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Journal of Microbiology

, Volume 57, Issue 9, pp 725–731 | Cite as

Aeromicrobium endophyticum sp. nov., an endophytic actinobacterium isolated from reed (Phragmites australis)

  • Fei-Na Li
  • Shui-Lin Liao
  • Shao-Wei Liu
  • Tao Jin
  • Cheng-Hang SunEmail author
Microbial Systematics and Evolutionary Microbiology

Abstract

A Gram-staining-positive, motile and short-rod-shaped actinobacterium designated 9W16Y-2T was isolated from surface-sterilized leaves of reed (Phragmites australis) collected from Taklamakan Desert in Xinjiang Uygur Autonomous Region, China. Colonies were pale greenish yellow, circular, smooth, and convex. The 16S rRNA gene sequence of strain 9W16Y-2T exhibited highest sequence similarities with Aeromicrobium camelliae CGMCC 1.12942T (99.0%) and Aeromicrobium erythreum NRRL B-3381T (97.2%). Phylogenetic analyses based on 16S rRNA gene sequences and single-copy phylogenetic marker genes (pMGs) showed that strain 9W16Y-2T belonged to the genus Aeromicrobium and formed a monophyletic clade with Aeromicrobium camelliae CGMCC 1.12942T. Furthermore, average nucleotide identity (ANI) and DNA-DNA hybridization (DDH) clearly separated strain 9W16Y-2T from the other species of the genus Aeromicrobium with values below the thresholds for species delineation. The G+C content of the genomic DNA is 68.9 mol%. The diagnostic diamino acid of the cell-wall peptidoglycan was ll-diaminopimelic acid. The predominant menaquinone was MK-9(H4). The major fatty acids (> 10% of the total fatty acids) were C18:0 10-methyl (TBSA) (28.2%), C16:0 (21.0%), C16:0 2-OH (20.8%) and C18:1ω9c (12.8%). The polar lipid profile comprised diphosphatidylglycerol, phosphatidylglycerol, phosphatidylcholine, phosphatidylinositol, an unidentified aminophospholipid and an unidentified lipid. Based on the phylogenic, phenotypic and chemotaxonomic features, strain 9W16Y-2T represents a novel species of the genus Aeromicrobium, for which the name Aeromicrobium endophyticum sp. nov. is proposed. The type strain is 9W16Y-2T (= CGMCC 1.13876T = JCM 33141T).

Keywords

endophytic actinobacterium Aeromicrobium endophyticum genome comparison single-copy phylogenetic marker genes 

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Notes

Acknowledgements

This research was partly supported by the CAMS Innovation Fund for Medical Sciences (Grant No. CAMS 2017-I2M-B&R-08; CAMS 2017-I2M-1-012), PUMC Youth Fund (2017350022), National Natural Sciences Foundation of China (Grant No.81621064) and International S&T Cooperation (2016YFE0122000). We are grateful to Dr. Zhanfeng Xia at the Tarim University, Xinjiang, China, for assistance in sampling at Taklamakan Desert and Dr. Rongfeng Li from The Johns Hopkins University, Maryland, USA, for useful discussion with this paper.

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References

  1. Ber, P., Trappen, S.V., Vandamme, P., and Trček, J. 2017. Aeromicrobium choanae sp. nov., an actinobacterium isolated from the choana of a garden warbler. Int. J. Syst. Evol. Microbiol. 67, 357–361.CrossRefPubMedGoogle Scholar
  2. Bruns, A., Philipp, H., Cypionka, H., and Brinkhoff, T. 2003. Aeromicrobium marinum sp. nov., an abundant pelagic bacterium isolated from the German Wadden Sea. Int. J. Syst. Evol. Microbiol. 53, 1917–1923.CrossRefPubMedGoogle Scholar
  3. Cappuccino, J.G. and Sherman, N. 2002. Microbiology: A laboratory manual, 6th edn. Benjamin Cummings Pearson Education, San Francisco, USA.Google Scholar
  4. Chen, Y., Chen, Y., Shi, C., Huang, Z., Zhang, Y., Li, S., Li, Y., Ye, J., Yu, C., Li, Z., et al. 2017. SOAPnuke: a MapReduce acceleration supported software for integrated quality control and pre-processing of high-throughput sequencing data. GigaScience 7, 1–6.PubMedCentralGoogle Scholar
  5. 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.CrossRefPubMedGoogle Scholar
  6. Collins, M.D., Pirouz, T., Goodfellow, M., and Minnikin, D.E. 1977. Distribution of menaquinones in actinomycetes and corynebacteria. J. Gen. Microbiol. 100, 221–230.CrossRefPubMedGoogle Scholar
  7. Collins, M.D. and Stackebrandt, E. 1989. Molecular taxonomic studies on some LL-diaminopimelic acid-containing coryneforms from herbage: description of Nocardioides fastidiosa sp. nov. FEMS Microbiol. Lett. 57, 289–293.PubMedGoogle Scholar
  8. Cui, Y.S., Im, W.T., Yin, C.R., Lee, J.S., Lee, K.C., and Lee, S.T. 2007. Aeromicrobium panaciterrae sp. nov., isolated from soil of a ginseng field in South Korea. Int. J. Syst. Evol. Microbiol. 57, 687–691.CrossRefPubMedGoogle Scholar
  9. DeLong, E.F. 1992. Archaea in coastal marine environments. Proc. Natl. Acad. Sci. USA 89, 5685–5689.CrossRefPubMedGoogle Scholar
  10. Felsenstein, J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17, 368–376.CrossRefPubMedGoogle Scholar
  11. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Fitch, W.M. 1971. Toward defining the course of evolution: minimum change for a specific tree topology. Syst. Zool. 20, 406–416.CrossRefGoogle Scholar
  13. Gonzalez, C., Gutierrez, C., and Ramirez, C. 1978. Halobacterium vallismortis sp. nov., an amylolytic and carbohydrate-metabolizing, extremely halophilic bacterium. Can. J. Microbiol. 24, 710–715.CrossRefPubMedGoogle Scholar
  14. Guo, L., Tuo, L., Habden, X., Zhang, Y., Liu, J., Jiang, Z., Liu, S., Dilbar, T., and Sun, C. 2015. Allosalinactinospora lopnorensis gen. nov., sp. nov., a new member of the family Nocardiopsaceae isolated from soil. Int. J. Syst. Evol. Microbiol. 65, 206–213.CrossRefPubMedGoogle Scholar
  15. Hyatt, D., Chen, G.L., Locascio, P.F., Land, M.L., Larimer, F.W., and Hauser, L.J. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 119.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Kelly, K.L. 1964. Inter-society color council-national bureau of standards color name charts illustrated with centroid colors. US Government Printing Office, Washington, DC, USA.Google Scholar
  17. Kim, M., Oh, H.S., Park, S.C., and Chun, J. 2014. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int. J. Syst. Evol. Microbiol. 64, 346–351.CrossRefPubMedGoogle Scholar
  18. Kim, M.K., Park, M.J., Im, W.T., and Yang, D.C. 2008. Aeromicrobium ginsengisoli sp. nov., isolated from a ginseng field. Int. J. Syst. Evol. Microbiol. 58, 2025–2030.CrossRefPubMedGoogle Scholar
  19. Kim, S.H., Yang, H.O., Sohn, Y.C., and Kwon, H.C. 2010. Aeromicrobium halocynthiae sp. nov., a taurocholic acid-producing bacterium isolated from the marine ascidian Halocynthia roretzi. Int. J. Syst. Evol. Microbiol. 60, 2793–2798.CrossRefPubMedGoogle Scholar
  20. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequence. J. Mol. Evol. 16, 111–120.CrossRefGoogle Scholar
  21. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Lee, S.D. and Kim, S.J. 2007. Aeromicrobium tamlense sp. nov., isolated from dried seaweed. Int. J. Syst. Evol. Microbiol. 57, 337–341.CrossRefPubMedGoogle Scholar
  23. Lee, D.W. and Lee, S.D. 2008. Aeromicrobium ponti sp. nov., isolated from seawater. Int. J. Syst. Evol. Microbiol. 58, 987–991CrossRefPubMedGoogle Scholar
  24. Li, F.N., Tuo, L., Lee, M.Y., Jin, T., Liao, S., Li, W., Yan, X., and Sun, C.H. 2018. Amnibacterium endophyticum sp. nov., an endophytic actinobacterium isolated from Aegiceras corniculatum. Int. J. Syst. Evol. Microbiol. 68, 1327–1332.CrossRefPubMedGoogle Scholar
  25. Li, F.N., Tuo, L., Pan, Z., Guo, M., Lee, M.Y., Chen, L., Hu, L., and Sun, C.H. 2017. Aureimonas endophytica sp. nov., a novel endophytic bacterium isolated from Kandelia candel. Int. J. Syst. Evol. Microbiol. 67, 2934–2940.CrossRefPubMedGoogle Scholar
  26. Li, W.J., Xu, P., Schumann, P., Zhang, Y.Q., Pukall, R., Xu, L.H., Stackebrandt, E., and Jiang, C.L. 2007. Georgenia ruanii sp. nov., a novel actinobacterium isolated from forest soil in Yunnan (China) and emended description of the genus Georgenia. Int. J. Syst. Evol. Microbiol. 57, 1424–1428.CrossRefPubMedGoogle Scholar
  27. Magee, C.M., Rodeheaver, G., Edgerton, M.T., and Edlich, R.F. 1975. A more reliable gram staining technic for diagnosis of surgical infections. Am. J. Surg. 130, 341–346.CrossRefPubMedGoogle Scholar
  28. Marmur, J. 1961. A procedure for the isolation of deoxyribonucleic acid from microorganisms. J. Mol. Biol. 3, 208–218.CrossRefGoogle Scholar
  29. Mende, D.R., Sunagawa, S., Zeller, G., and Bork, P. 2013. Accurate and universal delineation of prokaryotic species. Nat. Methods 10, 881–884.CrossRefPubMedGoogle Scholar
  30. Mikheenko, A., Valin, G., Prjibelski, A., Saveliev, V., and Gurevich, A. 2016. Icarus: visualize for de novo assembly evaluation. Bioinformatics 32, 3321–3323.CrossRefPubMedGoogle Scholar
  31. Miller, E.S., Woese, C.R., and Brenner, S. 1991. Description of the erythromycin-producing bacterium Arthrobacter sp. strain NRRL B-3381 as Aeromicrobium erythreum gen. nov., sp. nov. Int. J. Syst. Bacteriol. 41, 363–368.CrossRefPubMedGoogle Scholar
  32. 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.CrossRefGoogle Scholar
  33. Nesterenko, O.A., Kvasnikov, E.I., and Nogina, T.M. 1985. Nocardioidaceae fam. nov., a new family of the order Actinomycetales Buchanan 1917. Mikrobiol. Z. 47, 3–12.Google Scholar
  34. Niu, L., Xiong, M., Tang, T., Song, L., Hu, X., Zhao, M., and Zhang, K. 2015. Aeromicrobium camelliae sp. nov., isolated from Pu’er tea. Int. J. Syst. Evol. Microbiol. 65, 4369–4373.CrossRefPubMedGoogle Scholar
  35. Peng, Y., Leung, H.C., Yiu, S.M., and Chin, F.Y. 2012. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28, 1420–1428.CrossRefPubMedGoogle Scholar
  36. Qin, S., Wang, H.B., Chen, H.H., Zhang, Y.Q., Jiang, C.L., Xu, L.H., and Li, W.J. 2008. Glycomyces endophyticus sp. nov., an endophytic actinomycete isolated from the root of Carex baccans Nees. Int. J. Syst. Evol. Microbiol. 58, 2525–2528.CrossRefPubMedGoogle Scholar
  37. Ramasamy, D., Kokcha, S., Lagier, J.C., Nguyen, T.T., Raoult, D., and Fournier, P.E. 2012. Genome sequence and description of Aeromicrobium massiliense sp. nov. Stand. Genomic Sci. 7, 246–257.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Richter, M. and Rosselló-Móra, R. 2009. Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl. Acad. Sci. USA 106, 19126–19131.CrossRefPubMedGoogle Scholar
  39. Saitou, N. and Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425.PubMedGoogle Scholar
  40. Sasser, M. 1990. Identification of bacteria by gas chromatography of cellular fatty acids, MIDI Technical Note 101. MIDI Inc., Newark, DE, USA.Google Scholar
  41. Shirling, E.B. and Gottlieb, D. 1966. Methods for characterization of Streptomyces species. Int. J. Syst. Bacteriol. 16, 313–340.CrossRefGoogle Scholar
  42. Staneck, J.L. and Roberts, G.D. 1974. Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl. Microbiol. 28, 226–231.PubMedPubMedCentralGoogle Scholar
  43. Swindell, S.R. and Plasterer, T.N. 1997. SEQMAN. Contig assembly. Methods Mol. Biol. 70, 75–89.PubMedGoogle Scholar
  44. Tamura, T. and Yokota, A. 1994. Transfer of Nocardioides fastidiosa Collins and Stackebrandt 1989 to the genus Aeromicrobium as Aeromicrobium fastidiosum comb. nov. Int. J. Syst. Bacteriol. 44, 608–611.CrossRefGoogle Scholar
  45. Tang, Y., Zhou, G., Zhang, L., Mao, J., Luo, X., Wang, M., and Fang, C. 2008. Aeromicrobium flavum sp. nov., isolated from air. Int. J. Syst. Evol. Microbiol. 58, 1860–1863.CrossRefPubMedGoogle Scholar
  46. Wayne, L.G., Brenner, D.J., Colwell, R.R., Grimont, P.A.D., Kandler, O., Krichevsky, M.I., Moore, L.H., Moore, W.E.C., Murray, R.G.E., Stackebrandt, E., et al. 1987. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int. J. Syst. Evol. Microbiol. 37, 463–464.CrossRefGoogle Scholar
  47. Xu, P., Li, W.J., Tang, S.K., Zhang, Y.Q., Chen, G.Z., Chen, H.H., Xu, L.H., and Jiang, C.L. 2005. Naxibacter alkalitolerans gen. nov., sp. nov., a novel member of the family Oxalobacteraceae isolated from China. Int. J. Syst. Evol. Microbiol. 55, 1149–1153.CrossRefPubMedGoogle Scholar
  48. Yoon, J.H., Lee, C.H., and Oh, T.K. 2005. Aeromicrobium alkaliterrae sp. nov., isolated from an alkaline soil, and emended description of the genus Aeromicrobium. Int. J. Syst. Evol. Microbiol. 55, 2171–2175.CrossRefPubMedGoogle Scholar

Copyright information

© The Microbiological Society of Korea 2019

Authors and Affiliations

  • Fei-Na Li
    • 1
  • Shui-Lin Liao
    • 2
    • 3
    • 4
  • Shao-Wei Liu
    • 1
  • Tao Jin
    • 2
    • 3
  • Cheng-Hang Sun
    • 1
    Email author
  1. 1.Institute of Medicinal BiotechnologyChinese Academy of Medical Sciences & Peking Union Medical CollegeBeijingP. R. China
  2. 2.BGI-Shenzhen, Beishan Industrial ZoneShenzhenP. R. China
  3. 3.China National GeneBank, BGI-ShenzhenShenzhenP. R. China
  4. 4.BGI Education CenterUniversity of Chinese Academy of SciencesShenzhenP. R. China

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