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Phenylobacterium terrae sp. nov., isolated from a soil sample of Khyber-Pakhtun-Khwa, Pakistan

  • Inam Ullah Khan
  • Neeli Habib
  • Min Xiao
  • Xing Huang
  • Nasr Ullah Khan
  • Wan-Taek Im
  • Iftikhar Ahmed
  • Xiao-Yang Zhi
  • Wen-Jun Li
Original Paper

Abstract

A Gram-stain negative, aerobic, motile, non-spore-forming and rod-shaped bacterial strain, designated YIM 730227T, was isolated from a soil sample, collected from Karak district, Khyber-Pakhtun-Khwa, Pakistan. The bacterium was characterized using a polyphasic taxonomic approach. Pairwise comparison of the 16S rRNA gene sequences showed that strain YIM 730227T is closely related to Phenylobacterium lituiforme FaiI3T (97.5% sequence similarity), Phenylobacterium muchangponense A8T (97.4%), Phenylobacterium panacis DCY109T (97.1%), Phenylobacterium immobile ET (97.1%) and Phenylobacterium composti 4T-6T (97.0%), while also sharing 98.0% sequence similarity with Phenylobacterium hankyongense HKS-05T after NCBI blast, showing it represents a member of the family Caulobacteraceae. The major respiratory quinone was Q-10 and the major fatty acids were C16:0, summed feature 8 (comprising C18:1ω7c and/or C18:1ω6c), C18:1ω7c 11-methyl and C17:0. The polar lipids were phosphatidylglycerol, unidentified glycolipids, phospholipid and unidentified lipid. The G + C content of the genomic DNA was 68.2 mol%. The DNA–DNA relatedness values of strain YIM 730227T with P. hankyongense HKS-05T, P. lituiforme FaiI3T, P. muchangponense A8T, P. panacis DCY109T, P. immobile ET and P. composti 4T-6T were 31.3 ± 0.6, 26.1 ± 0.2, 24.3 ± 0.1, 21.8 ± 0.9, 19.8 ± 0.6 and 18.2 ± 1.1%, respectively, values lower than 70%. Besides the morphological and chemotaxonomic characteristics, phylogenetic analyses of 16S rRNA gene sequences and the biochemical characteristics indicated that the strain YIM 730227T represents a novel member of the genus Phenylobacterium, for which the name Phenylobacterium terrae sp. nov. (type strain YIM 730227T = KCTC62324T = CGMCC 1.16326T) is proposed.

Keywords

Phenylobacterium terrae sp. nov. A soil sample Karak Khyber-Pakhtun-Khwa Pakistan Polyphasic taxonomic approaches 

Notes

Acknowledgements

We are grateful to Dr Rüdiger Pukall (DSMZ, Germany) and Professor Jung-Sook Lee (KCTC, Korea) for kindly providing the reference type strains. This work was supported by Science and Technology Infrastructure work project of Ministry of Science & Technology (No. 2015FY110100) and National Natural Science Foundation of China (No. 31470139). W-J Li was also supported by Guangdong Province Higher Vocational Colleges & Schools Pearl River Scholar Funded Scheme (2014).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no direct or indirect conflict of interest.

Ethical approval

It is the original work of the authors. The work described has not been submitted elsewhere for publication, in whole or in part, and all authors listed carry out the data analysis and manuscript writing and ‘‘This article does not contain any studies with human participants or animals performed by any of the authors’’. Moreover, all authors read and approved the final manuscript.

Supplementary material

10482_2018_1064_MOESM1_ESM.doc (2.9 mb)
Supplementary material 1 (DOC 3003 kb)

References

  1. Abraham WR, Macedo AJ, Lünsdorf H, Fischer R, Pawelczyk S, Smit J, Vancanneyt M (2008) Phylogeny by a polyphasic approach of the order Caulobacterales, proposal of Caulobacter mirabilis sp. nov., Phenylobacterium haematophilum sp. nov. and Phenylobacterium conjunctum sp. nov., and emendation of the genus Phenylobacterium. Int J Syst Evol Microbiol 58:1939–1949CrossRefPubMedGoogle Scholar
  2. Aslam Z, Im WT, Ten LN, Lee ST (2005) Phenylobacterium koreense sp. nov., isolated from South Korea. Int J Syst Evol Microbiol 55:2001–2005CrossRefPubMedGoogle Scholar
  3. Choi GM, Lee SY, Choi KD, Im WT (2018) Phenylobacterium hankyongense sp. nov., isolated from ginseng field soil. Int J Syst Evol Microbiol 68:125–130CrossRefPubMedGoogle Scholar
  4. Christensen H, Angen O, Mutters R, Olsen JE, Bisgaard M (2000) DNA–DNA hybridization determined in microwells using covalent attachment of DNA. Int J Syst Bacteriol 50:1095–1102CrossRefGoogle Scholar
  5. Chu C, Yuan C, Liu X, Yao L, Zhu J, He J, Kwon SW, Huang X (2015) Phenylobacterium kunshanense sp. nov., isolated from the sludge of a pesticide manufacturing factory. Int J Syst Evol Microbiol 65:325–330CrossRefPubMedGoogle Scholar
  6. Collins MD, Jones D (1980) Lipids in the classification and identification of coryneform bacteria containing peptidoglycans based on 2, 4-diaminobutyric acid. J Appl Bacteriol 48:459–470CrossRefGoogle Scholar
  7. Collins MD, Pirouz T, Goodfellow M, Minnikin DE (1977) Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 100:221–230CrossRefPubMedGoogle Scholar
  8. Cui XL, Mao PH, Zeng M, Li WJ, Zhang LP, Xu LH, Jiang CL (2001) Streptimonospora salina gen. nov., sp. nov., a new member of the family Nocardiopsaceae. Int J Syst Evol Microbiol 51:357–363CrossRefPubMedGoogle Scholar
  9. Ezaki T, Hashimoto Y, Yabuuchi E (1989) Fluorometric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution well as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Bacteriol 39:224–229CrossRefGoogle Scholar
  10. Farh ME, Kim YJ, Singh P, Hoang VA, Yang DC (2016) Phenylobacterium panacis sp. nov., isolated from the rhizosphere of rusty mountain ginseng. Int J Syst Evol Microbiol 66:2691–2696CrossRefPubMedGoogle Scholar
  11. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376CrossRefPubMedGoogle Scholar
  12. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefPubMedGoogle Scholar
  13. Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416CrossRefGoogle Scholar
  14. Gonzalez C, Gutierrez C, Ramirez C (1978) Halobacterium vallismortis sp. nov. an amylolytic and carbohydrate-metabolizing, extremely halophilic bacterium. Can J Microbiol 24:710–715CrossRefPubMedGoogle Scholar
  15. Gordon RE, Barnett DA, Handerhan JE, Pang CH-N (1974) Nocardia coeliaca, Nocardia autotrophica, and the nocardin strain. Int J Syst Bacteriol 24:54–63CrossRefGoogle Scholar
  16. Gregersen T (1978) Rapid method for distinction of Gram-negative from Gram-positive bacteria. Eur J Appl Microbiol Biotechnol 5:123–127CrossRefGoogle Scholar
  17. Jo JH, Choi GM, Lee SY, Im WT (2016) Phenylobacterium aquaticum sp. nov., isolated from the reservoir of a water purifier. Int J Syst Evol Microbiol 66:3519–3523CrossRefPubMedGoogle Scholar
  18. Kanso S, Patel BKC (2004) Phenylobacterium lituiforme sp. nov., a moderately thermophilic bacterium from a subsurface aquifer, and emended description of the genus Phenylobacterium. Int J Syst Evol Microbiol 54:2141–2146CrossRefPubMedGoogle Scholar
  19. Khan IU, Hussain F, Habib N, Wadaan MAM, Ahmed I, Im WT, Hozzein WN, Zhi XY, Li WJ (2017) Phenylobacterium deserti sp. nov., isolated from desert soil. Int J Syst Evol Microbiol 67:4722–4727CrossRefPubMedGoogle Scholar
  20. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMedGoogle Scholar
  21. Kovacs N (1956) Identification of Pseudomonas pyocyaneaby the oxidase reaction. Nature 178:703CrossRefPubMedGoogle Scholar
  22. Kroppenstedt RM (1982) Separation of bacterial menaquinones by HPLC using reverse phase (RP18) and a silver loaded ion exchanger as stationary phases. J Liq Chromatogr 5:2359–2367CrossRefGoogle Scholar
  23. Li WJ, Xu P, Schuman P, Zhang YQ, Pukall R, Xu LH, Stackebrandt E, Jiang CL (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 57:1424–1428CrossRefPubMedGoogle Scholar
  24. Lingens F, Blecher R, Blecher H, Blobel F, Eberspächer J, Fröhner C, Görisch H, Görisch H, Layh G (1985) Phenylobacterium immobile gen. nov., sp. nov., a Gram-negative bacterium that degrades the herbicide chloridazon. Int J Syst Bacteriol 35:26–39CrossRefGoogle Scholar
  25. Macfaddin JF (1976) Biochemical tests for identification of medical bacteria. Williams & Wilkins Co, PhiladelphiaGoogle Scholar
  26. Mergaert J, Cnockaert MC, Swings J (2002) Fulvimonas soli gen. nov., sp. nov., a gamma-proteobacterium isolated from soil after enrichment on acetylated starch plastic. Int J Syst Evol Microbiol 52:1285–1289PubMedGoogle Scholar
  27. Mesbah M, Premachandran U, Whitman WB (1989) Precise measurement of the G + C content of deoxyribonucleic acid by high performance liquid chromatography. Int J Syst Bacteriol 39:159–167CrossRefGoogle Scholar
  28. Minnikin D, Collins M, Goodfellow M (1979) Fatty acid and polar lipid composition in the classification of Cellulomonas, Oerskovia and related taxa. J Appl Bacteriol 47:87–95CrossRefGoogle Scholar
  29. Oh YS, Roh DH (2012) Phenylobacterium muchangponense sp. nov., isolated from beach soil, and emended description of the genus Phenylobacterium. Int J Syst Evol Microbiol 62:977–983CrossRefPubMedGoogle Scholar
  30. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  31. Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 20:16Google Scholar
  32. Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, DC, pp 607–654Google Scholar
  33. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  34. Tiago I, Mendes V, Pires C, Morais PV, Vers´simo A (2005) Phenylobacterium falsum sp. nov., an Alphaproteobacterium isolated from a nonsaline alkaline groundwater, and emended description of the genus Phenylobacterium. Syst Appl Microbiol 28:295–302CrossRefPubMedGoogle Scholar
  35. Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE (1987) International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464CrossRefGoogle Scholar
  36. Weon HY, Kim BY, Kwon SW, Go SJ, Koo BS, Stackebrandt E (2008) Phenylobacterium composti sp. nov., isolated from cotton waste compost in Korea. Int J Syst Evol Microbiol 58:2301–2304CrossRefPubMedGoogle Scholar
  37. Xu P, Li WJ, Tang SK, Zhang YQ, Chen GZ, Chen HH, Xu H, Jiang CL (2005) Naxibacter alkalitolerans gen. nov., sp. nov., a novel member of the family Oxalobacteraceae isolated from China. Int J Syst Evol Microbiol 55:1149–1153CrossRefPubMedGoogle Scholar
  38. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies. Int J Syst Evol Microbiol 67:1613–1617CrossRefPubMedPubMedCentralGoogle Scholar
  39. Zhang K, Han W, Zhang R, Xu X, Pan Q, Hu X (2007) Phenylobacterium zucineum sp. nov., a facultative intracellular bacterium isolated from a human erythroleukemia cell line K562. Syst Appl Microbiol 30:207–212CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Inam Ullah Khan
    • 1
    • 3
  • Neeli Habib
    • 1
  • Min Xiao
    • 2
  • Xing Huang
    • 4
  • Nasr Ullah Khan
    • 5
  • Wan-Taek Im
    • 6
  • Iftikhar Ahmed
    • 7
  • Xiao-Yang Zhi
    • 1
  • Wen-Jun Li
    • 1
    • 2
  1. 1.Yunnan Institute of Microbiology, School of Life SciencesYunnan UniversityKunmingPeople’s Republic of China
  2. 2.State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life SciencesSun Yat-Sen UniversityGuangzhouPeople’s Republic of China
  3. 3.Department of Biological SciencesGomal UniversityDera Ismail KhanPakistan
  4. 4.Key Laboratory of Microbiological Engineering of Agricultural Environment, Ministry of AgricultureLife Sciences College of Nanjing Agricultural UniversityNanjingPeople’s Republic of China
  5. 5.The Applied Plant Genomics Laboratory of Crop Genomics and Bioinformatics CentreNanjing Agricultural UniversityNanjingPeople’s Republic of China
  6. 6.Department of BiotechnologyHankyong National UniversityAnseong-siRepublic of Korea
  7. 7.Institute of Microbial Culture Collection of Pakistan (IMCCP), National Agricultural Research Centre (NARC)IslamabadPakistan

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