Skip to main content
Log in

Comparative genome analysis of the Flavobacteriales bacterium strain UJ101, isolated from the gut of Atergatis reticulatus

  • Systems and Synthetic Microbiology and Bioinformatics
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Here we report the comparative genomic analysis of strain UJ101 with 15 strains from the family Flavobacteriaceae, using the CGExplorer program. Flavobacteriales bacterium strain UJ101 was isolated from a xanthid crab, Atergatis reticulatus, from the East Sea near Korea. The complete genome of strain UJ101 is a 3,074,209 bp, single, circular chromosome with 30.74% GC content. While the UJ101 genome contains a number of annotated genes for many metabolic pathways, such as the Embden–Meyerhof pathway, the pentose phosphate pathway, the tricarboxylic acid (TCA) cycle, and the glyoxylate cycle, genes for the Entner-Douddoroff pathway are not found in the UJ101 genome. Overall, carbon fixation processes were absent but nitrate reduction and denitrification pathways were conserved. The UJ101 genome was compared to genomes from other marine animals (three invertebrate strains and 5 fish strains) and other marine animal- derived genera. Notable results by genome comparisons showed that UJ101 is capable of denitrification and nitrate reduction, and that biotin-thiamine pathway participation varies among marine bacteria; fish-dwelling bacteria, freeliving bacteria, invertebrate-dwelling bacteria, and strain UJ101. Pan-genome analysis of the 16 strains in this study included 7,220 non-redundant genes that covered 62% of the pan-genome. A core-genome of 994 genes was present and consisted of 8% of the genes from the pan-genome. Strain UJ101 is a symbiotic hetero-organotroph isolated from xanthid crab, and is a metabolic generalist with nitrate-reducing abilities but without the ability to synthesize biotin. There is a general tendency of UJ101 and some fish pathogens to prefer thiamine-dependent glycolysis to gluconeogenesis. Biotin and thiamine auxotrophy or prototrophy may be used as important markers in microbial community studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aziz, R.K., Bartels, D., Best, A.A., DeJongh, M., Disz, T., Edwards, R.A., Formsma, K., Gerdes, S., Glass, E.M., Kubal, M., et al. 2008. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9, 75.

    Article  PubMed  PubMed Central  Google Scholar 

  • Braker, G., Fesefeldt, A., and Witzel, K.P. 1998. Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl. Environ. Microbiol. 64, 3769–3775.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Castillo, D., Christiansen, R.H., Dalsgaard, I., Madsen, L., Espejo, R., and Middelboe, M. 2016. Comparative genome analysis provides insights into the pathogenicity of Flavobacterium psychrophilum. PLoS One 11, e0152515.

    Google Scholar 

  • Cho, C. 1990. Fish nutrition, feeds, and feeding: with special emphasis on salmonid aquaculture. Food Rev. Int. 6, 333–357.

    Article  CAS  Google Scholar 

  • Declercq, A.M., Haesebrouck, F., Van den Broeck, W., Bossier, P., and Decostere, A. 2013. Columnaris disease in fish: a review with emphasis on bacterium-host interactions. Vet. Res. 44, 27.

    Article  PubMed  PubMed Central  Google Scholar 

  • Du, Q., Wang, H., and Xie, J. 2011. Thiamin (Vitamin B1) biosynthesis and regulation: a rich source of antimicrobial drug targets? Int. J. Biol. Sci. 7, 41–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duchaud, E., Boussaha, M., Loux, V., Bernardet, J.F., Michel, C., Kerouault, B., Mondot, S., Nicolas, P., Bossy, R., Caron, C., et al. 2007. Complete genome sequence of the fish pathogen Flavobacterium psychrophilum. Nat. Biotechnol. 25, 763–769.

    Article  CAS  PubMed  Google Scholar 

  • Fu, Y., Tang, X., Lai, Q., Zhang, C., Zhong, H., Li, W., Liu, Y., Chen, L., Sun, F., and Shao, Z. 2011. Flavobacterium beibuense sp. nov., isolated from marine sediment. Int. J. Syst. Evol. Microbiol. 61, 205–209.

    Article  CAS  PubMed  Google Scholar 

  • Gil-Solsona, R., Nácher-Mestre, J., Lacalle-Bergeron, L., Sancho, J.V., Calduch-Giner, J.A., Hernández, F., and Pérez-Sánchez, J. 2017. Untargeted metabolomics approach for unraveling robust biomarkers of nutritional status in fasted gilthead sea bream (Sparus aurata). PeerJ. 5, e2920.

    Article  Google Scholar 

  • Giovannoni, S.J. 2012. Vitamins in the sea. Proc. Natl. Acad. Sci. USA 109, 13888–13889.

    Article  CAS  Google Scholar 

  • Helen, D., Kim, H., Tytgat, B., and Anne, W. 2016. Highly diverse nirK genes comprise two major clades that harbour ammoniumproducing denitrifiers. BMC Genomics 17, 155.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jang, H., Yang, S.H., Seo, H.S., Lee, J.H., Kim, S.J., and Kwon, K.K. 2015. Amphritea spongicola sp. nov., isolated from a marine sponge, and emended description of the genus Amphritea. Int. J. Syst. Evol. Microbiol. 65, 1866–1870.

    Article  CAS  PubMed  Google Scholar 

  • Jit, S., Dadhwal, M., Prakash, O., and Lal, R. 2008. Flavobacterium lindanitoleran sp. nov., isolated from hexachlorocyclohexanecontaminated soil. Int. J. Syst. Evol. Microbiol. 58, 1665–1669.

    Article  CAS  PubMed  Google Scholar 

  • Jitrapakdee, S., St Maurice, M., Rayment, I., Cleland, W.W., Wallace, J.C., and Attwood, P.V. 2008. Structure, mechanism and regulation of pyruvate carboxylase. Biochem. J. 413, 369–387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kabisch, A., Otto, A., Konig, S., Becher, D., Albrecht, D., Schuler, M., Teeling, H., Amann, R.I., and Schweder, T. 2014. Functional characterization of polysaccharide utilization loci in the marine Bacteroidetes 'Gramella forsetii' KT0803. ISME J. 8, 1492–1502.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan, S.T., Nakagawa, Y., and Harayama, S. 2006. Sandarakinotalea sediminis gen. nov., sp. nov., a novel member of the family Flavobacteriaceae. Int. J. Syst. Evol. Microbiol. 56, 959–963.

    Article  CAS  PubMed  Google Scholar 

  • Kolton, M., Sela, N., Elad, Y., and Cytryn, E. 2013. Comparative genomic analysis indicates that niche adaptation of terrestrial Flavobacteria is strongly linked to plant glycan metabolism. PLoS One 8, e76704.

    Article  Google Scholar 

  • Kopel, M., Helbert, W., Henrissat, B., Doniger, T., and Banin, E. 2014. Draft genome sequence of Nonlabens ulvanivorans, an ulvan-degrading bacterium. Genome Announc. 2, e00793–14.

    Google Scholar 

  • Kwon, S.K., Kim, B.K., Song, J.Y., Kwak, M.J., Lee, C.H., Yoon, J.H., Oh, T.K., and Kim, J.F. 2013. Genomic makeup of the marine flavobacterium Nonlabens (Donghaeana) dokdonensis and identification of a novel class of rhodopsins. Genome Biol. Evol. 5, 187–199.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lagesen, K., Hallin, P., Rodland, E.A., Staerfeldt, H.H., Rognes, T., and Ussery, D.W. 2007. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35, 3100–3108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lau, S.C., Tsoi, M.M., Li, X., Plakhotnikova, I., Dobretsov, S., Wong, P.K., and Qian, P.Y. 2005. Gramella portivictoriae sp. nov., a novel member of the family Flavobacteriaceae isolated from marine sediment. Int. J. Syst. Evol. Microbiol. 55, 2497–2500.

    Article  CAS  PubMed  Google Scholar 

  • Lefébure, T. and Stanhope, M.J. 2007. Evolution of the core and pan-genome of Streptococcus: positive selection, recombination, and genome composition. Genome Biol. 8, R71.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lowe, T.M. and Eddy, S.R. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955–964.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nedashkovskaya, O.I., Kim, S.B., Lysenko, A.M., Frolova, G.M., Mikhailov, V.V., Bae, K.S., Lee, D.H., and Kim, I.S. 2005. Gramella echinicola gen. nov., sp. nov., a novel halophilic bacterium of the family Flavobacteriaceae isolated from the sea urchin Strongylocentrotus intermedius. Int. J. Syst. Evol. Microbiol. 55, 391–394.

    Article  CAS  PubMed  Google Scholar 

  • Nedashkovskaya, O.I., Suzuki, M., Vysotskii, M.V., and Mikhailov, V.V. 2003. Vitellibacter vladivostokensis gen. nov., sp. nov., a new member of the phylum Cytophaga-Flavobacterium-Bacteroides. Int. J. Syst. Evol. Microbiol. 53, 1281–1286.

    Article  CAS  PubMed  Google Scholar 

  • Nelson, D.L. and Cox, M.M. 2013. Lehninger principles of biochemistry, p. 653.

    Google Scholar 

  • Park, S., Yoshizawa, S., Chiura, H.X., Muramatsu, Y., Nakagawa, Y., Kogure, K., and Yokota, A. 2012. Nonlabens marinus sp. nov., a novel member of the Flavobacteriaceae isolated from the Pacific Ocean. Antonie van Leeuwenhoek 102, 669–676.

    Article  CAS  PubMed  Google Scholar 

  • Poston, H. 1976. Optimum level of dietary biotin for growth, feed utilization, and swimming stamina of fingerling lake trout (Salvelinus namaycush). J. Fish. Board Can. 33, 1803–1806.

    Article  Google Scholar 

  • Ramírez, C. and Romero, J. 2017. Fine flounder (Paralichthys adspersus) microbiome showed important differences between wild and reared specimens. Front. Microbiol. 8, 271.

    Article  PubMed  PubMed Central  Google Scholar 

  • Robinson, E. and Lovell, R. 1978. Essentiality of biotin for channel catfish (Ictalurus punctatus) fed lipid and lipid-free diets. J. Nutrit. 108, 1600–1605.

    CAS  PubMed  Google Scholar 

  • Sañudo-Wilhelmy, S.A., Cutter, L.S., Durazo, R., Smail, E.A., Gómez-Consarnau, L., Webb, E.A., Prokopenko, M.G., Berelson, W.M., and Karl, D.M. 2012. Multiple B-vitamin depletion in large areas of the coastal ocean. Proc. Natl. Acad. Sci. USA 109, 14041–14045.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sañudo-Wilhelmy, S.A., Gómez-Consarnau, L., Suffridge, C., and Webb, E.A. 2014. The role of B vitamins in marine biogeochemistry. Ann. Rev. Mar. Sci. 6, 339–367.

    Article  PubMed  Google Scholar 

  • Saisho, T., Noguchi, T., Koyama, K., Uzu, A., Kikuta, T., and Hashimoto, K. 1983. Examination of stomach contents in xanthid crabs. Bull. Jap. Soc. Sci. Fish. 49, 939–947.

    Article  Google Scholar 

  • Sang, M.K. and Kim, K.D. 2012. The volatile-producing Flavobacterium johnsoniae strain GSE09 shows biocontrol activity against Phytophthora capsici in pepper. J. Appl. Microbiol. 113, 383–398.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki, M., Nakagawa, Y., Harayama, S., and Yamamoto, S. 2001. Phylogenetic analysis and taxonomic study of marine Cytophagalike bacteria: proposal for Tenacibaculum gen. nov. with Tenacibaculum maritimum comb. nov. and Tenacibaculum ovolyticum comb. nov., and description of Tenacibaculum mesophilum sp. nov. and Tenacibaculum amylolyticum sp. nov. Int. J. Syst. Evol. Microbiol. 51, 1639–1652.

    Article  CAS  PubMed  Google Scholar 

  • Tatusov, R.L., Galperin, M.Y., Natale, D.A., and Koonin, E.V. 2000. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 28, 33–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Touchon, M., Barbier, P., Bernardet, J.F., Loux, V., Vacherie, B., Barbe, V., Rocha, E.P., and Duchaud, E. 2011. Complete genome sequence of the fish pathogen Flavobacterium branchiophilum. Appl. Environ. Microbiol. 77, 7656–7662.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Touchon, M., Hoede, C., Tenaillon, O., Barbe, V., Baeriswyl, S., Bidet, P., Bingen, E., Bonacorsi, S., Bouchier, C., Bouvet, O., et al. 2009. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet. 5, e1000344.

    Article  Google Scholar 

  • Xing, P., Hahnke, R.L., Unfried, F., Markert, S., Huang, S., Barbeyron, T., Harder, J., Becher, D., Schweder, T., Glöckner, et al. 2015. Niches of two polysaccharide-degrading Polaribacter isolates from the North Sea during a spring diatom bloom. ISME J. 9, 1410–1422.

    Article  CAS  PubMed  Google Scholar 

  • Yang, J.A., Kang, I., Moon, M., Ryu, U.C., Kwon, K.K., Cho, J.C., and Oh, H.M. 2016. Complete genome sequence of Celeribacter marinus IMCC12053T, the host strain of marine bacteriophage P12053L. Mar. Genomics 26, 5–7.

    Article  PubMed  Google Scholar 

  • Yang, J.A., Kwon, K.K., and Oh, H.M. 2017. Complete genome sequence of Flavobacteriales bacterium strain UJ101 isolated from a Xanthid Crab. Genome Announc. 5, e01551–16.

    Google Scholar 

  • Yasumura, D., Oshima, Y., Yasumoto, T., Alcala, A.C., and Alcala, L.C. 1986. Tetrodotoxin and paralytic shellfish toxins in Philippine crabs. Agricul. Biol. Chem. 50, 593–598.

    CAS  Google Scholar 

  • Yoon, S.H., Ha, S.M., Kwon, S., Lim, J., Kim, Y., Seo, H., and Chun, J. 2016. Introducing EzBioCloud: A taxonomically united database of 16S rRNA and whole genome assemblies. Int. J. Syst. Evol. Microbiol. 67, 1613–1617.

    Google Scholar 

  • Yoon, J.H., Kang, S.J., and Oh, T.K. 2005. Tenacibaculum lutimaris sp. nov., isolated from a tidal flat in the Yellow Sea, Korea. Int. J. Syst. Evol. Microbiol. 55, 793–798.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Y., Liu, J., Tang, K., Yu, M., Coenye, T., and Zhang, X.H. 2015. Genome analysis of Flaviramulus ichthyoenteri Th78T in the family Flavobacteriaceae: insights into its quorum quenching property and potential roles in fish intestine. BMC Genomics 16, 38.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hyun-Myung Oh.

Additional information

Supplemental material for this article may be found at http://www.springerlink.com/content/120956.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, JA., Yang, SH., Kim, J. et al. Comparative genome analysis of the Flavobacteriales bacterium strain UJ101, isolated from the gut of Atergatis reticulatus . J Microbiol. 55, 583–591 (2017). https://doi.org/10.1007/s12275-017-7172-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-017-7172-2

Keywords

Navigation