSPs (high-scoring segment pairs) was 99.6%, whereas the average coverage by HSPs was 18.7%. Regarding the 20 hits to sequences from other members of the genus, the average identity within HSPs was 98.0%, whereas the average coverage by HSPs was 18.7%. Among all other species, the one yielding the highest score was P. inhibens (AY177712), which corresponded to a 16S rDNA gene identity of 99.5% and an HSP coverage of 18.6%. (Note that the Greengenes database uses the INSDC (= EMBL/NCBI/DDBJ) annotation, which is not an authoritative source for nomenclature or classification.) The highest-scoring environmental sequence was AJ296158 (Greengenes short name ‘Spain:Galicia isolate str. PP-154’), which showed an identity of 99.8% and an HSP coverage of 18.7%. The most frequently occurring keywords within the labels of all environmental samples which yielded hits were ‘microbi’ (2.8%), ‘marin’ (2.5%), ‘coral’ (2.4%), ‘sediment’ (2.0%) and ‘biofilm’ (1.9%) (509 hits in total). Environmental samples which yielded hits of a higher score than the highest scoring species were not found.
Morphology and physiology
BS107T is able to use the following substrates as sole carbon source and energy source: D-mannose, D-galactose, D-fructose, D-glucose, D-xylose, melibiose, trehalose, maltose, cellobiose, sucrose, meso-erythritol, D-mannitol, glycerol, D-sorbitol, meso-inositol, succinate, propionate, butyrate, γ-aminobutyrate, DL-hydroxybutyrate, 2-ketoglutarate, pyruvate, fumarate, glycine, L-a-alanine, p-alanine, L-glutamate, L-lysine, L-arginine, L-ornithine, L-proline, acetate and leucine. Bacteriochlorophyll a was not detected .
Species Phaeobacter gallaeciensis
Subspecific genetic lineage (strain) BS107T
Reference for biomaterial
Ruiz-Ponte et al. 1998
motile, via polar flagella
0.1–2.0 M NaC1
Relationship to oxygen
complex substrates, butyrate, DL-hydroxybutyrate, D-xylose
seawater, Pecten maximus
4.0–10.0, optimum 7.0
free living, facultative symbiont
Health status of host
seawater of larval cultures of the scallop Pecten maximus
A Coruna, Galicia, Spain
Time of sample collection
about sea level
The chemical composition of strain BS107T confirmed ubiquinones as the sole respiratory lipoquinones and revealed Q10 as predominant. Polar lipids consisted of an unidentified phospholipid, two uncharacterized lipids, aminolipids, phosphatidylenthanolamine, phosphatidylglycerole and phosphatidylcholine .
The major fatty acids are the monounsaturated acids C18:1 ω7c (76.1%), and 11-methyl C18:1 ω7c (6.1%), followed by hydroxy fatty acid C16:0 2-OH (5.1%) as well as C16:0 (4.0%), C14:1 (3.1%), C18:0 (2.6%), C10:0 3-OH (2.2%) and C18:1 ω9c (0.9%) .
Genome sequencing and annotation
Growth conditions and DNA extraction
A culture of CIP 105210T was grown aerobically in 100 ml of DSMZ medium 514  on a shaker at 28°C. Genomic DNA was isolated using the Qiagen Genomic DNA Kit, following the standard protocol for Bacteria 500G provided by the manufacturer. The extracted DNA had a concentration of 200 ng/µl. The quality of the DNA was checked with the NanoDrop.
Genome sequencing and assembly
Genome sequencing project information
One draft assembly of standard shotgun library, one 3 kbp paired-end library
Roche/454 GS FLX Titanium
Newbler assembler version 2.6 (Software Release: 2.6 (20110517_1502)
Gene calling method
GenBank Date of Release
NCBI project ID
Source material identifier
Tree of Life, carbon cycle, scallop rearing, plasmid
Genes were identified using Prodigal  as part of the Integrated Microbial Genomes Expert Review (IMG/ER) annotation pipeline . The predicted CDSs were translated and used to search the National Center for Biotechnology Information (NCBI) nonredundant database, UniProt, TIGR-Fam, Pfam, PRIAM, KEGG, COG, and InterPro databases.
% of Total
Genome size (bp)
DNA coding region (bp)
DNA G+C content (bp)
Number of replicons
Genes with function prediction
Genes in paralog clusters
Genes assigned to COGs
Genes assigned Pfam domains
Genes with signal peptides
Genes with transmembrane helices
Number of genes associated with the general COG functional categories
Translation, ribosomal structure and biogenesis
RNA processing and modification
Replication, recombination and repair
Chromatin structure and dynamics
Cell cycle control, cell division, chromosome partitioning
Signal transduction mechanisms
Cell wall/membrane/envelope biogenesis
Intracellular trafficking, secretion, and vesicular transport
Posttranslational modification, protein turnover, chaperones
Energy production and conversion
Carbohydrate transport and metabolism
Amino acid transport and metabolism
Nucleotide transport and metabolism
Coenzyme transport and metabolism
Lipid transport and metabolism
Inorganic ion transport and metabolism
Secondary metabolites biosynthesis, transport and catabolism
General function prediction only
Not in COGs
Insights into the genome
A search for specific genes in the genome of P. gallaeciensis CIP 105210T compared to the P. inhibens strains DSM 24588 (= 2.10), DSM 16374T (= T5T) and DSM 17395, based on an e-value of 1e-5 and a minimum identity of 30%, resulted in a total number of 551 specific genes. 296 (54%) of these genes were located on the chromosome and 255 (46%) on extrachromosomal replicons. In comparison with the other completely sequenced bacterial strains of the genus Phaeobacter, 8% of the chromosomal and 35% of the extrachromosomal P. gallaeciensis CIP 105210T genes were unique, thus reflecting the considerable contribution of extrachromosomal elements to unique gene content.
The observed distribution may be influenced by the presence of two chromosome-encoded bacterial MobC mobilization proteins (Gal_00154, Gal_01073). MobC, which is missing in all three completely sequenced P. inhibens strains, is part of the relaxosome at the origin of transfer and increases the frequency of plasmid mobilization and therefore conjugal transfer of plasmids , which is also in agreement with the comparably large number of seven extrachromosomal replicons present in CIP 105210T.
The probable function of some of the unique genes is explained below. Genes Gal_01405 and Gal_01407 constitute methane monooxygenases (EC 126.96.36.199) facilitating the degradation of aromatic compounds and phenols . Gal_01397, a monoamine oxidase could provide an additional source of ammonium .
Unique genes are also provided by phage-like elements. In CIP 105210T these so-called “morons” (because they add “more on” the genome ) comprise, e.g., an ABC-2 family drug transporter (Gal_01752) , and a negative regulator of beta-lactamase expression (Gal_02239).
Six genomic islands could be identified on the chromosome with the web-based island-viewer system . Island-viewer combines the methods IslandPick , which uses a comparative genomics approach, SIGI-HMM , which relies upon deviating codon usage signatures, and IslandPath-DIMOB , which identifies genomic islands based on deviating GC content, dinucleotide bias in gene clusters and the presence of island specific genes like mobility genes and tRNAs.
Island-I ranging from position 155,977 to 177,667 (21,690 bp) contains a tRNA gene (Phe GAA, Gal_00137) next to a site-specific recombinase XerD (Gal_00138) and the bacterial mobilization protein (MobC, Gal_00154; see above). Furthermore, it contains a transcriptional regulator of the LysR family (Gal_00160) and an adjacent ABC-type transport system for glycine/proline/betaine. Island-II (422,441 to 434,165; 11,725 bp) mainly consists of hypothetical proteins, but it also contains a large type II restriction enzyme (905aa, Gal_00442) and another site specific XerD recombinase (Gal_00444) next to a tRNA for proline (Gal_00445). Island-III (1,085,143 to 1,096,105; 10,962 bp) contains three XerD recombinases in row (Gal_01065 to Gal_01067, a MobC protein (Gal_01073) and the typical VirD2 relaxase (Gal_01074) as well as the VirD4 coupling protein (Gal_01075) of type IV secretion systems  indicating a plasmid-derived origin of this island. Island-IV (1,626,663 to 1,641,677; 15,014 bp) contains an ABC-type cobalt transport system and a XerC recombinase (Gal_01616). Island-V (2,821,359 to 2,848,860; 27,501 bp) consists mainly of regulated TRAP C4-dicarboxylate and ABC-type dipeptide/oligopeptide/nickel transport proteins and also the epsilon subunit of DNA polymerase III (Gal_02817). Island-VI (3,328,870 to 3,344,910; 16,040 bp) lies adjacent to a ribosomal rRNA-operon and contains an ABC-type amino acid/amide transport system and an E1 component of the pyruvate dehydrogenase complex (Gal_03286, E.C.: 188.8.131.52).
Prophage regions in the chromosome of P. gallaeciensis CIP 105210Ta
Gene transfer agent (GTA)
integrase, region invertase, helicase
Portal protein, head maturation protease
Integrase, peptidoglycan hydrolase
General genomic features of the chromosome and extrachromosomal elements from P. gallaeciensis strain CIP 105210Ta
Integrated Microbial Genome (IMG) locus tags of P. gallaeciensis CIP 105210T genes for the initiation of replication, toxin/antitoxin modules and type IV secretion systems (T4SS) required for conjugation.
Type IV Secretion
Genome sequencing of P. inhibens DSM 16374T (T5T) revealed the presence of the complete dissimilatory nitrate reduction pathway and anaerobic growth on nitrite has been validated experimentally . The genes of the pathway are located on three different replicons, i.e. the chromosome, the DnaA-like I type plasmid pInhi_A227 and the RepABC-8 type plasmid pInhi_B88. The genome of the sister species P. gallaeciensis CIP 105210T exhibits a conspicuous synteny for the chromosome and three extrachromosomal replicons (DnaA-like I (pGal_A255, pInhi_A227), RepB-I (pGal_D78, pInhi_C78), RepA-I (pGal_F69, pInhi_D69)). However, the RepABC-8 type plasmid including the crucial nitrous oxide reductase (EC 184.108.40.206) is missing in P. gallaeciensis CIP 105210T, and this strain is accordingly unable to grow anaerobically.
The phylogenetic analysis of 16S rRNA gene type-strain sequences places P. gallaeciensis together with both P. caeruleus and P. daeponensis, whereas P. inhibens forms a cluster with P. leonis and P. arcticus. Both clusters are set apart from each other, but the 16S rRNA gene tree is unresolved and does not allow one to infer the evolutionary interrelationships in this group. Previous results  showed that the reported P. gallaeciensis type-strain deposit DSM 17395 belongs to P. inhibens and that CIP 105210T (= DSM 26640T) is the authentic type strain of P. gallaeciensis. Moreover, the genome sequenced strain ANG1 has been referred to as P. gallaeciensis based on 16S rRNA analyses , but our recent study revealed a well-supported association with P. caeruleus and P. daeponensis . The relationships between these Phaeobacter strains have not been coroborated using genome sequences. Thus, we used the Genome-to-Genome Distance Calculator (GGDC)  to investigate the affiliation of strain ANG1 and the genomic similarities between P. inhibens and P. gallaeciensis strains from available genome sequences and conducted phylogenomic analyses to address the relationship between P. gallaeciensis and P. inhibens.
DDH similarities with standard deviations between P. gallaeciensis CIP 105210T, P. inhibens DSM 16374T (T5T) and other Phaeobacter strains calculated in silico with the GGDC server version 2.0 . The numbers in parentheses are IMG Taxon IDs identifying the genome sequence.
Formula reference species
identities/HSP length [%] P. gallaeciensis DSM 26640T (= CIP 105210T = BS107T)
identities/HSP length [%] P. inhibens DSM 16374T (T5T)
P. inhibens DSM 24588 (2.10) (2501651220)
38.00% ± 2.49
79.50% ± 2.80
P. inhibens DSM 17395 (2510065029)
38.40% ± 2.50
78.70% ± 2.83
P. gallaeciensis ANG 1 (2526164696)
21.40% ± 2.34
21.10% ± 2.33
P. inhibens DSM 16374T (T5T) (2516653078)
38.20% ± 2.50
P. gallaeciensis DSM 26640T (= CIP 105210T) (2545555837)
38.20% ± 2.50
With the exception of P. gallaeciensis ANG 1, which neither belongs to P. gallaeciensis nor P. inhibens based on DDH values, the analysis supports the current classification. P. inhibens with the type strain DSM 16374T (T5T) includes the strains DSM 17395 and DSM 24588 (2.10), whereas the strain P. gallaeciensis CIP 105210T (= DSM 26640T) is the sole representative of P. gallaeciensis analyzed in the current study.
For the phylogenomic analysis, protein sequences from the available Phaeobacter genomes were retrieved from the IMG website (P. arcticus DSM 23566T; ID 2516653081; P. caeruleus DSM 24564T (13T), ID 2512047087; P. daeponensis DSM 23529T (TF-218T), ID 2516493020; P. inhibens DSM 16374T (T5T), ID 2516653078) or from NCBI (P. inhibens DSM 24588 (2.10), CP002972 – CP002975; P. sp. ANG1, AFCF00000000; P. gallaeciensis CIP 105210T (= DSM 26640T), AOQA00000000; P. inhibens DSM 17395, CP002976 – CP002979; P. sp. Y4I, ABXF00000000).
These sequences were investigated using the DSMZ phylogenomics pipeline as previously described [67–70] using NCBI BLAST , TribeMCL , OrthoMCL , MUSCLE , RASCAL , GBLOCKS  and MARE  to generate gene- and ortholog-content matrices as well as concatenated alignments of distinct selections of genes.
Thus, the analyses supported the earlier conclusion  that DSM 17395 belongs to P. inhibens. The analyses also confirmed that P. “gallaeciensis” ANG1 belongs neither to P. gallaeciensis nor to P. inhibens and might therefore represent a novel, not yet named seventh species in the genus Phaeobacter. Further, the analysis confirms P. gallaeciensis CIP 105210T (= DSM 26640T) as the sole representative of the species Phaeobacter gallaeciensis.
The authors gratefully acknowledge the assistance of Victoria Michael for growing P. gallaeciensis cultures and DNA extraction and quality control. The work conducted by members of the Roseobacter consortium was supported by the German Research Foundation (DFG) Transregio-SFB 51.
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