Skip to main content
SpringerLink
Log in

Flavobacterium psychrotrophum sp. nov. and Flavobacterium panacagri sp. nov., Isolated from Freshwater and Soil

  • Microbial Systematics and Evolutionary Microbiology
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Two novel bacterial strains CJ74T and CJ75T belonging to the genus Flavobacterium were isolated from freshwater of Han River and ginseng soil, South Korea, respectively. Strain CJ74T was Gram-stain-negative, aerobic, rod-shaped, non-motile, and non-flagellated, and did not produce flexirubin-type pigments. Strain CJ75T was Gram-stain-negative, aerobic, rod-shaped, motile by gliding, and non-flagellated, and produced flexirubin-type pigments. Both strains were shown to grow optimally at 30 °C in the absence of NaCl on R2A medium. Phylogenetic analysis based on 16S rRNA gene sequences showed that strains CJ74T and CJ75T belonged to the genus Flavobacterium and were most closely related to Flavobacterium niveum TAPW14T and Flavobacterium foetidum CJ42T with 96.17% and 97.29% 16S rRNA sequence similarities, respectively. Genomic analyses including the reconstruction of phylogenomic tree, average nucleotide identity, and digital DNA-DNA hybridization suggested that they were novel species of the genus Flavobacterium. Both strains contained menaquinone 6 (MK-6) as the primary respiratory quinone and phosphatidylethanolamine as a major polar lipid. The predominant fatty acids of both strains were iso-C15:0 and summed feature 3 (C16:1 ω7c and/or C16:1 ω6c). Based on the polyphasic taxonomic study, strains CJ74T and CJ75T represent novel species of the genus Flavobacterium, for which names Flavobacterium psychrotrophum sp. nov. and Flavobacterium panacagri sp. nov. are proposed, respectively. The type strains are CJ74T (=KACC 19819T =JCM 32889T) and CJ75T (=KACC 23149T =JCM 36132T).

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ali, Z., Cousin, S., Frühling, A., Brambilla, E., Schumann, P., Yang, Y., & Stackebrandt, E. (2009). Flavobacterium rivuli sp. nov., Flavobacterium subsaxonicum sp. nov., Flavobacterium swingsii sp. nov. and Flavobacterium reichenbachii sp. nov., isolated from a hard water rivulet. International Journal of Systematic and Evolutionary Microbiology, 59, 2610–2617.

    Article  CAS  PubMed  Google Scholar 

  • Baek, C., Shin, S. K., & Yi, H. (2018). Flavobacterium magnum sp. nov., Flavobacterium pallidum sp. nov., Flavobacterium crocinum sp. nov. and Flavobacterium album sp. nov. International Journal of Systematic and Evolutionary Microbiology, 68, 3837–3843.

    Article  CAS  PubMed  Google Scholar 

  • Baker, G. C., Smith, J. J., & Cowan, D. A. (2003). Review and re-analysis of domain-specific 16S primers. Journal of Microbiological Methods, 55, 541–555.

    Article  CAS  PubMed  Google Scholar 

  • Bayliss, S. C., Thorpe, H. A., Coyle, N. M., Sheppard, S. K., & Feil, E. J. (2019). PIRATE: a fast and scalable pangenomics toolbox for clustering diverged orthologues in bacteria. Gigascience, 8, 119.

    Article  Google Scholar 

  • Bergey, D., Harrison, F., Breed, R., Hammer, B., & Huntoon, F. (1923). Genus II. Flavobacterium gen. nov. Bergey’s manual of determinative bacteriology (pp. 97–117). Baltimore: The Williams & Wilkins Co.

    Google Scholar 

  • Bernardet, J. F., & Bowman, J. P. (2006). The genus Flavobacterium. In M. Dworkin, S. Falkow, E. Rosenberg, K. H. Schleifer, & E. Stackebrandt (Eds.), The prokaryotes: The biology of bacteria (3rd ed., pp. 481–531). Springer.

    Chapter  Google Scholar 

  • Bernardet, J. F., Nakagawa, Y., Holmes, B., Subcommittee On The Taxonomy Of Flavobacterium And Cytophaga-Like Bacteria Of The International Committee On Systematics Of Prokaryotes. (2002). Proposed minimal standards for describing new taxa of the family Flavobacteriaceae and emended description of the family. International Journal of Systematic and Evolutionary Microbiology, 52, 1049–1070.

    CAS  PubMed  Google Scholar 

  • Bernardet, J. F., Segers, P., Vancanneyt, M., Berthe, F., Kersters, K., & Vandamme, P. (1996). Cutting a Gordian knot: Emended classification and description of the genus Flavobacterium, emended description of the family Flavobacteriaceae, and proposal of Flavobacterium hydatis nom. nov. (Basonym, Cytophaga aquatilis Strohl and Tait 1978). International Journal of Systematic and Evolutionary Microbiology, 46, 128–148.

    Google Scholar 

  • Blin, K., Shaw, S., Kloosterman, A. M., Charlop-Powers, Z., van Wezel, G. P., Medema, M. H., & Weber, T. (2021). antiSMASH 6.0: Improving cluster detection and comparison capabilities. Nucleic Acids Research, 49, W29–W35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bu, J. H., & Cha, C. J. (2018). Flavobacterium foetidum sp. nov., isolated from ginseng soil. International Journal of Systematic and Evolutionary Microbiology, 68, 616–622.

    Article  CAS  PubMed  Google Scholar 

  • Chan, P. P., Lin, B. Y., Mak, A. J., & Lowe, T. M. (2021). tRNAscan-SE 2.0: Improved detection and functional classification of transfer RNA genes. Nucleic Acids Research, 49, 9077–9096.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaudhary, D. K., & Kim, J. (2018). Flavobacterium naphthae sp. nov., isolated from oil-contaminated soil. International Journal of Systematic and Evolutionary Microbiology, 68, 305–309.

    Article  CAS  PubMed  Google Scholar 

  • Chen, W. M., Chen, W. T., Young, C. C., & Sheu, S. Y. (2019). Flavobacterium niveum sp. nov., isolated from a freshwater creek. International Journal of Systematic and Evolutionary Microbiology, 69, 271–277.

    Article  CAS  PubMed  Google Scholar 

  • Chin, C. S., Alexander, D. H., Marks, P., Klammer, A. A., Drake, J., Heiner, C., Clum, A., Copeland, A., Huddleston, J., Eichler, E. E., et al. (2013). Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nature Methods, 10, 563–569.

    Article  CAS  PubMed  Google Scholar 

  • Chun, J., Oren, A., Ventosa, A., Christensen, H., Arahal, D. R., da Costa, M. S., Rooney, A. P., Yi, H., Xu, X. W., De Meyer, S., et al. (2018). Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. International Journal of Systematic and Evolutionary Microbiology, 68, 461–466.

    Article  CAS  PubMed  Google Scholar 

  • Collins, M. D. (1985). Analysis of isoprenoid quinones. In T. Bergan (Ed.), Methods in microbiology (Vol. 18, pp. 329–366). Academic Press.

    Google Scholar 

  • Declercq, A. M., Haesebrouck, F., Van den Broeck, W., Bossier, P., & Decostere, A. (2013). Columnaris disease in fish: A review with emphasis on bacterium-host interactions. Veterinary Research, 44, 27.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dong, K., Chen, F., Du, Y., & Wang, G. (2013a). Flavobacterium enshiense sp. nov., isolated from soil, and emended descriptions of the genus Flavobacterium and Flavobacterium cauense, Flavobacterium saliperosum and Flavobacterium suncheonense. International Journal of Systematic and Evolutionary Microbiology, 63, 886–892.

    Article  CAS  PubMed  Google Scholar 

  • Dong, K., Chen, F., Du, Y., & Wang, G. (2013b). Flavobacterium hauense sp. nov., isolated from soil and emended descriptions of Flavobacterium subsaxonicum, Flavobacterium beibuense and Flavobacterium rivuli. International Journal of Systematic and Evolutionary Microbiology, 63, 3237–3242.

    Article  CAS  PubMed  Google Scholar 

  • Dusa, A. (2021). Venn: Draw venn diagrams. https://github.com/dusadrian/venn.

  • Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feldgarden, M., Brover, V., Gonzalez-Escalona, N., Frye, J. G., Haendiges, J., Haft, D. H., Hoffmann, M., Pettengill, J. B., Prasad, A. B., Tillman, G. E., et al. (2021). AMRFinderPlus and the reference gene catalog facilitate examination of the genomic links among antimicrobial resistance, stress response, and virulence. Scientific Reports, 11, 12728.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39, 783–791.

    Article  PubMed  Google Scholar 

  • Frank, J. A., Reich, C. I., Sharma, S., Weisbaum, J. S., Wilson, B. A., & Olsen, G. J. (2008). Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Applied and Environmental Microbiology, 74, 2461–2470.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holmes, B., & Owen, R. (1979). Proposal that Flavobacterium breve be substituted as the type species of the genus in place of Flavobacterium aquatile and emended description of the genus Flavobacterium. International Journal of Systematic and Evolutionary Microbiology, 29, 416–426.

    Google Scholar 

  • Hyatt, D., Chen, G. L., Locascio, P. F., Land, M. L., Larimer, F. W., & Hauser, L. J. (2010). Prodigal: Prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics, 11, 119.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jain, C., Rodriguez-R, L. M., Phillippy, A. M., Konstantinidis, K. T., & Aluru, S. (2018). High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nature Communications, 9, 5114.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jukes, T. H., & Cantor, C. R. (1969). Evolution of protein molecules. In H. N. Munro (Ed.), Mammalian protein metabolism (Vol. 3, pp. 21–132). Academic Press.

    Chapter  Google Scholar 

  • Kalvari, I., Nawrocki, E. P., Ontiveros-Palacios, N., Argasinska, J., Lamkiewicz, K., Marz, M., Griffiths-Jones, S., Toffano-Nioche, C., Gautheret, D., Weinberg, Z., et al. (2021). Rfam 14: Expanded coverage of metagenomic, viral and microRNA families. Nucleic Acids Research, 49, D192–D200.

    Article  CAS  PubMed  Google Scholar 

  • Kang, J. Y., Chun, J., & Jahng, K. Y. (2013). Flavobacterium aciduliphilum sp. nov., isolated from freshwater, and emended description of the genus Flavobacterium. International Journal of Systematic and Evolutionary Microbiology, 63, 1633–1638.

    Article  CAS  PubMed  Google Scholar 

  • Kim, J., Na, S. I., Kim, D., & Chun, J. (2021). UBCG2: Up-to-date bacterial core genes and pipeline for phylogenomic analysis. Journal of Microbiology, 59, 609–615.

    Article  CAS  PubMed  Google Scholar 

  • Kim, M., Oh, H. S., Park, S. C., & Chun, J. (2014). Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. International Journal of Systematic and Evolutionary Microbiology, 64, 346–351.

    Article  CAS  PubMed  Google Scholar 

  • Kuo, I., Saw, J., Kapan, D. D., Christensen, S., Kaneshiro, K. Y., & Donachie, S. P. (2013). Flavobacterium akiainvivens sp. nov., from decaying wood of Wikstroemia oahuensis, Hawai ‘i, and emended description of the genus Flavobacterium. International Journal of Systematic and Evolutionary Microbiology, 63, 3280–3286.

    Article  CAS  PubMed  Google Scholar 

  • Laslett, D., & Canback, B. (2004). ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Research, 32, 11–16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, K., Kim, D. W., & Cha, C. J. (2021). Overview of bioinformatic methods for analysis of antibiotic resistome from genome and metagenome data. Journal of Microbiology, 59, 270–280.

    Article  CAS  PubMed  Google Scholar 

  • Li, A., Liu, H., Sun, B., Zhou, Y., & Xin, Y. (2014). Flavobacterium lacus sp. nov., isolated from a high-altitude lake, and emended description of Flavobacterium filum. International Journal of Systematic and Evolutionary Microbiology, 64, 933–939.

    Article  CAS  PubMed  Google Scholar 

  • Liu, Y., Le Han, H., Zou, Y., & Kim, S. G. (2019). Flavobacterium ustbae sp. nov., isolated from rhizosphere soil of Alhagi sparsifolia. International Journal of Systematic and Evolutionary Microbiology, 69, 3955–3960.

    Article  CAS  PubMed  Google Scholar 

  • Manni, M., Berkeley, M. R., Seppey, M., & Zdobnov, E. M. (2021). BUSCO: assessing genomic data quality and beyond. Current Protocols, 1, e323.

    Article  PubMed  Google Scholar 

  • McBride, M. J., & Zhu, Y. (2013). Gliding motility and Por secretion system genes are widespread among members of the phylum Bacteroidetes. Journal of Bacteriology, 195, 270–278.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meier-Kolthoff, J. P., Carbasse, J. S., Peinado-Olarte, R. L., & Göker, M. (2022). TYGS and LPSN: A database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Research, 50, 801–807.

    Article  Google Scholar 

  • Minh, B. Q., Schmidt, H. A., Chernomor, O., Schrempf, D., Woodhams, M. D., von Haeseler, A., & Lanfear, R. (2020). IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution, 37, 1530–1534.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minnikin, D. E., Odonnell, A. G., Goodfellow, M., Alderson, G., Athalye, M., Schaal, A., & Parlett, J. H. (1984). An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. Journal of Microbiological Methods, 2, 233–241.

    Article  CAS  Google Scholar 

  • Nematollahi, A., Decostere, A., Pasmans, F., & Haesebrouck, F. (2003). Flavobacterium psychrophilum infections in salmonid fish. Journal of Fish Diseases, 26, 563–574.

    Article  CAS  PubMed  Google Scholar 

  • Nogi, Y., Soda, K., & Oikawa, T. (2005). Flavobacterium frigidimaris sp. nov., isolated from Antarctic seawater. Systematic and Applied Microbiology, 28, 310–315.

    Article  CAS  PubMed  Google Scholar 

  • Parte, A. C., SardàCarbasse, J., Meier-Kolthoff, J. P., Reimer, L. C., & Göker, M. (2020). List of prokaryotic names with standing in nomenclature (LPSN) moves to the DSMZ. International Journal of Systematic and Evolutionary Microbiology, 70, 5607–5612.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rhoads, A., & Au, K. F. (2015). PacBio sequencing and its applications. Genomics, Proteomics & Bioinformatics, 13, 278–289.

    Article  Google Scholar 

  • Richter, M., & Rosselló-Móra, R. (2009). Shifting the genomic gold standard for the prokaryotic species definition. Proceedings of the National Academy of Sciences of the United States of America, 106, 19126–19131.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosselló-Móra, R., & Amann, R. (2015). Past and future species definitions for Bacteria and Archaea. Systematic and Applied Microbiology, 38, 209–216.

    Article  PubMed  Google Scholar 

  • Sasser, M. (1990). Identification of bacteria by gas chromatography of cellular fatty acids. Technical Note 101. Microbial ID, Inc., Newark, Delaware

  • Schwengers, O., Jelonek, L., Dieckmann, M. A., Beyvers, S., Blom, J., & Goesmann, A. (2021). Bakta: Rapid and standardized annotation of bacterial genomes via alignment-free sequence identification. Microbial Genomics, 7, 000685.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38, 3022–3027.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • The UniProt Consortium. (2021). UniProt: The universal protein knowledgebase in 2021. Nucleic Acids Research, 49, D480–D489.

    Article  Google Scholar 

  • Tindall, B. J. (1990a). A comparative study of the lipid composition of Halobacterium saccharovorum from various sources. Systematic and Applied Microbiology, 13, 128–130.

    Article  CAS  Google Scholar 

  • Tindall, B. J. (1990b). Lipid composition of Halobacterium lacusprofundi. FEMS Microbiology Letters, 66, 199–202.

    Article  CAS  Google Scholar 

  • Vancanneyt, M., Segers, P., Torck, U., Hoste, B., Bernardet, J. F., Vandamme, P., & Kersters, K. (1996). Reclassification of Flavobacterium odoratum (Stutzer 1929) strains to a new genus, Myroides, as Myroides odoratus comb. nov. and Myroides odoratimimus sp. nov. International Journal of Systematic and Evolutionary Microbiology, 46, 926–932.

    Google Scholar 

  • Wakabayashi, H., Huh, G. J., & Kimura, N. (1989). Flavobacterium branchiophila sp. nov., a causative agent of bacterial gill disease of freshwater fishes. International Journal of Systematic and Evolutionary Microbiology, 39, 213–216.

    Google Scholar 

  • Wick, R. R., Judd, L. M., Gorrie, C. L., & Holt, K. E. (2017a). Completing bacterial genome assemblies with multiplex MinION sequencing. Microbial Genomics, 3, e000132.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wick, R. R., Judd, L. M., Gorrie, C. L., & Holt, K. E. (2017b). Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Computational Biology, 13, e1005595.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yoon, J. H., Kang, S. J., & Oh, T. K. (2006). Flavobacterium soli sp. nov., isolated from soil. International Journal of Systematic and Evolutionary Microbiology, 56, 997–1000.

    Article  CAS  PubMed  Google Scholar 

  • Yoon, S. H., Ha, S. M., Kwon, S., Lim, J., Kim, Y., Seo, H., & Chun, J. (2017). Introducing EzBioCloud: A taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. International Journal of Systematic and Evolutionary Microbiology, 67, 1613–1617.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, D. C., Wang, H. X., Liu, H. C., Dong, X. Z., & Zhou, P. J. (2006). Flavobacterium glaciei sp. nov., a novel psychrophilic bacterium isolated from the China No.1 glacier. International Journal of Systematic and Evolutionary Microbiology, 56, 2921–2925.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, R., Zhang, X. Y., Sun, X. K., Mu, D. S., & Du, Z. J. (2019). Flavobacterium cerinum sp. nov., isolated from Arctic tundra soil. International Journal of Systematic and Evolutionary Microbiology, 69, 3745–3750.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Prof. Aharon Oren for his help for nomenclature. We thank J. Kim for technical help at the BT research facility center, Chung-Ang University. This work was supported by the National Institute of Biological Resources funded by the Ministry of Environment (No. NIBR202304204) and the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT)(NRF-2023R1A2C1003654).

Author information

Author notes

  1. Yong-Seok Kim and Eun-Mi Hwang contributed equally to this work.

Authors and Affiliations

  1. Department or Systems Biotechnology, Chung-Ang University, Anseong, 17546, Republic of Korea

    Yong-Seok Kim, Eun-Mi Hwang, Chang-Myeong Jeong & Chang-Jun Cha

Authors
  1. Yong-Seok Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eun-Mi Hwang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chang-Myeong Jeong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chang-Jun Cha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chang-Jun Cha.

Ethics declarations

Conflict of Interest

The authors declare no conflict of interest.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 965 KB)

Supplementary file2 (PDF 249 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, YS., Hwang, EM., Jeong, CM. et al. Flavobacterium psychrotrophum sp. nov. and Flavobacterium panacagri sp. nov., Isolated from Freshwater and Soil. J Microbiol. 61, 891–901 (2023). https://doi.org/10.1007/s12275-023-00081-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-023-00081-1

Keywords

Search

Navigation