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Nocardioides pakistanensis sp. nov., isolated from a hot water spring of Tatta Pani in Pakistan

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Abstract

A Gram-staining positive, non-spore forming, non-pigmented and non-motile bacterium, designated as NCCP-1340T, was isolated from a hot water spring, Tatta Pani, Pakistan. Cells of strain NCCP-1340T were observed to be aerobic, rod shaped, catalase and urease positive but H2S production and oxidase negative. Growth was observed at pH 6.0–8.0 (optimum pH 7.0) and at 20–40 °C (optimum 37 °C). The strain could tolerate 0–8 % NaCl (optimum 2 %, w/v). Phylogenetic analysis based on 16S rRNA gene sequence comparisons revealed that strain NCCP-1340T belongs to the genus Nocardioides and is closely related to Nocardioides iriomotensis JCM 17985T (96.8 %), Nocardioides daedukensis KCTC 19601T (96.6 %), Nocardioides jensenii KCTC 9134T (96.1 %) and Nocardioides daejeonensis KCTC 19772T (96.1 %). The DNA–DNA relatedness values of strain NCCP-1340T with N. iriomotensis JCM 17985T, N. daedukensis KCTC 19601T and N. jensenii KCTC 9134T were found to be less than 53 %. The DNA G+C content of strain NCCP-1340T was determined to be 71.8 mol  %. The affiliation of strain NCCP-1340T to the genus Nocardioides was further supported by chemotaxonomic data which showed the presence of MK-8(H4) as major menaquinone system; iso-C16:0, C17:0, C16:0 10-methyl, iso-C15:0 and C 15:0 as major cellular fatty acids; and diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylinositol and unidentified glycolipids and polar lipids in the polar lipids profile. The cell wall peptidoglycan contained LL-diaminopimelic acid as the diagnostic amino acid. On the basis of physiological and biochemical characteristics and the phylogenetic analyses, strain NCCP-1340T can be distinguished from the closely related taxa and thus represents a novel species of the genus Nocardioides, for which the name Nocardioides pakistanensis sp. nov. is proposed with the type strain NCCP-1340T (= DSM 29942T = JCM 30630T).

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References

  • Ahn JH, Lim JM, Kim SJ, Song J, Kwon SW, Weon HY (2014) Nocardioides paucivorans sp. nov. isolated from soil. J Microbiol 52:990–994

    Article  CAS  PubMed  Google Scholar 

  • Christensen H, Angen O, Mutters R, Olsen JE, Bisgaard M (2000) DNA–DNA hybridization determined in micro-wells using covalent attachment of DNA. Int J Syst Evol Microbiol 50:1095–1102

    Article  CAS  PubMed  Google Scholar 

  • Collins M, Jones D (1980) Lipids in the classification and identification of coryneform bacteria containing peptidoglycans based on 2, 4-diaminobutyric acid. J Appl Bacteriol 48:459–470

    Article  CAS  Google Scholar 

  • Collins MD, Pirouz T, Goodfellow M, Minnikin DE (1977) Distribution of menaquinones in Actinomycetes and Corynebacteria. J Gen Microbiol 100:221–230

    Article  CAS  PubMed  Google Scholar 

  • Collins M, Dorsch M, Stackebrandt E (1989) Transfer of Pimelobacter tumescens to Terrabacter gen. nov. as Terrabacter tumescens comb. nov. and of Pimelobacter jensenii to Nocardioides as Nocardioides jensenii comb. nov. Int J Syst Evol Microbiol 39:1–6

    CAS  Google Scholar 

  • Dastager SG, Lee JC, Ju YJ, Park DJ, Kim CJ (2008a) Nocardioides koreensis sp. nov., Nocardioides bigeumensis sp. nov. and Nocardioides agariphilus sp. nov., isolated from soil from Bigeum Island. Korea Int J Syst Evol Microbiol 58:2292–2296

    Article  CAS  PubMed  Google Scholar 

  • Dastager SG, Lee JC, Ju YJ, Park DJ, Kim CJ (2008b) Nocardioides tritolerans sp. nov., isolated from soil in Bigeum Island. Korea J Microbiol Biotechnol 18:1203–1206

    CAS  PubMed  Google Scholar 

  • Dastager SG, Lee JC, Ju YJ, Park DJ, Kim CJ (2009) Nocardioides sediminis sp. nov., isolated from a sediment sample. Int J Syst Evol Microbiol 59:280–284

    Article  CAS  PubMed  Google Scholar 

  • Dastager SG, Lee JC, Pandey A, Kim CJ (2010) Nocardioides mesophilus sp. nov., isolated from soil. Int J Syst Evol Microbiol 60:2288–2292

    Article  CAS  PubMed  Google Scholar 

  • Evtushenko LI, Krausova VI, Yoon J-H (2015) Nocardioides. In: Bergey’s manual of systematics of archaea and bacteria. Wiley, New York

  • Ezaki T, Hashimoto Y, Yabuuchi E (1989) Fluorometric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Bacteriol 39:224–229

    Article  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 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evol 39:783–791

    Article  Google Scholar 

  • Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416

    Article  Google Scholar 

  • Goris J, K-i Suzuki, Vos PD, Nakase T, Kersters K (1998) Evaluation of a microplate DNA–DNA hybridization method compared with the initial renaturation method. Can J Microbiol 44:1148–1153

    Article  CAS  Google Scholar 

  • Hasegawa T, Takizawa M, Tanida S (1983) A rapid analysis for chemical grouping of aerobic Actinomycetes. J Gen Appl Microbiol 29:319–322

    Article  CAS  Google Scholar 

  • Kim HM, Choi DH, Hwang CY, Cho BC (2008) Nocardioides salarius sp. nov., isolated from seawater enriched with zooplankton. Int J Syst Evol Microbiol 58:2056–2064

    Article  CAS  PubMed  Google Scholar 

  • Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721

    Article  CAS  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kovacs N (1956) Identification of Pseudomonas pyocyanea by the oxidase reaction. Nature 178:703

    Article  CAS  PubMed  Google Scholar 

  • Kroppenstedt RM (1982) Separation of bacterial menaquinones by HPLC using reverse phase (RP18) and a silver loaded ion exchanger as stationary phases. J Liq Chromat 5:2359–2367

    Article  CAS  Google Scholar 

  • Kubota M, Kawahara K, Sekiya K, Uchida T, Hattori Y, Futamata H, Hiraishi A (2005) Nocardioides aromaticivorans sp. nov., a dibenzofuran-degrading bacterium isolated from dioxin-polluted environments. Syst Appl Microbiol 28:165–174

    Article  CAS  PubMed  Google Scholar 

  • Lechevalier MP, Lechevalier H (1970) Chemical composition as a criterion in the classification of aerobic Actinomycetes. Int J Syst Bacteriol 20:435–443

    Article  CAS  Google Scholar 

  • Lee SD, Lee DW (2014) Nocardioides rubroscoriae sp. nov., isolated from volcanic ash. Antonie Van Leeuwenhoek 105:1017–1023

    Article  CAS  PubMed  Google Scholar 

  • Lee DW, Hyun CG, Lee SD (2007) Nocardioides marinisabuli sp. nov., a novel actinobacterium isolated from beach sand. Int J Syst Evol Microbiol 57:2960–2963. doi:10.1099/ijs.0.65127-0

    Article  CAS  PubMed  Google Scholar 

  • Li WJ, Zhang YG, Zhang YQ, Tang SK, Xu P, Xu LH, 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 57:1424–1428

    Article  PubMed  Google Scholar 

  • Lin SY, Wen CZ, Hameed A, Liu YC, Hsu YH, Shen FT, Lai WA, Young CC (2015) Nocardioides echinoideorum sp. nov., isolated from sea urchins (Tripneustes gratilla). Int J Syst Evol Microbiol 65:1953–1958

    Article  CAS  PubMed  Google Scholar 

  • Marmur J (1963) A procedure for the isolation of deoxyribonucleic acid from microorganisms. Meth Enzymol 6:726–738

    Article  CAS  Google Scholar 

  • 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 39:159–167

    Article  CAS  Google Scholar 

  • 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 47:87–95

    Article  CAS  Google Scholar 

  • O’Donnell AG, Goodfellow M, Minnikin DE (1982) Lipids in the classification of Nocardioides: Reclassification of Arthrobacter simplex (Jensen) lochhead in the genus Nocardioides (Prauser) emend. O’Donnell et al. as Nocardioides simplex comb. nov. Arch Microbiol 133:323–329

    Article  PubMed  Google Scholar 

  • Pitcher D, Saunders N, Owen R (1989) Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett Appl Microbiol 8:151–156

    Article  CAS  Google Scholar 

  • Prauser H (1976) Nocardioides, a new genus of the order Actinomycetales. Int J Syst Bacteriol 26:58–65

    Article  Google Scholar 

  • Qin S, Yuan B, Zhang YJ, Bian GK, Tamura T, Sun BZ, Li WJ, Jiang JH (2012) Nocardioides panzhihuaensis sp. nov., a novel endophytic actinomycete isolated from medicinal plant Jatropha curcas L. Antonie Van Leeuwenhoek 102:353–360

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, 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

  • Schippers A, Schumann P, Sproer C (2005) Nocardioides oleivorans sp. nov., a novel crude-oil-degrading bacterium. Int J Syst Evol Microbiol 55:1501–1504

    Article  CAS  PubMed  Google Scholar 

  • Shirling E, Gottlieb D (1966) Method for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340

    Article  Google Scholar 

  • Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA–DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Evol Microbiol 44:846–849

    Article  CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA 6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang SK, Wang Y, Chen Y, Lou K, Cao LL, Xu LH, Li WJ (2009a) Zhihengliuella alba sp. nov., and emended description of the genus Zhihengliuella. Int J Syst Evol Microbiol 59:2025–2031

    Article  CAS  PubMed  Google Scholar 

  • Tang SK, Wang Y, Lou K, Mao PH, Jin X, Jiang CL, Xu LH, Li WJ (2009b) Gracilibacillus saliphilus sp. nov., a moderately halophilic bacterium isolated from a salt lake. Int J Syst Evol Microbiol 59:1620–1624

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuo L, Dong YP, Habden X, Liu JM, Guo L, Liu XF, Chen L, Jiang ZK, Liu SW, Zhang YB, Zhang YQ, Sun CH (2015) Nocardioides deserti sp. nov., an actinobacterium isolated from desert soil. Int J Syst Evol Microbiol 65:1604–1610

    Article  CAS  PubMed  Google Scholar 

  • Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt E, Starr MP, Trüper HG (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464

    Article  Google Scholar 

  • Xu P, Li WJ, Tang SK, Zhang YQ, Chen GZ, Chen HH, Xu LH, Jiang CL (2005) Naxibacter alkalitolerans gen. nov., sp. nov., a novel member of the family ‘Oxalobacteraceae’ isolated from China. Int J Syst Evol Microbiol 55:1149–1153

    Article  CAS  PubMed  Google Scholar 

  • Yamamura H et al (2011) Nocardioides iriomotensis sp. nov., an actinobacterium isolated from forest soil. Int J Syst Evol Microbiol 61:2205–2209

    Article  CAS  PubMed  Google Scholar 

  • Yoon JH, Cho YG, Lee ST, Suzuki K, Nakase T, Park YH (1999) Nocardioides nitrophenolicus sp. nov., a p-nitrophenol-degrading bacterium. Int J Syst Bacteriol 49:675–680

    Article  CAS  PubMed  Google Scholar 

  • Yoon JH, Kim IG, Kang KH, Oh TK, Park YH (2004) Nocardioides aquiterrae sp. nov., isolated from groundwater in Korea. Int J Syst Evol Microbiol 54:71–75

    Article  CAS  PubMed  Google Scholar 

  • Yoon JH, Lee JK, Jung SY, Kim JA, Kim HK, Oh TK (2006) Nocardioides kongjuensis sp. nov., an N-acylhomoserine lactone-degrading bacterium. Int J Syst Evol Microbiol 56:1783–1787

    Article  CAS  PubMed  Google Scholar 

  • Yoon JH, Park S, Kang SJ, Lee JS, Lee KC, Oh TK (2010) Nocardioides daedukensis sp. nov., a halotolerant bacterium isolated from soil. Int J Syst Evol Microbiol 60:1334–1338

    Article  CAS  PubMed  Google Scholar 

  • Zhang DC, Schumann P, Redzic M, Zhou YG, Liu HC, Schinner F, Margesin R (2012) Nocardioides alpinus sp. nov., a psychrophilic actinomycete isolated from alpine glacier cryoconite. Int J Syst Evol Microbiol 62:445–450

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Prof. Takuji Kudo (JCM, Japan) and Miss Sang-Mi Lee (KCTC, Korea) for kindly providing the reference type strains. This work was supported by the Key Project of International Cooperation of Ministry of Science & Technology (MOST) (No. 2013DFA31980), Science and technology infrastructure work project (No. 2015FY110100) and the Deanship of Scientific Research at King Saud University (through the research group no. 1436-27). W-J Li was also supported by Guangdong Province Higher Vocational Colleges & Schools Pearl River Scholar Funded Scheme (2014).

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Correspondence to Iftikhar Ahmed or Wen-Jun Li.

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Amin, A., Ahmed, I., Habib, N. et al. Nocardioides pakistanensis sp. nov., isolated from a hot water spring of Tatta Pani in Pakistan. Antonie van Leeuwenhoek 109, 1101–1109 (2016). https://doi.org/10.1007/s10482-016-0711-8

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