PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of jbacterPermissionsJournals.ASM.orgJournalJB ArticleJournal InfoAuthorsReviewers
 
J Bacteriol. 2009 November; 191(22): 7144–7145.
Published online 2009 September 18. doi:  10.1128/JB.01191-09
PMCID: PMC2772462

Complete Genome Sequence of Robiginitalea biformata HTCC2501[down-pointing small open triangle]

Abstract

Robiginitalea biformata HTCC2501, isolated from the Sargasso Sea by dilution-to-extinction culturing, has been known as an aerobic chemoheterotroph with carotenoid pigments and dimorphic growth phases. Here, we announce the complete sequence of the R. biformata HTCC2501 genome, which contains genes for carotenoid biosynthesis and several macromolecule-degrading enzymes.

Members of the phylum Bacteroidetes constitute 6 to ~30% of total bacterial communities in the ocean, as shown by fluorescence in situ hybridization (4, 6, 8). The family Flavobacteriaceae, one of the major phylogenetic lineages in the phylum Bacteroidetes, forms a well-defined clade in the 16S rRNA gene phylogeny (2). Members of the family Flavobacteriaceae are gram negative, non-spore forming, and have low DNA G+C contents (27 to 44 mol%). They are short to moderately long rods that cannot degrade crystalline cellulose, according to the description of the family (1). They have been considered to be typical chemoheterotrophs that have the ability to degrade high-molecular-weight compounds. Some bacterial species from the genera Polaribacter and Dokdonia in the family Flavobacteriaceae have also been shown to have the light-dependent proton pump proteorhodopsin and display light-stimulated photoheterotrophic growth (9, 10).

Robiginitalea biformata HTCC2501 was originally isolated from the Sargasso Sea (Atlantic Ocean) by dilution-to-extinction culturing; based on the organism's low level of 16S rRNA gene sequence similarity to known members of the family Flavobacteriaceae, its distinctively high DNA G+C content, and carotenoid pigments, it was identified as a member of a new genus of Flavobacteriaceae (3). Recently, another member of the genus Robiginitalea, R. myxolifaciens (12), which exhibits ca. 8.5% DNA-DNA relatedness to strain HTCC2501, was reported to produce the monocyclic carotenoid (3R, 2′S)-myxol (12, 16). As the species name implies, the morphology of R. biformata varies from straight rods (in exponential phase) to coccoid cells (in stationary phase) (3), which is also observed for R. myxolifaciens (12).

Here, we report the genome sequence of R. biformata HTCC2501, which was initially determined by the J. Craig Venter Institute as a part of the Moore Foundation Microbial Genome Sequencing Project (http://www.moore.org/microgenome) and completed in the present study. Gaps between contigs were closed using direct sequencing of combinatorial PCR products by Genotech Co., Ltd. (Republic of Korea). The finished genome contig was analyzed by a genome annotation system built on GenDB (13) at the Center for Genome Research and Biocomputing at Oregon State University or by the NCBI Prokaryotic Genomes Automatic Annotation Pipeline (5). The R. biformata HTCC2501 genome contains one circular chromosome of 3,530,383 bp with no plasmid and a 55.29% G+C content. The number of protein coding genes is 3,211; there are two copies of 16S-23S-5S rRNA genes and 40 tRNA genes encoding 20 aminoacyl-tRNAs. No prophage sequences were found in the genome by the Phage_Finder program (7). The genome comprises a normal complement of genes for metabolic enzymes involved in aerobic respiration, morphogenesis (rod shape-determining protein), and the biosynthesis of 20 amino acids, fatty acids, menaquinone, and phylloquinone, as well as essential genes including those for nucleotide metabolism, transcription, replication, and protein synthesis.

R. biformata HTCC2501 forms colonies with a characteristic rusty red pigment (3). The complete genome contains genes for carotenoid biosynthesis but no genes for phototrophy, confirming the organism's obligately chemoheterotrophic metabolism. The genome of strain HTCC2501 has a set of genes for a putative carbon monoxide dehydrogenase and enzymes required to degrade high-molecular-weight compounds, including protease, sulfatase, pectinase, chitinase, α-amylases, and a predicted glycogen debranching enzyme. Aerobic carbon monoxide (CO) oxidation is an important biogeochemical process in marine environments (11, 14), and it is mediated by aerobic-type CO dehydrogenase (CODH), a molybdopterin protein (15). Although the genome contains genes (coxL and coxS) for a putative aerobic-type CODH, a complete pathway for CO utilization could not be reconstructed in strain HTCC2501 because the HTCC2501 genome lacks coxM and other genes that are thought to be required to produce a functional molybdopterin CODH.

Flavobacterial monocyclic carotenoids, such as saproxanthin and myxol, are rarely found in nature but were demonstrated previously to show significant antioxidative activities against lipid peroxidation and neuroprotective effects against l-glutamate toxicity (16). As Shindo et al. (16) suggested, members of the Flavobacteriaceae may be promising sources of diverse novel monocyclic carotenoids. Thus, the HTCC2501 genome may provide a model for studying the biosynthesis of carotenoid congeners produced by marine Flavobacteriaceae and related species.

Nucleotide sequence accession numbers.

The complete genome sequence of R. biformata HTCC2501 was deposited in GenBank under accession number CP001712. The GenDB-generated data were also processed to be accessible in the Marine Microbial Genomics database 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 Oregon State University High Throughput Culturing Laboratory with support from a Gordon and Betty Moore Foundation investigator award and the Gordon and Betty Moore Foundation Marine Microbiology Initiative (http://www.moore.org/marine-micro.aspx). The present work was supported by the 21C Frontier Program of Microbial Genomics and Applications, funded by the MEST, and the Marine and Extreme Genome Research Center Program, funded by the MLTM, Republic of Korea.

We thank Jason Miller, Granger Sutton, Saul A. Kravitz, Robert Friedman, and Yu-Hui Rogers for their technical and scientific support of the Gordon and Betty Moore Foundation-funded project. We are also grateful to Haeyoung Jeong (KRIBB) for his graceful bioinformatics support.

Footnotes

[down-pointing small open triangle]Published ahead of print on 18 September 2009.

REFERENCES

1. 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. [PubMed]
2. 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: a handbook on the biology of bacteria, 3rd ed., vol. 7. Springer, New York, NY.
3. Cho, J. C., and S. J. Giovannoni. 2004. Robiginitalea biformata gen. nov., sp nov., a novel marine bacterium in the family Flavobacteriaceae with a higher G+C content. Int. J. Syst. Evol. Microbiol. 54:1101-1106. [PubMed]
4. 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. [PMC free article] [PubMed]
5. Daraselia, N., D. Dernovoy, Y. Tian, M. Borodovsky, R. Tatusov, and T. Tatusova. 2003. Reannotation of Shewanella oneidensis genome. OMICS 7:171-175. [PubMed]
6. 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. [PMC free article] [PubMed]
7. Fouts, D. E. 2006. Phage_Finder: automated identification and classification of prophage regions in complete bacterial genome sequences. Nucleic Acids Res. 34:5839-5851. [PubMed]
8. 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. [PMC free article] [PubMed]
9. Gomez-Consarnau, L., J. M. Gonzalez, M. Coll-Llado, P. Gourdon, T. Pascher, R. Neutze, C. Pedros-Alio, and J. Pinhassi. 2007. Light stimulates growth of proteorhodopsin-containing marine Flavobacteria. Nature 445:210-213. [PubMed]
10. Gonzalez, J. M., B. Fernandez-Gomez, A. Fernandez-Guerra, L. Gomez-Consarnau, O. Sanchez, M. Coll-Llado, J. del Campo, L. Escudero, R. Rodriguez-Martinez, L. Alonso-Saez, M. Latasa, I. Paulsen, O. Nedashkovskaya, I. Lekunberri, J. Pinhassi, and C. Pedros-Alio. 2008. Genome analysis of the proteorhodopsin-containing marine bacterium Polaribacter sp. MED152 (Flavobacteria). Proc. Natl. Acad. Sci. USA 105:8724-8729. [PubMed]
11. King, G. M., and C. F. Weber. 2007. Distribution, diversity and ecology of aerobic CO-oxidizing bacteria. Nat. Rev. Microbiol. 5:107-118. [PubMed]
12. Manh, H. D., Y. Matsuo, A. Katsuta, S. Matsuda, Y. Shizuri, and H. Kasai. 2008. Robiginitalea myxolifaciens sp. nov., a novel myxol-producing bacterium isolated from marine sediment, and emended description of the genus Robiginitalea. Int. J. Syst. Evol. Microbiol. 58:1660-1664. [PubMed]
13. 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. [PMC free article] [PubMed]
14. Moran, M. A., and W. L. Miller. 2007. Resourceful heterotrophs make the most of light in the coastal ocean. Nat. Rev. Microbiol. 5:792-800. [PubMed]
15. Ragsdale, S. W. 2004. Life with carbon monoxide. Crit. Rev. Biochem. Mol. Biol. 39:165-195. [PubMed]
16. Shindo, K., K. Kikuta, A. Suzuki, A. Katsuta, H. Kasai, M. Yasumoto-Hirose, Y. Matsuo, N. Misawa, and S. Takaichi. 2007. Rare carotenoids, (3R)-saproxanthin and (3R,2′S)-myxol, isolated from novel marine bacteria (Flavobacteriaceae) and their antioxidative activities. Appl. Microbiol. Biotechnol. 74:1350-1357. [PubMed]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)