Skip to main content
SpringerLink
Log in

Leucobacter coleopterorum sp. nov., Leucobacter insecticola sp. nov., and Leucobacter viscericola sp. nov., isolated from the intestine of the diving beetles, Cybister brevis and Cybister lewisianus, and emended description of the genus Leucobacter

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

Abstract

Three novel bacterial strains, HDW9AT, HDW9BT, and HDW9CT, isolated from the intestine of the diving beetles Cybister lewisianus and Cybister brevis, were characterized as three novel species using a polyphasic approach. The isolates were Gram-staining-positive, strictly aerobic, non-motile, and rod-shaped. They grew optimally at 30°C (pH 7) in the presence of 0.5% (wt/vol) NaCl. Phylogenetic analysis based on the 16S rRNA gene sequences revealed that they belong to the genus Leucobacter and are closely related to L. denitrificans M1T8B10T (98.4–98.7% sequence similarity). Average nucleotide identity (ANI) values among the isolates were 76.4–84.1%. ANI values for the isolates and the closest taxonomic species, L. denitrificans KACC 14055T, were 72.3–73.1%. The isolates showed ANI values of < 76.5% with all analyzable Leucobacter strains in the EzBioCloud database. The genomic DNA G + C content of the isolates was 60.3–62.5%. The polar lipid components were phosphatidylglycerol, diphosphatidylglycerol, and other unidentified glycolipids, phospholipids, and lipids. The major cellular fatty acids were anteiso-C15:0, iso-C16:0, and anteiso-C17:0. MK-10 was the major respiratory quinone, and MK-7 and MK-11 were the minor respiratory quinones. The whole-cell sugar components of the isolates were ribose, glucose, galactose, and mannose. The isolates harbored l-2,4-diaminobutyric acid, l-serine, l-lysine, l-aspartic acid, glycine, and d-glutamic acid within the cell wall peptidoglycan. Based on phylogenetic, phenotypic, chemotaxonomic, and genotypic analyses, strains HDW9AT, HDW9BT, and HDW9CT represent three novel species within the genus Leucobacter. We propose the name Leucobacter coleopterorum sp. nov. for strain HDW9AT (= KACC 21331T = KCTC 49317T = JCM 33667T), the name Leucobacter insecticola sp. nov. for strain HDW9BT (= KACC 21332T = KCTC 49318T = JCM 33668T), and the name Leucobacter viscericola sp. nov. for strain HDW9CT (= KACC 21333T = KCTC 49319T = JCM 33669T).

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

Similar content being viewed by others

References

  • Benga, L., Spröer, C., Schumann, P., Verbarg, S., Bunk, B., Engelhardt, E., Benten, W.P.M., and Sager, M. 2019. Leucobacter muris sp. nov., isolated from the nose of a laboratory mouse. Int. J. Syst. Evol. Microbiol. 69, 2095–2100.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Chakraborty, S., Rene, E.R., and Lens, P.N.L. 2019. Reduction of selenite to elemental Se(0) with simultaneous degradation of phenol by co-cultures of Phanerochaete chrysosporium and Delftia lacustris. J. Microbiol. 57, 738–747.

    Article  CAS  PubMed  Google Scholar 

  • Chen, I.M.A., Chu, K., Palaniappan, K., Pillay, M., Ratner, A., Huang, J., Huntemann, M., Varghese, N., White, J.R., Seshadri, R., et al. 2019. IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes. Nucleic Acids Res. 47, D666–D677.

    Article  CAS  PubMed  Google Scholar 

  • Chun, B.H., Lee, H.J., Jeong, S.E., Schumann, P., and Jeon, C.O. 2017. Leucobacter ruminantium sp. nov., isolated from the bovine rumen. Int. J. Syst. Evol. Microbiol. 67, 2634–2639.

    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 

  • Das, S., Dash, H.R., and Chakraborty, J. 2016. Genetic basis and importance of metal resistant genes in bacteria for bioremediation of contaminated environments with toxic metal pollutants. Appl. Microbiol. Biotechnol. 100, 2967–2984.

    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. Zool. 20, 406–416.

    Article  Google Scholar 

  • Goszczynska, T. and Serfontein, J. 1998. Milk-Tween agar, a semiselective 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 

  • Hou, S.Y., Wang, F., Zhang, M.Y., Cheng, J., and Zhang, Y.X. 2018. A novel pigmented and heavy metal biosorptive bacterium, Leucobacter epilobiisoli sp. nov., isolated from rhizosphere soil of Epilobium hirsutum L. Antonie van Leeuwenhoek 111, 1825–1833.

    Article  CAS  PubMed  Google Scholar 

  • Kang, C.H., Kwon, Y.J., and So, J.S. 2016. Bioremediation of heavy metals by using bacterial mixtures. Ecol. Eng. 89, 64–69.

    Article  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 

  • Lai, W.A., Lin, S.Y., Hameed, A., Hsu, Y.H., Liu, Y.C., Huang, H.R., Shen, F.T., and Young, C.C. 2015. Leucobacter zeae sp. nov., isolated from the rhizosphere of maize (Zea mays L.). Int. J. Syst. Evol. Microbiol. 65, 4734–4742.

    Article  CAS  PubMed  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, I., Kim, Y.O., 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., Huang, S., and Zhang, Y. 2016. Cr(VI) removal from aqueous solution by thermophilic denitrifying bacterium Chelatococcus daeguensis TAD1 in the presence of single and multiple heavy metals. J. Microbiol. 54, 602–610.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y., Fang, W., Xie, S., Yang, X., and Wang, L. 2017. Leucobacter corticis sp. nov., isolated from symptomatic bark of Populus × euramericana canker. Int. J. Syst. Evol. Microbiol. 67, 2248–2252.

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Morais, P.V., Paulo, C., Francisco, R., Branco, R., Paula Chung, A., and da Costa, M.S. 2006. Leucobacter luti sp. nov., and Leucobacter alluvii sp. nov., two new species of the genus Leucobacter isolated under chromium stress. Syst. Appl. Microbiol. 29, 414–421.

    Article  CAS  PubMed  Google Scholar 

  • Na, S.I., Kim, Y.O., Yoon, S.H., Ha, S.M., 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 

  • Qu, Y., Li, H., Li, A., Ma, F., and Zhou, J. 2011. Identification and characterization of Leucobacter sp. N-4 for Ni (II) biosorption by response surface methodology. J. Hazard. Mater. 190, 869–875.

    Article  CAS  PubMed  Google Scholar 

  • Ryan, R.P., Monchy, S., Cardinale, M., Taghavi, S., Crossman, L., Avison, M.B., Berg, G., van der Lelie, D., and Dow, J.M. 2009. The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat. Rev. Microbiol. 7, 514–525.

    Article  CAS  PubMed  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 

  • Schumann, P. and Pukall, R. 2017. Leucobacter weissii sp. nov., an isolate from activated sludge once described as first representative of the peptidoglycan variation B2δ, and emended description of the genus Leucobacter. Int. J. Syst. Evol. Microbiol. 67, 5244–5251.

    Article  CAS  PubMed  Google Scholar 

  • Shin, N.R., Kim, M.S., Jung, M.J., Roh, S.W., Nam, Y.D., Park, E.J., and Bae, J.W. 2011. Leucobacter celer sp. nov., isolated from Korean fermented seafood. Int. J. Syst. Evol. Microbiol. 61, 2353–2357.

    Article  CAS  PubMed  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 

  • Sturm, G., Jacobs, J., Spröer, C., Schumann, P., and Gescher, J. 2011. Leucobacter chromiiresistens sp. nov., a chromate-resistant strain. Int. J. Syst. Evol. Microbiol. 61, 956–960.

    Article  CAS  PubMed  Google Scholar 

  • Sun, L.N., Pan, D.D., Wu, X.W., Yang, E.D., Hua, R.M., and Li, Q.X. 2018. Leucobacter triazinivorans sp. nov., a s-triazine herbicide prometryn-degrading bacterium isolated from sludge. Int. J. Syst. Evol. Microbiol. 68, 204–210.

    Article  CAS  PubMed  Google Scholar 

  • Takeuchi, M., Weiss, N., Schumann, P., and Yokota, A. 1996. Leucobacter komagatae gen. nov., sp. nov., a new aerobic Gram-positive, nonsporulating rod with 2,4-diaminobutyric acid in the cell wall. Int. J. Syst. Bacteriol. 46, 967–971.

    Article  CAS  PubMed  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 

  • 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 

  • Wadgaonkar, S.L., Nancharaiah, Y.V., Jacob, C., Esposito, G., and Lens, P.N.L. 2019. Microbial transformation of Se oxyanions in cultures of Delftia lacustris grown under aerobic conditions. J. Microbiol. 57, 362–371.

    Article  CAS  PubMed  Google Scholar 

  • Weon, H.Y., Anandham, R., Tamura, T., Hamada, M., Kim, S.J., Kim, Y.S., Suzuki, K., and Kwon, S.W. 2012. Leucobacter denitrificans sp. nov., isolated from cow dung. J. Microbiol. 50, 161–165.

    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 

  • Yi, Y.J., Lim, J.M., Gu, S., Lee, W.K., Oh, E., Lee, S.M., and Oh, B.T. 2017. Potential use of lactic acid bacteria Leuconostoc mesenteroides as a probiotic for the removal of Pb(II) toxicity. J. Microbiol. 55, 296–303.

    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 

  • Yun, J.H., Cho, Y.J., Chun, J., Hyun, D.W., and Bae, J.W. 2014. Genome sequence of the chromate-resistant bacterium Leucobacter salsicius type strain M1-8T. Stand. Genomic Sci. 9, 495–504.

    Article  PubMed  Google Scholar 

  • Yun, J.H., Roh, S.W., Kim, M.S., Jung, M.J., Park, E.J., Shin, K.S., Nam, Y.D., and Bae, J.W. 2011. Leucobacter salsicius sp. nov., from a salt-fermented food. Int. J. Syst. Evol. Microbiol. 61, 502–506.

    Article  CAS  PubMed  Google Scholar 

  • Zhu, D., Zhang, P., Li, P., Wu, J., Xie, C., Sun, J., and Niu, L. 2016. Description of Leucobacter holotrichiae sp. nov., isolated from the gut of Holotrichia oblita larvae. Int. J. Syst. Evol. Microbiol. 66, 1857–1861.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

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 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

  1. Department of Biology and Department of Biomedical and Pharmaceutical Sciences, Kyung Hee University, Seoul, 02447, Republic of Korea

    Dong-Wook Hyun, Hojun Sung, Pil Soo Kim, Ji-Hyun Yun & Jin-Woo Bae

Authors
  1. Dong-Wook Hyun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hojun Sung
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pil Soo Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ji-Hyun Yun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jin-Woo Bae
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jin-Woo Bae.

Ethics declarations

Conflicts 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 number: KHUASP(SE)-18-048) and complied with 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., Sung, H., Kim, P.S. et al. Leucobacter coleopterorum sp. nov., Leucobacter insecticola sp. nov., and Leucobacter viscericola sp. nov., isolated from the intestine of the diving beetles, Cybister brevis and Cybister lewisianus, and emended description of the genus Leucobacter. J Microbiol. 59, 360–368 (2021). https://doi.org/10.1007/s12275-021-0472-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-021-0472-6

Keywords

Search

Navigation