Skip to main content
Log in

Description of Nocardioides piscis sp. nov., Sphingomonas piscis sp. nov. and Sphingomonas sinipercae sp. nov., isolated from the intestine of fish species Odontobutis interrupta (Korean spotted sleeper) and Siniperca scherzeri (leopard mandarin fish)

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

Abstract

A polyphasic taxonomic approach was used to characterize three novel bacterial strains, designated as HDW12AT, HDW-15BT, and HDW15CT, isolated from the intestine of fish species Odontobutis interrupta or Siniperca scherzeri. All isolates were obligate aerobic, non-motile bacteria, and grew optimally at 30°C. Phylogenetic analysis based on 16S rRNA sequences revealed that strain HDW12AT was a member of the genus Nocardioides, and closely related to Nocardioides allogilvus CFH 30205T (98.9% sequence identities). Furthermore, strains HDW15BT and HDW15CT were members of the genus Sphingomonas, and closely related to Sphingomonas lutea JS5T and Sphingomonas sediminicola Dae 20T (97.1% and 97.9% sequence identities), respectively. Strain HDW12AT contained MK-8 (H4), and strains HDW15BT and HDW15CT contained Q-10 as the respiratory quinone. Major polar lipid components of strain HDW12AT were diphosphatidylglycerol, phosphatidylglycerol, and phosphatidylinositol, and those of strains HDW15BT and HDW15CT were sphingoglycolipid, diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, and phosphatidylcholine. The G + C content of strains HDW12AT, HDW15BT, and HDW15CT were 69.7, 63.3, and 65.5%, respectively. The results of phylogenetic, phenotypic, chemotaxonomic, and genotypic analyses suggest that strain HDW12AT represents a novel species within the genus Nocardioides, and strains HDW15BT and HDW15CT represent two novel species within the genus Sphingomonas. We propose the names Nocardioides piscis for strain HDW12AT (= KACC 21336T = KCTC 49321T = JCM 33670T), Sphingomonas piscis for strain HDW15BT (= KACC 21341T = KCTC 72588T = JCM 33738T), and Sphingomonas sinipercae for strain HDW15CT (= KACC 21342T = KCTC 72589T = JCM 33739T).

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

  • Benson, H. 1994. Microbiological Application: Laboratory manual in General Microbiology. Wan C. Publishers. Dubuque, USA.

    Google Scholar 

  • Bousfield, G.R., Sugino, H., and Ward, D.N. 1985. Demonstration of a COOH-terminal extension on equine lutropin by means of a common acid-labile bond in equine lutropin and equine chorionic gonadotropin. J. Biol. Chem. 260, 9531–9533.

    Article  CAS  PubMed  Google Scholar 

  • Buonaurio, R., Stravato, V.M., Kosako, Y., Fujiwara, N., Naka, T., Kobayashi, K., Cappelli, C., and Yabuuchi, E. 2002. Sphingomonas melonis sp. nov., a novel pathogen that causes brown spots on yellow Spanish melon fruits. Int. J. Syst. Evol. Microbiol. 52, 2081–2087.

    CAS  PubMed  Google Scholar 

  • Busse, H.J., Denner, E.B.M., Buczolits, S., Salkinoja-Salonen, M., Bennasar, A., and Kämpfer, P. 2003. Sphingomonas aurantiaca sp. nov., Sphingomonas aerolata sp. nov. and Sphingomonas faeni sp. nov., air- and dustborne and Antarctic, orange-pigmented, psychrotolerant bacteria, and emended description of the genus Sphingomonas. Int. J. Syst. Evol. Microbiol. 53, 1253–1260.

    Article  CAS  PubMed  Google Scholar 

  • Chen, I.M.A., Chu, K., Palaniappan, K., Ratner, A., Huang, J., Huntemann, M., Hajek, P., Ritter, S., Varghese, N., Seshadri, R., et al. 2020. The IMG/M data management and analysis system v.6.0: new tools and advanced capabilities. Nucleic Acids Res. 49, D751–D763.

    Article  PubMed Central  Google Scholar 

  • Chen, N., Jiang, J., Gao, X., Li, X., Zhang, Y., Liu, X., Yang, H., Bing, X., and Zhang, X. 2018. Histopathological analysis and the immune related gene expression profiles of mandarin fish (Siniperca chuatsi) infected with Aeromonas hydrophila. Fish Shellfish Immunol. 83, 410–415.

    Article  CAS  PubMed  Google Scholar 

  • Chen, H., Jogler, M., Rohde, M., Klenk, H.P., Busse, H.J., Tindall, B.J., Spröer, C., and Overmann, J. 2012. Reclassification and emended description of Caulobacter leidyi as Sphingomonas leidyi comb. nov., and emendation of the genus Sphingomonas. Int. J. Syst. Evol. Microbiol. 62, 2835–2843.

    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. Int. J. Syst. Evol. Microbiol. 68, 461–466.

    Article  CAS  PubMed  Google Scholar 

  • Collins, M.D. and Jones, D. 1981. Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implication. Microbiol. Rev. 45, 316–354.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Contreras-Moreira, B. and Vinuesa, P. 2013. GET_HOMOLOGUES, a versatile software package for scalable and robust microbial pangenome analysis. Appl. Environ. Microbiol. 79, 7696–7701.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong, K., Lu, S., Yang, J., Pu, J., Lai, X.H., Jin, D., Li, J., Zhang, G., Wang, X., Liang, J., et al. 2020. Nocardioides jishulii sp. nov., isolated from faeces of Tibetan gazelle (Procapra picticaudata). Int. J. Syst. Evol. Microbiol. 70, 3665–3672.

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein, J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17, 368–376.

    Article  CAS  PubMed  Google Scholar 

  • Fitch, W.M. 1971. Toward defining the course of evolution: minimum change for a specific tree topology. Syst. Biol. 20, 406–416.

    Article  Google Scholar 

  • Fredrickson, J.K., Balkwill, D.L., Drake, G.R., Romine, M.F., Ringelberg, D.B., and White, D.C. 1995. Aromatic-degrading Sphingomonas isolates from the deep subsurface. Appl. Environ. Microbiol. 61, 1917–1922.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goszczynska, T. and Serfontein, J. 1998. Milk-Tween agar, a semi-selective medium for isolation and differentiation of Pseudomonas syringae pv. syringae, Pseudomonas syringae pv. phaseolicola and Xanthomonas axonopodis pv. phaseoli. J. Microbiol. Methods 32, 65–72.

    Article  CAS  Google Scholar 

  • Ha, S.M., Kim, C.K., Roh, J., Byun, J.H., Yang, S.J., Choi, S.B., Chun, J., and Yong, D. 2019. Application of the whole genome-based bacterial identification system, TrueBac ID, using clinical isolates that were not identified with three matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) systems. Ann. Lab. Med. 39, 530–536.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hiraishi, A., Ueda, Y., Ishihara, J., and Mori, T. 1996. Comparative lipoquinone analysis of influent sewage and activated sludge by high-performance liquid chromatography and photodiode array detection. J. Gen. Appl. Microbiol. 42, 457–469.

    Article  CAS  Google Scholar 

  • Hyun, D.W., Tak, E.J., Kim, P.S., and Bae, J.W. 2021. Description of Vagococcus coleopterorum sp. nov., isolated from the intestine of the diving beetle, Cybister lewisianus, and Vagococcus hydrophili sp. nov., isolated from the intestine of the dark diving beetle, Hydrophilus acuminatus, and emended description of the genus Vagococcus. J. Microbiol. 59, 132–141.

    Article  CAS  PubMed  Google Scholar 

  • Kilic, A., Senses, Z., Kurekci, A.E., Aydogan, H., Sener, K., Kismet, E., and Basustaoglu, A.C. 2007. Nosocomial outbreak of Sphingomonas paucimobilis bacteremia in a hemato/oncology unit. Jpn. J. Infect. Dis. 60, 394–396.

    PubMed  Google Scholar 

  • Kumar, S., Stecher, G., and Tamura, K. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lane, D. 1991. 16S/23S rRNA sequencing. In Stackbrandt, E. and Goodfellow, M. (eds.), Nucleic acid techniques in bacterial systematics, pp. 115–175. John Wiley & Sons Ltd., Hoboken, New Jersey, USA.

    Google Scholar 

  • Lee, S., Lee, W., Chung, H.M., and Park, S. 2017. Nocardioides suum sp. nov. isolated from the air environment in an indoor pig farm. J. Microbiol. 55, 417–420.

    Article  CAS  PubMed  Google Scholar 

  • Lee, I., Ouk Kim, Y., Park, S.C., and Chun, J. 2016. OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int. J. Syst. Evol. Microbiol. 66, 1100–1103.

    Article  CAS  PubMed  Google Scholar 

  • Li, H., Zhou, Y., Ling, H., Luo, L., Qi, D., and Feng, L. 2019. The effect of dietary supplementation with Clostridium butyricum on the growth performance, immunity, intestinal microbiota and disease resistance of tilapia (Oreochromis niloticus). PLoS ONE 14, e0223428.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin, S.Y., Wen, C.Z., Hameed, A., Liu, Y.C., Hsu, Y.H., Shen, F.T., Lai, W.A., and Young, C.C. 2015. Nocardioides echinoideorum sp. nov., isolated from sea urchins (Tripneustes gratilla). Int. J. Syst. Evol. Microbiol. 65, 1953–1958.

    Article  CAS  PubMed  Google Scholar 

  • Liu, Y.H., Fang, B.Z., Mohamad, O.A.A., Zhang, Y.G., Jiao, J.Y., Dong, Z.Y., Xiao, M., Li, L., and Li, W.J. 2019. Nocardioides ferulae sp. nov., isolated from root of an endangered medicinal plant Ferula songorica Pall. ex Spreng. Int. J. Syst. Evol. Microbiol. 69, 1253–1258.

    Article  CAS  PubMed  Google Scholar 

  • Liu, S.W., Xue, C.M., Li, F.N., and Sun, C.H. 2020. Nocardioides vastitatis sp. nov., isolated from Taklamakan desert soil. Int. J. Syst. Evol. Microbiol. 70, 77–82.

    Article  CAS  PubMed  Google Scholar 

  • Matsumura, Y., Akahira-Moriya, A., and Sasaki-Mori, M. 2015. Bioremediation of bisphenol-A polluted soil by Sphingomonas bisphenolicum AO1 and the microbial community existing in the soil. Biocontrol Sci. 20, 35–42.

    Article  CAS  PubMed  Google Scholar 

  • MIDI. 1999. Sherlock Microbial Identification System Operating Manual, version 3.0. MIDI, Inc., Newark, Delaware, USA.

    Google Scholar 

  • Na, S.I., Kim, Y.O., Yoon, S.H., Ha, S., Baek, I., and Chun, J. 2018. UBCG: Up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J. Microbiol. 56, 280–285.

    Article  CAS  PubMed  Google Scholar 

  • Parte, A.C., Sardà Carbasse, J., Meier-Kolthoff, J.P., Reimer, L.C., and Göker, M. 2020. List of Prokaryotic names with Standing in Nomenclature (LPSN) moves to the DSMZ. Int. J. Syst. Evol. Microbiol. 70, 5607–5612.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pękala-Safińska, A. 2018. Contemporary threats of bacterial infections in freshwater fish. J. Vet. Res. 62, 261–267.

    Article  PubMed  PubMed Central  Google Scholar 

  • Picchietti, S., Miccoli, A., and Fausto, A.M. 2021. Gut immunity in European sea bass (Dicentrarchus labrax): a review. Fish Shellfish Immunol. 108, 94–108.

    Article  CAS  PubMed  Google Scholar 

  • Piutti, S., Semon, E., Landry, D., Hartmann, A., Dousset, S., Lichtfouse, E., Topp, E., Soulas, G., and Martin-Laurent, F. 2003. Isolation and characterisation of Nocardioides sp. SP12, an atrazine-degrading bacterial strain possessing the gene trzN from bulk- and maize rhizosphere soil. FEMS Microbiol. Lett. 221, 111–117.

    Article  CAS  PubMed  Google Scholar 

  • Prauser, H. 1976. Nocardioides, a new genus of the order Actinomycetales. Int. J. Syst. Evol. Microbiol. 26, 58–65.

    Google Scholar 

  • Saitou, N. and Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425.

    CAS  PubMed  Google Scholar 

  • Sasser, M. 1990. Identification of bacteria by gas chromatography of cellular fatty acids. MIDI Technical Note 101. MIDI Inc., Newark, Delaware, USA.

    Google Scholar 

  • Schleifer, K.H. and Kandler, O. 1972. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36, 407–477.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su, S.Q., Zhang, H.Q., He, Z.Y., and Zhang, Z.X. 2005. A comparative study of the nutrients and amino acid composition of the muscle of Siniperca chuatsi and Siniperca scherzeri. Journal of Southwest Agricultural University 27, 898–901.

    Google Scholar 

  • Teather, R.M. and Wood, P.J. 1982. Use of Congo red-polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rumen. Appl. Environ. Microbiol. 43, 777–780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson, J.D., Higgins, D.G., and Gibson, T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian, J., Sun, B., Luo, Y., Zhang, Y., and Nie, P. 2009. Distribution of IgM, IgD and IgZ in mandarin fish, Siniperca chuatsi lymphoid tissues and their transcriptional changes after Flavobacterium columnare stimulation. Aquaculture 288, 14–21.

    Article  CAS  Google Scholar 

  • Tindall, B. 1990. Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol. Lett. 66, 199–202.

    Article  CAS  Google Scholar 

  • Tittsler, R.P. and Sandholzer, L.A. 1936. The use of semi-solid agar for the detection of bacterial motility. J. Bacteriol. 31, 575–580.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuo, L., Dong, Y.P., Habden, X., Liu, J.M., Guo, L., Liu, X.F., Chen, L., Jiang, Z.K., Liu, S.W., Zhang, Y.B., et al. 2015. Nocardioides deserti sp. nov., an actinobacterium isolated from desert soil. Int. J. Syst. Evol. Microbiol. 65, 1604–1610.

    Article  CAS  PubMed  Google Scholar 

  • Xiao, F., Liao, L., Xu, Q., He, Z., Xiao, T., Wang, J., Huang, J., Yu, Y., Wu, B., and Yan, Q. 2021. Host-microbiota interactions and responses to grass carp reovirus infection in Ctenopharyngodon idellus. Environ. Microbiol. 23, 431–447.

    Article  CAS  PubMed  Google Scholar 

  • Xin, H., Itoh, T., Zhou, P., Suzuki, K., Kamekura, M., and Nakase, T. 2000. Natrinema versiforme sp. nov., an extremely halophilic archaeon from Aibi salt lake, Xinjiang, China. Int. J. Syst. Evol. Microbiol. 50, 1297–1303.

    Article  CAS  PubMed  Google Scholar 

  • Yabuuchi, E., Yano, I., Oyaizu, H., Hashimoto, Y., Ezaki, T., and Yamamoto, H. 1990. Proposals of Sphingomonas paucimobilis gen. nov. and comb. nov., Sphingomonas parapaucimobilis sp. nov., Sphingomonas yanoikuyae sp. nov., Sphingomonas adhaesiva sp. nov., Sphingomonas capsulata comb. nov., and two genospecies of the genus Sphingomonas. Microbiol. Immunol. 34, 99–119.

    Article  CAS  PubMed  Google Scholar 

  • Yoon, S.H., Ha, S.M., Kwon, S., Lim, J., Kim, Y., Seo, H., and Chun, J. 2017. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int. J. Syst. Evol. Microbiol. 67, 1613–1617.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon, J. and Park, Y. 2006. The genus Nocardioides. In Dworkin, M., Falkow, S., Schleifer, K.H., and Stackebrandt, E. (eds.), The Prokaryotes, pp. 1099–1113. Springer, New York, USA.

    Chapter  Google Scholar 

  • Zhang, M.L., Li, M., Sheng, Y., Tan, F., Chen, L., Cann, I., and Du, Z.Y. 2020. Citrobacter species increase energy harvest by modulating intestinal microbiota in fish: nondominant species play important functions. mSystems 5, e00303–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou, C., Yang, Q., and Cai, D. 1988. On the classification and distribution of the Sinipercinae fishes (Family Serranidae). Zool. Res. 9, 113–125.

    Google Scholar 

  • Zhou, X.Y., Zhang, L., Su, X.J., Hang, P., Hu, B., and Jiang, J.D. 2019. Sphingomonas flavalba sp. nov., isolated from a procymidone-contaminated soil. Int. J. Syst. Evol. Microbiol. 69, 2936–2941.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Dr. Aharon Oren (The Hebrew University of Jerusalem, Israel) and Dr. Bernard Schink (University of Konstanz, Germany) for etymological advice. This work was supported by grants from the Mid-career Researcher Program (NRF-2020R1A2C3012797) funded by the Ministry of Science and ICT, and the Basic Science Research Program (NRF-2019R1A6A3A01096031) funded by the Ministry of Education through the National Research Foundation of Korea (NRF). This work was also supported by grants from the National Institute of Biological Resources (NIBR201801106), funded by the Ministry of Environment of Korea (MOE).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jin-Woo Bae.

Ethics declarations

Conflict of Interest The authors declare that there are no conflicts of interest.

Ethical Statement All sampling conducted in this study was approved by the Institutional Animal Care and Use Committee of Kyung Hee University (permit no. KHSASP-20-221) and complied with the guidelines of the Committee.

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

Hyun, DW., Jeong, YS., Lee, JY. et al. Description of Nocardioides piscis sp. nov., Sphingomonas piscis sp. nov. and Sphingomonas sinipercae sp. nov., isolated from the intestine of fish species Odontobutis interrupta (Korean spotted sleeper) and Siniperca scherzeri (leopard mandarin fish). J Microbiol. 59, 552–562 (2021). https://doi.org/10.1007/s12275-021-1036-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-021-1036-5

Keywords

Navigation