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Journal of Bacteriology logoLink to Journal of Bacteriology
. 2010 Sep;192(18):4796–4797. doi: 10.1128/JB.00733-10

Complete Genome Sequence of Croceibacter atlanticus HTCC2559T

Hyun-Myung Oh 1, Ilnam Kang 1, Steve Ferriera 2, Stephen J Giovannoni 3, Jang-Cheon Cho 1,*
PMCID: PMC2937408  PMID: 20639333

Abstract

Here we announce the complete genome sequence of Croceibacter atlanticus HTCC2559T, which was isolated by high-throughput dilution-to-extinction culturing from the Bermuda Atlantic Time Series station in the Western Sargasso Sea. Strain HTCC2559T contained genes for carotenoid biosynthesis, flavonoid biosynthesis, and several macromolecule-degrading enzymes. The genome confirmed physiological observations of cultivated Croceibacter atlanticus strain HTCC2559T, which identified it as an obligate chemoheterotroph.


The phylum Bacteroidetes comprises 6 to ∼30% of total bacterial communities in the ocean by fluorescence in situ hybridization (8-10). Most marine Bacteroidetes are in the family Flavobacteriaceae, most of which are aerobic respiratory heterotrophs that form a well-defined clade by 16S rRNA phylogenetic analyses (4). The members of this family are well known for degrading macromolecules, including chitin, DNA, cellulose, starch, and pectin (17), suggesting their environmental roles as detritus decomposers in the ocean (6). Marine Polaribacter and Dokdonia species in the Flavobacteriaceae have also shown to have photoheterotrophic metabolism mediated by proteorhodopsins (11, 12).

Several strains of the family Flavobacteriaceae were isolated from the Sargasso Sea and Oregon coast, using high-throughput culturing approaches (7). Croceibacter atlanticus HTCC2559T was cultivated from seawater collected at a depth of 250 m from the Sargasso Sea and was identified as a new genus in the family Flavobacteriaceae based on its 16S rRNA gene sequence similarities (6). Strain HTCC2559T met the minimal standards for genera of the family Flavobacteriaceae (3) on the basis of phenotypic characteristics (6).

Here we report the complete genome sequence of Croceibacter atlanticus HTCC2559T. The genome sequencing was initiated by the J. Craig Venter Institute as a part of the Moore Foundation Microbial Genome Sequencing Project and completed in the current announcement. Gaps among contigs were closed by Genotech Co., Ltd. (Daejeon, Korea), using direct sequencing of combinatorial PCR products (16). The HTCC2559T genome was analyzed with a genome annotation system based on GenDB (14) at Oregon State University and with the NCBI Prokaryotic Genomes Automatic Annotation Pipeline (15, 16).

The HTCC2559T genome is 2,952,962 bp long, with 33.9 mol% G+C content, and there was no evidence of plasmids. The number of protein-coding genes was 2,715; there were two copies of the 16S-23S-5S rRNA operon and 36 tRNA genes. The HTCC2559T genome contained genes for a complete tricarboxylic acid cycle, glycolysis, and a pentose phosphate pathway. The genome also contained sets of genes for metabolic enzymes involved in carotenoid biosynthesis and also a serine/glycine hydroxymethyltransferase, which is often associated with the assimilatory serine cycle (13). The potential for HTCC2559T to use bacterial type III polyketide synthase (PKS) needs to be confirmed because this organism had a naringenin-chalcone synthase (CHS) or chalcone synthase (EC 2.3.1.74), a key enzyme in flavonoid biosynthesis. CHS initiates the addition of three molecules of malonyl coenzyme A (malonyl-CoA) to a starter CoA ester (e.g., 4-coumaroyl-CoA) (1) and takes part in a few bacterial type III polyketide synthase systems (1, 2, 5, 18).

The complete genome sequence confirmed that strain HTCC2559T is an obligate chemoheterotroph because no genes for phototrophy were found. As expected from physiological characteristics (6), the HTCC2559T genome contained a set of genes coding for enzymes required to degrade high-molecular-weight compounds, including peptidases, metallo-/serine proteases, pectinase, alginate lyases, and α-amylase.

Nucleotide sequence accession number.

The complete genome sequence of HTCC2559 was deposited under GenBank accession no. CP002046. The GenDB-generated data were also processed to be accessed at the Marine Microbial Genomics site at Oregon State University (http://bioinfo.cgrb.oregonstate.edu/microbes/).

Acknowledgments

The initial phase of sequencing, assembly, and annotation efforts were carried out at the OSU High Throughput Culturing Laboratory, with support from a Gordon and Betty Moore Foundation investigator award and the Gordon and Betty Moore Foundation Marine Microbial Sequencing Project (www.moore.org/marinemicro). Completion of the genome sequence and data interpretation were supported by the 21C Frontier Program of Microbial Genomics and Applications, funded by the MEST, Republic of Korea (to J.-C.C.); and the Basic Science Research Program, through the National Research Foundation of Korea (NRF grant no. 2009-0069493 to H.-M.O.).

Special thanks are given to Sun Ho Cha and Hyun Jung Lee at Genotech for technical support.

Footnotes

Published ahead of print on 16 July 2010.

REFERENCES

  • 1.Austin, M. B., and J. P. Noel. 2003. The chalcone synthase superfamily of type III polyketide synthases. Nat. Prod. Rep. 20:79-110. [DOI] [PubMed] [Google Scholar]
  • 2.Bauer, M., M. Kube, H. Teeling, M. Richter, T. Lombardot, E. Allers, C. A. Würdemann, C. Quast, H. Kuhl, F. Knaust, D. Woebkin, K. Bischof, M. Mussmann, J. V. Choudhuri, F. Meyer, R. Reinhardt, R. I. Amann, and F. O. Glöckner. 2006. Whole genome analysis of the marine BacteroidetesGramella forsetii’ reveals adaptations to degradation of polymeric organic matter. Environ. Microbiol. 8:2201-2213. [DOI] [PubMed] [Google Scholar]
  • 3.Bernardet, J. F., Y. Nakagawa, and B. Holmes. 2002. Proposed minimal standards for describing new taxa of the family Flavobacteriaceae and emended description of the family. Int. J. Syst. Evol. Microbiol. 52:1049-1070. [DOI] [PubMed] [Google Scholar]
  • 4.Bowman, J. P. 2006. The marine clade of the family Flavobacteriaceae: the genera Aequorivita, Arenibacter, Cellulophaga, Croceibacter, Formosa, Gelidibacter, Gillisia, Maribacter, Mesonia, Muricauda, Polaribacter, Psychroflexus, Psychroserpens, Robiginitalea, Salegentibacter, Tenacibaculum, Ulvibacter, Vitellibacter, and Zobellia, p. 677-694. In M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, and E. Stackebrandt (ed.), The prokaryotes, 3rd ed., vol. 7 Springer, New York, NY. [Google Scholar]
  • 5.Capuano, V., N. Galleron, P. Pujic, A. Sorokin, and S. D. Ehrlich. 1996. Organization of the Bacillus subtilis 168 chromosome between kdg and the attachment site of the SPβ prophage: use of Long Accurate PCR and yeast artificial chromosomes for sequencing. Microbiology 142:3005-3015. [DOI] [PubMed] [Google Scholar]
  • 6.Cho, J.-C., and S. J. Giovannoni. 2003. Croceibacter atlanticus gen. nov., sp nov., a novel marine bacterium in the family Flavobacteriaceae. Syst. Appl. Microbiol. 26:76-83. [DOI] [PubMed] [Google Scholar]
  • 7.Connon, S. A., and S. J. Giovannoni. 2002. High-throughput methods for culturing microorganisms in very-low-nutrient media yield diverse new marine isolates. Appl. Environ. Microbiol. 68:3878-3885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Cottrell, M. T., and D. L. Kirchman. 2000. Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl. Environ. Microbiol. 66:1692-1697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Eilers, H., J. Pernthaler, F. O. Glöckner, and R. Amann. 2000. Culturability and in situ abundance of pelagic bacteria from the North Sea. Appl. Environ. Microbiol. 66:3044-3051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Glöckner, F. O., B. M. Fuchs, and R. Amann. 1999. Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl. Environ. Microbiol. 65:3721-3726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Gómez-Consarnau, L., J. M. González, M. Coll-Lladó, P. Gourdon, T. Pascher, R. Neutze, C. Pedrós-Alió, and J. Pinhassi. 2007. Light stimulates growth of proteorhodopsin-containing marine Flavobacteria. Nature 445:210-213. [DOI] [PubMed] [Google Scholar]
  • 12.González, J., B. Fernández-Gómez, A. Fernàndez-Guerra, L. Gómez-Consarnau, O. Sánchez, M. Coll-Lladó, J. Del Campo, L. Escudero, R. Rodríguez-Martínez, L. Alonso-Sáez, M. Latasa, I. Paulsen, O. Nedashkovskaya, I. Lekunberri, J. Pinhassi, and C. Pedrós-Alió. 2008. Genome analysis of the proteorhodopsin-containing marine bacterium Polaribacter sp MED152 (Flavobacteria). Proc. Natl. Acad. Sci. U. S. A. 105:8724-8729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Lidstrom, M. 2006. Aerobic methylotrophic prokaryotes, p. 618-634. In S. F. Martin Dworkin, E. Rosenberg, K.-H. Schleifer, and E. Stackebrandt (ed.), The prokaryotes, 3rd ed., vol. 2 Springer, New York, NY. [Google Scholar]
  • 14.Meyer, F., A. Goesmann, A. C. McHardy, D. Bartels, T. Bekel, J. Clausen, J. Kalinowski, B. Linke, O. Rupp, R. Giegerich, and A. Puhler. 2003. GenDB—an open source genome annotation system for prokaryote genomes. Nucleic Acids Res. 31:2187-2195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Oh, H.-M., S. J. Giovannoni, S. Ferriera, J. Johnson, and J.-C. Cho. 2009. Complete genome sequence of Erythrobacter litoralis HTCC2594. J. Bacteriol. 191:2419-2420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Oh, H.-M., S. J. Giovannoni, K. Lee, S. Ferriera, J. Johnson, and J.-C. Cho. 2009. Complete genome sequence of Robiginitalea biformata HTCC2501. J. Bacteriol. 191:7144-7145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Reichenbach, H., and M. Dworkin. 1992. The order Cytophagales, p. 3631-3675. In H. G. T. A. Balows, M. Dworkin, W. Harder, and K.-H. Schleifer, (ed.), The prokaryotes, 2nd ed., vol. 4 Springer, Berlin, Germany. [Google Scholar]
  • 18.Schneiker, S., O. Perlova, O. Kaiser, K. Gerth, A. Alici, M. O. Altmeyer, D. Bartels, T. Bekel, S. Beyer, E. Bode, H. B. Bode, C. J. Bolten, J. V. Choudhuri, S. Doss, Y. A. Elnakady, B. Frank, L. Gaigalat, A. Goesmann, C. Groeger, F. Gross, L. Jelsbak, L. Jelsbak, J. Kalinowski, C. Kegler, T. Knauber, S. Konietzny, M. Kopp, L. Krause, D. Krug, B. Linke, T. Mahmud, R. Martinez-Arias, A. C. McHardy, M. Merai, F. Meyer, S. Mormann, J. Munoz-Dorado, J. Perez, S. Pradella, S. Rachid, G. Raddatz, F. Rosenau, C. Ruckert, F. Sasse, M. Scharfe, S. C. Schuster, G. Suen, A. Treuner-Lange, G. J. Velicer, F.-J. Vorholter, K. J. Weissman, R. D. Welch, S. C. Wenzel, D. E. Whitworth, S. Wilhelm, C. Wittmann, H. Blocker, A. Puhler, and R. Muller. 2007. Complete genome sequence of the myxobacterium Sorangium cellulosum Nat. Biotechnol. 25:1281-1289. [DOI] [PubMed] [Google Scholar]

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