Genome sequence of Phaeobacter daeponensis type strain (DSM 23529T), a facultatively anaerobic bacterium isolated from marine sediment, and emendation of Phaeobacter daeponensis
- Marco Dogs1,
- Hazuki Teshima2,
- Jörn Petersen3,
- Anne Fiebig3,
- Olga Chertkov2,
- Hajnalka Dalingault2,
- Amy Chen4,
- Amrita Pati5,
- Lynne A. Goodwin2, 5,
- Patrick Chain5,
- John C. Detter2, 5,
- Natalia Ivanova5,
- Alla Lapidus5,
- Manfred Rohde6,
- Sabine Gronow3,
- Nikos C. Kyrpides5,
- Tanja Woyke5,
- Meinhard Simon1,
- Markus Göker3Email author,
- Hans-Peter Klenk3 and
- Thorsten Brinkhoff1
© The Author(s) 2013
Published: 16 October 2013
TF-218T is the type strain of the species Phaeobacter daeponensis Yoon et al. 2007, a facultatively anaerobic Phaeobacter species isolated from tidal flats. Here we describe the draft genome sequence and annotation of this bacterium together with previously unreported aspects of its phenotype. We analyzed the genome for genes involved in secondary metabolite production and its anaerobic lifestyle, which have also been described for its closest relative Phaeobacter caeruleus. The 4,642,596 bp long genome of strain TF-218T contains 4,310 protein-coding genes and 78 RNA genes including four rRNA operons and consists of five replicons: one chromosome and four extrachromosomal elements with sizes of 276 kb, 174 kb, 117 kb and 90 kb. Genome analysis showed that TF-218T possesses all of the genes for indigoidine biosynthesis, and on specific media the strain showed a blue pigmentation. We also found genes for dissimilatory nitrate reduction, gene-transfer agents, NRPS/PKS genes and signaling systems homologous to the LuxR/I system.
KeywordsMarine microbiology e]facultative anaerobe e]indigoidine e]Rhodobacteraceae e]Roseobacter clade
The genus Phaeobacter currently is comprised of five species (P. daeponensis, P. gallaeciensis, P. inhibens, P. arcticus and P. caeruleus) and is a part of the marine Roseobacter clade within the Alphaproteobacteria [1–5]. The genus name was derived from the dark brownish pigmentation of the type species P. gallaeciensis (phaeos = dark, brown) . Strain TF-218T, however, was described as not pigmented. Strain TF-218T (= KCTC 12794T = JCM 13606T = DSM 23529T) is the type strain of the species Phaeobacter daeponensis . It was isolated from tidal flats at Daepo Beach (Yellow Sea), Korea, which led to the species name of P. daeponensis .
Secondary metabolite production is a well-known feature within the Roseobacter clade , especially within the Phaeobacter cluster, which shows high efficiency for secondary metabolite production . Examples include biosynthesis of the antibiotics tropdithietic acid (TDA) or indigoidine, quorum sensing by N-acyl homoserine lactones (AHLs), and presence of genes coding for nonribosomal peptide synthases (NRPS) and polyketide synthases (PKS) [6–11]. Furthermore, P. daeponensis was the first described facultatively anaerobic Phaeobacter species, which is capable of nitrate reduction .
Here we present the draft genome sequence and annotation of P. daeponensis TF-218T. We analyzed the genome for special features with a focus on secondary metabolite production. Novel aspects of the strain phenotype are also reported.
Classification and features
16S rRNA gene sequence analysis
Classification and general features of P. daeponensis TF-128T according to the MIGS recommendations .
Species Phaeobacter daeponensis
Type strain TF-218
L-malate, pyruvate, D-glucose, lycerol, leucine, serine, acetate, citrate and succinate
Tidal flat sediment
Daepo Beach (Yellow Sea), Korea
A representative genomic 16S rRNA gene sequence of P. daeponensis TF-218T was compared with the Greengenes database for determining the weighted relative frequencies of taxa and (truncated) keywords as previously described . The most frequently occurring genera were Ruegeria (31.6%), Phaeobacter (28.8%), Silicibacter (13.6%), Roseobacter (13.3%) and Nautella (3.6%) (713 hits in total). Regarding the five hits to sequences from the species, the average identity within HSPs was 99.9%, whereas the average coverage by HSPs was 19.0%. Regarding the 45 hits to sequences from other species of the genus, the average identity within HSPs was 97.8%, whereas the average coverage by HSPs was 18.9%. Among all other species, the one yielding the highest score was Roseobacter gallaeciensis (AY881240), which corresponded to an identity of 98.6% and an HSP coverage of 18.8%. (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 AF253467 (Greengenes short name ‘Key aromatic-ring-cleaving enzyme protocatechuate 34-dioxygenase ecologically important marine Roseobacter lineage d on Indulin seawater’), which showed an identity of 99.8% and an HSP coverage of 18.8%. The most frequently occurring keywords within the labels of all environmental samples which yielded hits were ‘microbi’ (2.8%), ‘marin’ (2.7%), ‘coral’ (2.4%), ‘diseas’ (1.8%) and ‘water’ (1.8%) (492 hits in total). The most frequently occurring keywords within the labels of those environmental samples which yielded hits of a higher score than the highest scoring species were ‘marin’ (17.4%), ‘sediment’ (8.5%), ‘aromatic-ring-cleav, ecolog, enzym, import, indulin, kei, lineag, protocatechu, roseobact, seawat’ (4.4%), ‘coco, island, near, site’ (4.3%) and ‘redox-stratifi, reef, sandi’ (4.3%) (4 hits in total).
Morphology and physiology
In addition to the findings reported in , we observed that strain DSM 23529T is able to form blue colonies on YTSS medium, as described for the closely related strain Y4I . This is probably due to the presence of genes for indigoidine biosynthesis in the genome (see below).
The utilization of carbon compounds by P. daeponensis was also determined for this study using Generation-III microplates in an OmniLog phenotyping device (BIOLOG Inc., Hayward, CA, USA). The microplates were inoculated at 28°C with a cell suspension at a cell density of 95–96% turbidity and dye IF-A. Further additives were vitamins, micronutrients and sea-salt solutions. The exported measurement data were further analyzed with the opm package for R [30,31], using its functionality for statistically estimating parameters from the respiration curves and translating them into negative, ambiguous, and positive reactions. The strain was studied in two independent biological replicates, and reactions with a different behavior between the two repetitions were regarded as ambiguous.
For P. daeponensis strain DSM 23529T, positive reactions were observed for pH 6, 1% NaCl, 4% NaCl, 8% NaCl, D-glucose, inosine, glycerol, D-aspartic acid, L-aspartic acid, L-glutamic acid, L-histidine, L-pyroglutamic acid, L-lactic acid, α-keto-glutaric acid, D-malic acid, L-malic acid, lithium chloride, α-hydroxy-butyric acid, β-hydroxy-butyric acid, α-keto-butyric acid, acetoacetic acid, propionic acid, acetic acid and sodium bromated. In contrast, negative reactions were observed for dextrin, D-maltose, D-trehalose, D-cellobiose, β-gentiobiose, sucrose, D-turanose, stachyose, pH 5, D-raffinose, α-D-lactose, D-melibiose, β-methyl-D-galactoside, D-salicin, N-acetyl-D-glucosamine, N-acetyl-β-D-mannosamine, N-acetyl-D-galactosamine, N-acetyl-neuraminic acid, D-mannose, D-fructose, D-galactose, 3-O-methyl-D-glucose, D-fucose, L-fucose, L-rhamnose, fusidic acid, D-serine, D-sorbitol, D-mannitol, D-arabitol, myo-inositol, D-glucose-6-phosphate, D-fructose-6-phosphate, D-serine, troleandomycin, rifamycin SV, minocycline, gelatin, L-alanine, L-arginine, L-serine, lincomycin, guanidine hydrochloride, niaproof 4, pectin, D-galacturonic acid, L-galactonic acid-γ-lactone, D-glucuronic acid, glucuronamide, mucic acid, quinic acid, D-saccharic acid, vancomycin, tetrazolium violet, methyl pyruvate, D-lactic acid methyl ester, citric acid, bromo-succinic acid, tween 40, aztreonam and butyric acid. Ambiguous results between the replicates were found for 1% sodium lactate, glycyl-L-proline, D-gluconic acid, tetrazolium blue, p-hydroxy-phenylacetic acid, nalidixic acid, potassium tellurite, γ-amino-n-butyric acid and sodium formate.
The principal fatty-acid profile of strain TF-128T consisted of major amounts of unsaturated fatty acid C18:1ω7c (57.7%) and 11-methyl C18:1ω7c (16.6%) in addition to straight-chain fatty acids (12.8%) and hydroxyl fatty acids (9.9%). Apart from the differences in the proportions, the fatty acid profile is similar to those of the type strains of P. gallaeciensis, P. inhibens and P. caeruleus. The major polar lipids of strain TF-218T are phosphatidylcholine, phosphatidylglycerol, phosphatidylethanolamine, two unidentified lipids and an aminolipid .
Genome sequencing and annotation
Genome project history
Genome sequencing project information
Two Illumina paired-end libraries (221 bp and 9 kb insert size)
Illumina GAii, PacBio
1,345 × Illumina
Allpaths version 38445, Velvet 1.1.05, phrap version SPS - 4.24
Gene calling method
Prodigal 1.4, GenePRIMP
GenBank Date of Release
September 30, 2013
NCBI project ID
Source material identifier
Tree of Life, carbon cycle, sulfur cycle, environmental
Growth conditions and DNA isolation
A culture of DSM 23529T was grown aerobically in DSMZ medium 514  at 37°C. Genomic DNA was isolated using a Jetflex Genomic DNA Purification Kit (GENOMED 600100) following the standard protocol provided by the manufacturer, but modified by an incubation time of 40 min, the incubation on ice over night on a shaker, the use of an additional 25 µl proteinase K, and the addition of 200 µl protein precipitation buffer. DNA is available from DSMZ through the DNA Bank Network .
Genome sequencing and assembly
The draft genome sequence was generated using Illumina sequencing technology. For this genome, we constructed and sequenced an Illumina short-insert paired-end library with an average insert size of 221 bp, which generated 21,978,034 reads, and an Illumina long-insert paired-end library with an average insert size of 9,327 +/− 1,586 bp, which generated 19,261,756 reads totaling 6,186 Mbp of Illumina data. All general aspects of library construction and sequencing performed can be found at the JGI web site . The initial draft assembly contained 15 contigs in 10 scaffold(s). The initial draft data was assembled with Allpaths  and the consensus was computationally shredded into 10 kbp overlapping fake reads (shreds). The Illumina draft data was also assembled with Velvet , and the consensus sequences were computationally shredded into 1.5 kbp overlapping fake reads (shreds). The Illumina draft data was assembled again with Velvet using the shreds from the first Velvet assembly to guide the next assembly. The consensus from the second Velvet assembly was shredded into 1.5 kbp overlapping fake reads. The fake reads from the Allpaths assembly, both Velvet assemblies, and a subset of the Illumina CLIP paired-end reads were assembled using parallel phrap (High Performance Software, LLC) . Possible mis-assemblies were corrected with manual editing in Consed . Gap closure was accomplished using repeat resolution software (Wei Gu, unpublished), and sequencing of bridging PCR fragments with PacBio (Cliff Han, unpublished) technologies. A total of 2 PCR PacBio consensus sequences were completed to close gaps and to raise the quality of the final sequence. The final assembly is based on 6,186 Mbp of Illumina draft data, which provides an average 1,345 × coverage of the genome.
Genes were identified using Prodigal  as part of the DOE-JGI genome annotation pipeline , followed by a round of manual curation using the JGI GenePRIMP 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. Additional gene prediction analysis and functional annotation was performed within the Integrated Microbial Genomes - Expert Review (IMG-ER) platform .
% 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 biogenesis
Intracellular trafficking and 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
General genomic features of the chromosome and extrachromosomal replicons
RepC-8 DnaA-like I
Integrated Microbial Genome (IMG) locus tags of P. daeponensis DSM 23529T†
Type IV Secretion
RepC-8 DnaA-like I1
The 174 kb plasmid pDaep_B174 contains two RepABC-9 type replication modules (Figure 3a). Both of them harbor a specific perfect palindrome sequence (5′-ATCCGCG’ [RepABC-9a]; 5′-TTGCACG’ [RepABC-9b]) that may represent the functional cis-acting anchor for plasmid partitioning . This composite replicon may have either originated from a plasmid fusion or from a horizontal recombination. The latter explanation is supported by two site-specific XerC recombinase genes (Daep_04383, Daep_04398) that are located head-to-head adjacent to the two replicases repC9-a and repC9-b.
This plasmid contains many transposases and putative phage-derived components including a DNA-primase (Daep_04238) and an RNA-directed DNA polymerase (Daep_04390). The general operon structure of this plasmid seems to be scrambled by transposition or recombination events, as illustrated by the type-IV secretion system. pDaep_B174 contains two copies of the characteristic virD-operon comprising the relaxase VirD2 and the coupling protein VirD4 (Table 6). Moreover, the operon contains a complete, as well as a partial, virB gene cluster for the transmembrane channel . The first four genes in the partial cluster are missing, and the truncated virB4 pseudogene (Daep_04339) is flanked by a transposase. But plasmid stability is probably ensured by a PSK system (Table 6).
Finally, the most conspicuous finding on this plasmid is the presence of a complete or nearly complete phenylacetate catabolon (Daep_04356 to Daep_04367), containing paa genes for the following proteins: PaaJ, PaaA, PaaB, PaaC, PaaD, PaaE, PaaZ, PaaY, PaaK, PaaF. The extrachromosomal localization of this catabolon has previously been shown for Silicibacter sp. TM1040, Jannaschia sp. CCS1 and Dinoroseobacter shibae DSM 16493T [60,61], which also belong to the Roseobacter clade.
The 117 kb RepA-I type replicon pDaep_C117 contains a LuxR-type two-component transcriptional regulator (Daep_03918) and a complete rhamnose operon  and is dominated by genes that are required for polysaccharide biosynthesis.
P. daeponensis was described as a facultatively anaerobic bacterium that uses nitrate as electron acceptor . We found genes involved in nitrogen metabolism scattered over the chromosome, involved in the pathways of the assimilatory and the dissimilatory nitrate reduction to ammonia (Daep_03263, _03264 and _03265; Daep_03099, _03100, _03263 and _03264) [63–65]. Furthermore, we detected all genes necessary for the dissimilatory nitrate reduction to nitrogen, including a cluster for the nitrate reductase (Daep_03099, _03100), the nitrite reductase (Daep_02798), the nitric oxide reductase (Daep_00020, _00021) and the nitrous oxide reductase (Daep_03697) .
P. daeponensis encodes a gene transfer agent (GTA), a virus-like particle that mediates the transfer of genomic DNA between prokaryotes . The GTA cluster has a length of ∼17 kb (Daep_01107 – Daep_01126) and has a high homology to GTAs of other Phaeobacter species, e.g. the P. inhibens strains DSM 17395, 2.10 and T5T [28,67]. Screenings for genes coding for phage-related proteins gave hits for a phage integrase (Daep_00002, _00008 and _01212) and a phage-related gene (Daep_02906), but no complete prophage genomes were detected.
Further genome analysis of P. daeponensis also revealed genes related to secondary metabolism. We found genes coding for a non-ribosomal peptide synthase (Daep_00048, _01832, _01834, _01837, _02357 and _03495) and a polyketide synthase (Daep_00050). Two homologs to the luxRI quorum sensing system  were also determined (Daep_01951 and _01952; Daep_03917 and _03918). Genes coding for biosynthesis of tropodithietic acid and siderophores, as described for the P. inhibens strains DSM 17395, 2.10 and T5T [66,67], were not detected.
P. daeponensis was described as a yellowish white colony forming bacterium on Marine Agar (MA; Difco) . Here we could show that P. daeponensis forms blue-framed colonies when grown on YTSS broth . In the genome we found genes probably encoding indigoidine biosynthesis . The respective operon (Daep_03493, _03494, _03495, _03496, _03497 and _03498) is similar to the operon recently described for the closely related strain Phaeobacter sp. Y4I . The luxRI genes and the gene Daep_01773 show homology to the quorum-sensing systems and the clpA gene of Phaeobacter sp. strain Y4I, respectively. Strain Y4I lost its pigmentation by transposon insertions in each of the two luxRI quorum-sensing systems, revealing that pigment production in strain Y4I is regulated via quorum sensing . Transposon insertion in gene clpA of strain Y4I, coding for a universal regulatory chaperone protein ClpA, which degrades abnormal and regulatory proteins, led to a higher pigment production. The presence of the biosynthesis operon and the regulatory systems indicates that P. daeponensis is also able to produce indigoidine in a similar way as strain Y4I.
Digital DDH similarities between P. daeponensis DSM 23529T and the other Phaeobacter and Leisingera species†
Reference strain (type strain unless indicated)
P. arcticus (AXBF00000000)
P. caeruleus (AXBI00000000)
P. inhibens (AXBB00000000)
P. gallaeciensis (AOQA01000000)
P. inhibens DSM 17395 (CP002976, CP002977, CP002978, CP002979))
P. inhibens 2.10 (NC_018286)
L. aquimarina (AXBE00000000)
L. methylohalidivorans (CP006773, CP006774, CP006775)
L. nanhaiensis (AXBG00000000)
Even though discrepancies between the current classification of the group and the genomic data apparently exist, it is also obvious that P. caeruleus, which forms blue colonies , is the closest known relative of P. daeponensis (Table 7). For this reason, the formation of blue colonies by P. daeponensis DSM 23529T on YTSS medium  observed in this study, confirmed by the presence of genes for indigoidine biosynthesis in the genome, is probably of taxonomic relevance. This warrants an update of the taxonomic description of P. daeponensis.
Emended description of the species Phaeobacter daeponensis Yoon et al. 2007
The description of the species Phaeobacter daeponensis is the one given by Yoon et al. 2007 , with the following modification. Forms blue colonies when cultivated on YTSS medium.
The authors would like to gratefully acknowledge the assistance of Iljana Schröder for growing P. daeponensis cultures and Evelyne-Marie Brambilla for DNA extraction and quality control (both at DSMZ). The work conducted by the U.S. Department of Energy Joint Genome Institute was supported by the Office of Science of the U.S. Department of Energy under contract No. DE-AC02-05CH11231; the work conducted by members of the Roseobacter consortium was supported by the German Research Foundation (DFG) Transregio-SFB 51. We also thank the European Commission which supported phenotyping via the Microme project 222886 within the Framework 7 program.
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