Abstract
A polyphasic taxonomic approach was used to characterize two novel bacterial strains, HDW17AT and HDW17BT, isolated from the intestine of the diving beetle Cybister lewisianus, and the dark diving beetle Hydrophilus acuminatus, respectively. Both strains were Gram-positive and facultative anaerobic cocci forming cream-colored colonies. The isolates grew optimally at 25°C, pH 7, in the presence of 0.3% (wt/vol) NaCl. Phylogenetic analysis based on 16S rRNA gene sequences and genome sequences showed that the isolates were members of the genus Vagococcus, and strain HDW17AT was closely related to Vagococcus fessus CCUG 41755T (98.9% of 16S rRNA gene sequence similarity and 74.3% of average nucleotide identity [ANI]), whereas strain HDW17BT was closely related to Vagococcus fluvialis NCFB 2497T (98.9% of 16S rRNA gene sequence similarity and 76.6% of ANI). Both strains contained C16:0, and C18:1ω9c as the major cellular fatty acids, but C16:1ω9c was also observed only in strain HDW17BT as the major cellular fatty acid. The respiratory quinone of the isolates was MK-7. The major polar lipid components were phosphatidylglycerol, phosphatidylethanolamine, and diphosphatidylglycerol. The genomic DNA G + C content of strains HDW17AT and HDW17BT were 36.6 and 34.4%, respectively. Both strains had cell wall peptidoglycan composed of the amino acids l-alanine, glycine, d-glutamic acid, l-tryptophan, l-lysine, and l-aspartic acid, and the sugars ribose, glucose, and galactose. Based on phylogenetic, phenotypic, chemotaxonomic, and genotypic analyses, strains HDW17AT and HDW17BT represent two novel species in the genus Vagococcus. We propose the name Vagococcus coleopterorum sp. nov. for strain HDW17AT (= KACC 21348T = KCTC 49324T = JCM 33674T) and the name Vagococcus hydrophili sp. nov. for strain HDW17BT (= KACC 21349T = KCTC 49325T = JCM 33675T).
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29 March 2021
An Erratum to this paper has been published: https://doi.org/10.1007/s12275-021-0697-4
References
Altintas, I., Andrews, V., and Larsen, M.V. 2020. First reported human bloodstream infection with Vagococcus lutrae. New Microbes New Infect. 34, 100649.
Ben Ami, E., Yuval, B., and Jurkevitch, E. 2010. Manipulation of the microbiota of mass-reared Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae) improves sterile male sexual performance. ISME J. 4, 28–37.
Benson, H. 1994. Microbiological application. Laboratory manual in General Microbiology. Wan C. Publishers, Dubuque, USA.
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.
Ceja-Navarro, J.A., Karaoz, U., Bill, M., Hao, Z., White, R.A., Arellano, A., Ramanculova, L., Filley, T.R., Berry, T.D., Conrad, M.E., et al. 2019. Gut anatomical properties and microbial functional assembly promote lignocellulose deconstruction and colony subsistence of a wood-feeding beetle. Nat. Microbiol. 4, 864–875.
Chen, I.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.
Cho, B.C., Hardies, S.C., Jang, G.I., and Hwang, C.Y. 2018. Complete genome of streamlined marine actinobacterium Pontimonas salivibrio strain CL-TW6T adapted to coastal planktonic lifestyle. BMC Genomics 19, 625.
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.
Collins, M.D., Ash, C., Farrow, J.A., Wallbanks, S., and Williams, A.M. 1989. 16S ribosomal ribonucleic acid sequence analyses of lactococci and related taxa. Description of Vagococcus fluvialis gen. nov., sp. nov. J. Appl. Bacteriol. 67, 453–460.
Collins, M.D. and Jones, D. 1981. Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implication. Microbiol. Rev. 45, 316.
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.
Crowson, R.A. 2013. The Biology of the Coleoptera. Academic Press, Messachusatts, USA.
Engel, P. and Moran, N.A. 2013. The gut microbiota of insects — diversity in structure and function. FEMS Microbiol. Rev. 37, 699–735.
Felsenstein, J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17, 368–376.
Fitch, W.M. 1971. Toward defining the course of evolution: minimum change for a specific tree topology. Syst. Biol. 20, 406–416.
Ge, Y., Yang, J., Lai, X.H., Zhang, G., Jin, D., Lu, S., Wang, B., Huang, Y., Huang, Y., Ren, Z., et al. 2020. Vagococcus xieshaowenii sp. nov., isolated from snow finch (Montifringilla taczanowskii) cloacal content. Int. J. Syst. Evol. Microbiol. 70, 2493–2498.
Giovannoni, S.J., Cameron Thrash, J., and Temperton, B. 2014. Implications of streamlining theory for microbial ecology. ISME J. 8, 1553–1565.
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.
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 (MALDITOF MS) systems. Ann. Lab Med. 39, 530–536.
Habineza, P., Muhammad, A., Ji, T., Xiao, R., Yin, X., Hou, Y., and Shi, Z. 2019. The promoting effect of gut microbiota on growth and development of Red Palm Weevil, Rhynchophorus ferrugineus (Olivier) (Coleoptera: Dryophthoridae) by modulating its nutritional metabolism. Front. Microbiol. 10, 1212.
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.
Hoyles, L., Lawson, P.A., Foster, G., Falsen, E., Ohlén, M., Grainger, J.M., and Collins, M.D. 2000. Vagococcus fessus sp. nov., isolated from a seal and a harbour porpoise. Int. J. Syst. Evol. Microbiol. 50, 1151–1154.
Jadhav, K.P. and Pai, P.G. 2019. A rare infective endocarditis caused by Vagococcus fluvialis. J. Cardiol. Cases 20, 129–131.
Jaffrès, E., Prévost, H., Rossero, A., Joffraud, J.J., and Dousset, X. 2010. Vagococcus penaei sp. nov., isolated from spoilage microbiota of cooked shrimp (Penaeus vannamei). Int. J. Syst. Evol. Microbiol. 60, 2159–2164.
Killer, J., Švec, P., Sedláćek, I., Černohlávková, J., Benada, O., Hroncová, Z., Havlík, J., Vlková, E., Rada, V., Kopečny, J., et al. 2014. Vagococcus entomophilus sp. nov., from the digestive tract of a wasp (Vespula vulgaris). Int. J. Syst. Evol. Microbiol. 64, 731–737.
Kim, S.B. 2014. Korean red list of threatened species, 2nd edn. National Institute of Biological Resources, Incheon, Republic of Korea.
Kim, S., Park, M.S., Song, J., Kang, I., and Cho, J.C. 2020. High-throughput cultivation based on dilution-to-extinction with catalase supplementation and a case study of cultivating acI bacteria from Lake Soyang. J. Microbiol. 58, 893–905.
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.
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.
Lawson, P.A., Falsen, E., Cotta, M.A., and Whitehead, T.R. 2007. Vagococcus elongatus sp. nov., isolated from a swine-manure storage pit. Int. J. Syst. Evol. Microbiol. 57, 751–754.
Lawson, P.A., Foster, G., Falsen, E., Ohlén, M., and Collins, M.D. 1999. Vagococcus lutrae sp. nov., isolated from the common otter (Lutra lutra). Int. J. Syst. Bacteriol. 49, 1251–1254.
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.
Matsuo, T., Mori, N., Kawai, F., Sakurai, A., Toyoda, M., Mikami, Y., Uehara, Y., and Furukawa, K. 2020. Vagococcus fluvialis as a causative pathogen of bloodstream and decubitus ulcer infection: Case report and systematic review of the literature. J. Infect. Chemother. doi: https://doi.org/10.1016/j.jiac.2020.09.019.
MIDI. 1999. Sherlock Microbial Identification System Operating Manual, version 3.0. MIDI, Inc., Newark, Delaware, USA.
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.
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.
Román, L., Acosta, F., Padilla, D., El Aamri, F., Bravo, J., Vega, B., Rodriguez, E., Vega, J., Déniz, S., and Real, F. 2015. The in vitro immunomodulatory effect of extracellular products (ECPs) of Vagococcus fluvialis L21 on European sea bass (Dicentrarchus labrax) leucocytes. Fish Shellfish Immunol. 42, 517–521.
Ryu, J.H., Ha, E.M., and Lee, W.J. 2010. Innate immunity and gut-microbe mutualism in Drosophila. Dev. Comp. Immunol. 34, 369–376.
Saitou, N. and Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425.
Sasser, M. 1990. Identification of bacteria by gas chromatography of cellular fatty acids. MIDI Technical Note 101. MIDI Inc., Newark, Delaware, USA.
Sato, S., Inoda, T., Niitsu, S., Kubota, S., Goto, Y., and Kobayashi, Y. 2017. Asymmetric larval head and mandibles of Hydrophilus acuminatus (Insecta: Coleoptera, Hydrophilidae): Fine structure and embryonic development. Arthropod. Struct. Dev. 46, 824–842.
Schleifer, K.H. and Kandler, O. 1972. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36, 407–477.
Shewmaker, P.L., Steigerwalt, A.G., Morey, R.E., Carvalho, M.G.S., Elliott, J.A., Joyce, K., Barrett, T.J., Teixeira, L.M., and Facklam, R.R. 2004. Vagococcus carniphilus sp. nov., isolated from ground beef. Int. J. Syst. Evol. Microbiol. 54, 1505–1510.
Shewmaker, P.L., Whitney, A.M., Gulvik, C.A., Humrighouse, B.W., Gartin, J., Moura, H., Barr, J.R., Moore, E.R.B., Karlsson, R., Pinto, T.C.A., et al. 2019. Vagococcus bubulae sp. nov., isolated from ground beef, and Vagococcus vulneris sp. nov., isolated from a human foot wound. Int. J. Syst. Evol. Microbiol. 69, 2268–2276.
Sorroza, L., Padilla, D., Acosta, F., Román, L., Grasso, V., Vega, J., and Real, F. 2012. Characterization of the probiotic strain Vagococcus fluvialis in the protection of European sea bass (Dicentrarchus labrax) against vibriosis by Vibrio anguillarum. Vet. Microbiol. 155, 369–373.
Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
Standish, I., Erickson, S., Leis, E., Baumgartner, W., Loch, T., Knupp, C., McCann, R., Puzach, C., Katona, R., Lark, E., et al. 2020. Vagococcus salmoninarum I-A chronic coldwater streptococcosis in broodstock brook trout (Salvelinus fontinalis) in Wisconsin, USA. J. Fish Dis. 43, 305–316.
Sundararaman, A., Srinivasan, S., and Lee, S.S. 2017. Vagococcus humatus sp. nov., isolated from soil beneath a decomposing pig carcass. Int. J. Syst. Evol. Microbiol. 67, 330–335.
Tak, E.J., Kim, H.S., Lee, J.Y., Kang, W., Hyun, D.W., Kim, P.S., Shin, N.R., and Bae, J.W. 2017. Vagococcus martis sp. nov., isolated from the small intestine of a marten, Martes flavigula. Int. J. Syst. Evol. Microbiol. 67, 3398–3402.
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.
Tindall, B.J. 1990. Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol. Lett. 66, 199–202.
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.
Tong, Q., Cui, L.Y., Du, X.P., Hu, Z.F., Bie, J., Xiao, J.H., Wang, H.B., and Zhang, J.T. 2020. Comparison of gut microbiota diversity and predicted functions between healthy and diseased captive Rana dybowskii. Front. Microbiol. 11, 2096.
Wallbanks, S., Martinez-Murcia, A.J., Fryer, J.L., Phillips, B.A., and Collins, M.D. 1990. 16S rRNA sequence determination for members of the genus Carnobacterium and related lactic acid bacteria and description of Vagococcus salmoninarum sp. nov. Int. J. Syst. Bacteriol. 40, 224–230.
Wang, L., Cui, Y.S., Kwon, C.S., Lee, S.T., Lee, J.S., and Im, W.T. 2011. Vagococcus acidifermentans sp. nov., isolated from an acidogenic fermentation bioreactor. Int. J. Syst. Evol. Microbiol. 61, 1123–1126.
Wilm, A., Higgins, D.G., and Notredame, C. 2008. R-Coffee: a method for multiple alignment of non-coding RNA. Nucleic Acids Res. 36, e52.
Woo, S., Song, I., and Cha, H.J. 2020. Fast and facile biodegradation of polystyrene by the gut microbial flora of Plesiophthalmus davidis larvae. Appl. Environ. Microbiol. 86, e01361–20.
Wu, Y.C., Lin, S.T., Guu, J.R., Tamura, T., Mori, K., Wang, L.T., Huang, L., and Watanabe, K. 2020. Vagococcus silagei sp. nov., isolated from brewer’s grain used to make silage in Taiwan. Int. J. Syst. Evol. Microbiol. 70, 1953–1960.
Wullschleger, S., Jans, C., Seifert, C., Baumgartner, S., Lacroix, C., Bonfoh, B., Stevens, M.J.A., and Meile, L. 2018. Vagococcus teuberi sp. nov., isolated from the Malian artisanal sour milk fènè. Syst. Appl. Microbiol. 41, 65–72.
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.
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.
Yun, J.H., Roh, S.W., Whon, T.W., Jung, M.J., Kim, M.S., Park, D.S., Yoon, C., Nam, Y.D., Kim, Y.J., Choi, J.H., et al. 2014. Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Appl. Environ. Microbiol. 80, 5254–5264.
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 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 (NIBR2018-01106), funded by the Ministry of Environment of Korea (MOE).
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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.
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Hyun, DW., Tak, E.J., Kim, P.S. et al. 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 (2021). https://doi.org/10.1007/s12275-021-0485-1
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DOI: https://doi.org/10.1007/s12275-021-0485-1