Skip to main content
Log in

Description of Ornithinimicrobium ciconiae sp. nov., and Ornithinimicrobium avium sp. nov., isolated from the faeces of the endangered and near-threatened birds

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

Abstract

Phenotypic and genomic analyses were performed to characterize two novel species, H23M54T and AMA3305T, isolated from the faeces of the Oriental stork (Ciconia boyciana) and the cinereous vulture (Aegypius monachus), respectively. Strains H23M54T and AMA3305T showed the highest similarities of 16S rRNA gene sequences and complete genome sequences with Ornithinimicrobium cavernae CFH 30183T (98.5% of 16S rRNA gene sequence similarity and 82.1% of average nucleotide identity, ANI) and O. pekingense DSM 21552T (98.5% of 16S rRNA gene sequence similarity and 82.3% of ANI), respectively. Both strains were Gram-stain-positive, obligate aerobes, non-motile, non-spore-forming, and coccoid- and rodshaped. Strain H23M54T grew optimally at 25–30°C and pH 8.0 and in the presence of 1.5–2% (wt/vol) NaCl, while strain AMA3305T grew optimally at 30°C and pH 7.0 and in the presence of 1–3% (wt/vol) NaCl. Both strains had iso-C15:0, iso-C16:0, and summed feature 9 (iso-C17:1ω9c and/or C16:0 10-methyl) as major cellular fatty acids. MK-8 (H4) was identified as the primary respiratory quinone in both strains. Strains H23M54T and AMA3305T possessed diphosphatidylglycerol and phosphatidylglycerol as major polar lipids. Moreover, strains H23M54T and AMA3305T commonly contained ribose and glucose as major sugars and l-ornithine, l-alanine, glycine, and aspartic acid as major amino acids. The polyphasic taxonomic data indicate that strains H23M54T and AMA3305T represent novel species of the genus Ornithinimicrobium. We propose the names Ornithinimicrobium ciconiae sp. nov. and Ornithinimicrobium avium sp. nov. for strains H23M54T (= KCTC 49151T = JCM 33221T) and AMA3305T (= KCTC 49180T = JCM 32873T), respectively.

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

  • Arkin, A.P., Cottingham, R.W., Henry, C.S., Harris, N.L., Stevens, R.L., Maslov, S., Dehal, P., Ware, D., Perez, F., Canon, S., et al. 2018. KBase: the United States department of energy systems biology knowledgebase. Nat. Biotechnol. 36, 566–569.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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  CAS  Google Scholar 

  • Barco, R.A., Garrity, G.M., Scott, J.J., Amend, J.P., Nealson, K.H., and Emerson, D. 2020. A genus definition for Bacteria and Archaea based on a standard genome relatedness index. mBio 11, e02475–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benson, H.J. 1973. Microbiological Applications: A Laboratory Manual in General Microbiology. 2nd edn, WC Brown, Dubuque, Iowa, USA.

    Google Scholar 

  • BirdLife International. 2018a. Aegypius monachus. The IUCN Red List of Threatened Species 2018: e.T22695231A131935194. https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22695231A131935194.en.

  • BirdLife International. 2018b. Ciconia boyciana. The IUCN Red List of Threatened Species 2018: e.T22697695A131942061. https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22697695A131942061.en.

  • Blumstein, D.T., Rangchi, T.N., Briggs, T., De Andrade, F.S., and Natterson-Horowitz, B. 2017. A systematic review of carrion eaters’ adaptations to avoid sickness. J. Wildl. Dis. 53, 577–581.

    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 

  • 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. Nat. 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. 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 

  • Fang, X.M., Du, H.J., Bai, J.L., He, W.N., Li, J., Wang, H., Su, J., Liu, H.Y., Zhang, Y.Q., and Yu, L.Y. 2020. Ornithinimicrobium cerasi sp. nov., isolated from the fruit of Cerasus pseudocerasus and emended description of the genus Ornithinimicrobium. Int. J. Syst. Evol. Microbiol. 70, 1691–1697.

    Article  CAS  PubMed  Google Scholar 

  • Fang, X.M., Yan, D., Bai, J.L., Su, J., Liu, H.Y., Ma, B.P., Zhang, Y.Q., and Yu, L.Y. 2017. Ornithinimicrobium flavum sp. nov., isolated from the leaf of Paris polyphylla. Int. J. Syst. Evol. Microbiol. 67, 4541–4545.

    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 

  • Fischer, S., Brunk, B.P., Chen, F., Gao, X., Harb, O.S., Iodice, J.B., Shanmugam, D., Roos, D.S., and Stoeckert, C.J.Jr. 2011. Using OrthoMCL to assign proteins to OrthoMCL-DB groups or to cluster proteomes into new ortholog groups. Curr. Protoc. Bioinformatics 35, 6.12.1-6.12.19.

    Article  Google Scholar 

  • Groth, I., Schumann, P., Weiss, N., Schuetze, B., Augsten, K., and Stackebrandt, E. 2001. Ornithinimicrobium humiphilum gen. nov., sp. nov., a novel soil actinomycete with L-ornithine in the peptidoglycan. Int. J. Syst. Evol. Microbiol. 51, 81–87.

    Article  CAS  PubMed  Google Scholar 

  • Guo, Q., Wang, B., Zhou, Z., Ke, X., Zhang, L., Chen, M., Lin, M., Wang, W., Zhang, W., and Li, X. 2020. Ornithinimicrobium pratense sp. nov., isolated from meadow soil. Int. J. Syst. Evol. Microbiol. 70, 6450–6457.

    Article  CAS  PubMed  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 

  • Kämpfer, P., Glaeser, S., Schäfer, J., Lodders, N., Martin, K., and Schumann, P. 2013. Ornithinimicrobium murale sp. nov., isolated from an indoor wall colonized by moulds. Int. J. Syst. Evol. Microbiol. 63, 119–123.

    Article  PubMed  CAS  Google Scholar 

  • Kim, D., Park, S., and Chun, J. 2021. Introducing EzAAI: a pipeline for high throughput calculations of prokaryotic average amino acid identity. J. Microbiol. 59, 476–480.

    Article  PubMed  CAS  Google Scholar 

  • Kluge, A.G. and Farris, J.S. 1969. Quantitative phyletics and the evolution of anurans. Syst. Biol. 18, 1–32.

    Article  Google Scholar 

  • Komagata, K. and Suzuki, K.I. 1988. 4 Lipid and cell-wall analysis in bacterial systematics. Methods Microbiol. 19, 161–207.

    Article  Google Scholar 

  • Konstantinidis, K.T. and Tiedje, J.M. 2005. Genomic insights that advance the species definition for prokaryotes. Proc. Natl. Acad. Sci. USA 102, 2567–2572.

    Article  CAS  PubMed  PubMed Central  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 Stackebrandt, E. and Goodfellow, M. (eds.), Nucleic acid techniques in bacterial systematics, pp. 115–175. John Wiley and Sons, New York, USA.

    Google Scholar 

  • Lee, S.Y., Kang, W., Kim, P.S., Kim, H.S., Sung, H., Shin, N.R., Whon, T.W., Yun, J.H., Lee, J.Y., Lee, J.Y., et al. 2019. Undibacterium piscinae sp. nov., isolated from Korean shiner intestine. Int. J. Syst. Evol. Microbiol. 69, 3148–3154.

    Article  CAS  PubMed  Google Scholar 

  • Lee, S.Y., Kang, W., Kim, P.S., Kim, H.S., Sung, H., Shin, N.R., Yun, J.H., Lee, J.Y., Lee, J.Y., Jung, M.J., et al. 2020. Jeotgalibaca ciconiae sp. nov., isolated from the faeces of an Oriental stork. Int. J. Syst. Evol. Microbiol. 70, 3247–3254.

    Article  CAS  PubMed  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 

  • Liu, L.Z., Liu, Y., Chen, Z., Liu, H.C., Zhou, Y.G., and Liu, Z.P. 2013. Ornithinimicrobium tianjinense sp. nov., isolated from a recirculating aquaculture system. Int. J. Syst. Evol. Microbiol. 63, 4489–4494.

    Article  CAS  PubMed  Google Scholar 

  • Liu, X.Y., Wang, B.J., Jiang, C.Y., and Liu, S.J. 2008. Ornithinimicrobium pekingense sp. nov., isolated from activated sludge. Int. J. Syst. Evol. Microbiol. 58, 116–119.

    Article  CAS  PubMed  Google Scholar 

  • Luo, C., Rodriguez-R, L.M., and Konstantinidis, K.T. 2014. MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences. Nucleic Acids Res. 42, e73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayilraj, S., Saha, P., Suresh, K., and Saini, H. 2006. Ornithinimicrobium kibberense sp. nov., isolated from the Indian Himalayas. Int. J. Syst. Evol. Microbiol. 56, 1657–1661.

    Article  CAS  PubMed  Google Scholar 

  • Meier-Kolthoff, J.P., Auch, A.F., Klenk, H.P., and Göker, M. 2013. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14, 60.

    Article  PubMed  PubMed Central  Google Scholar 

  • Minnikin, D.E., O’donnell, A.G., Goodfellow, M., Alderson, G., Athalye, M., Schaal, A., and Parlett, J.H. 1984. An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J. Microbiol. Methods 2, 233–241.

    Article  CAS  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 

  • Naito, K., Sagawa, S., and Ohsako, Y. 2014. Using the oriental white stork as an indicator species for farmland restoration. In Usio, N., and Miyashita, T. (eds), Social-ecological restoration in paddydominated landscapes. Ecological Research Monographs pp. 123–138. Springer, Tokyo, Japan.

    Chapter  Google Scholar 

  • Nouioui, I., Carro, L., García-López, M., Meier-Kolthoff, J.P., Woyke, T., Kyrpides, N.C., Pukall, R., Klenk, H.P., Goodfellow, M., and Göker, M. 2018. Genome-based taxonomic classification of the phylum Actinobacteria. Front. Microbiol. 9, 2007.

    Article  PubMed  PubMed Central  Google Scholar 

  • Park, W. 2018. Gut microbiomes and their metabolites shape human and animal health. J. Microbiol. 56, 151–153.

    Article  PubMed  Google Scholar 

  • Partridge, S. 1949. Aniline hydrogen phthalate as a spraying reagent for chromatography of sugars. Nature 164, 443.

    Article  CAS  PubMed  Google Scholar 

  • Price, M.N., Dehal, P.S., and Arkin, A.P. 2009. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26, 1641–1650.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramaprasad, E., Sasikala, C., and Ramana, C.V. 2015. Ornithinimicrobium algicola sp. nov., a marine actinobacterium isolated from the green alga of the genus Ulva. Int. J. Syst. Evol. Microbiol. 65, 4627–4631.

    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 

  • Salam, N., Jiao, J.Y., Zhang, X.T., and Li, W.J. 2020. Update on the classification of higher ranks in the phylum Actinobacteria. Int. J. Syst. Evol. Microbiol. 70, 1331–1355.

    Article  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 

  • Schaeffer, A.B. and Fulton, M.D. 1933. A simplified method of staining endospores. Science 77, 194.

    Article  CAS  PubMed  Google Scholar 

  • Sekercioglu, C.H. 2006. Increasing awareness of avian ecological function. Trends Ecol Evol. 21, 464–471.

    Article  PubMed  Google Scholar 

  • Sittipo, P., Lobionda, S., Lee, Y.K., and Maynard, C.L. 2018. Intestinal microbiota and the immune system in metabolic diseases. J. Microbiol. 56, 154–162.

    Article  CAS  PubMed  Google Scholar 

  • Skinnider, M.A., Johnston, C.W., Gunabalasingam, M., Merwin, N.J., Kieliszek, A.M., MacLellan, R.J., Li, H., Ranieri, M.R.M., Webster, A.L.H., Cao, M.P.T., et al. 2020. Comprehensive prediction of secondary metabolite structure and biological activity from microbial genome sequences. Nat. Commun. 11, 6058.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Staneck, J.L. and Roberts, G.D. 1974. Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl. Microbiol. 28, 226–231.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tawa, K. and Sagawa, S.J. 2021. Stable isotopic analysis of stuffed specimens revealed the feeding habits of oriental storks Ciconia boyciana in Japan before their extinction in the wild. J. Ornithol. 162, 193–206.

    Article  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 

  • Varghese, N.J., Mukherjee, S., Ivanova, N., Konstantinidis, K.T., Mavrommatis, K., Kyrpides, N.C., and Pati, A. 2015. Microbial species delineation using whole genome sequences. Nucleic Acids Res. 43, 6761–6771.

    Article  CAS  PubMed  PubMed Central  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, M.Y., Lee, K., and Yoon, S.S. 2014. Protective role of gut commensal microbes against intestinal infections. J. Microbiol. 52, 983–989.

    Article  PubMed  Google Scholar 

  • Zhang, L.Y., Ming, H., Meng, X.L., Fang, B.Z., Jiao, J.Y., Salam, N., Zhang, X.T., Li, W.J., and Nie, G.X. 2019. Ornithinimicrobium cavernae sp. nov., an actinobacterium isolated from a karst cave. Antonie van Leeuwenhoek 112, 179–186.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, H., Yohe, T., Huang, L., Entwistle, S., Wu, P., Yang, Z., Busk, P.K., Xu, Y., and Yin, Y. 2018. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 46, W95–W101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful for the etymological advice given by Dr. Aharon Oren (The Hebrew University of Jerusalem, Israel). This work was supported by grants from the Mid-Career Researcher Program (NRF-2020R1A2C3012797) through the National Research Foundation of Korea (NRF) and the National Institute of Biological Resources (NIBR201801106) funded by the Ministry of Environment of Korea (MOE). This work was also supported by the NRF grant funded by the Korean government (MSIT) (No. NRF-2018R1A5A1025077).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jin-Woo Bae.

Additional information

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

Conflict of Interest

The authors declare that there are no conflicts of interest.

Ethical Statements

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 the guidelines of the Committee.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, SY., Sung, H., Kim, P.S. et al. Description of Ornithinimicrobium ciconiae sp. nov., and Ornithinimicrobium avium sp. nov., isolated from the faeces of the endangered and near-threatened birds. J Microbiol. 59, 978–987 (2021). https://doi.org/10.1007/s12275-021-1323-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-021-1323-1

Keywords

Navigation