Abstract
A Gram-stain-positive, rod-shaped, non-spore-forming, alkane degrading bacterium, designated DJM-14T, was isolated from oilfield alkali-saline soil in Heilongjiang, Northeast China. On the basis of 16 S rRNA gene sequencing, strain DJM-14T was shown to belong to the genus Nocardioides, and related most closely to Nocardioides terrigena KCTC 19,217T (95.53% 16 S rRNA gene sequence similarity). Strain DJM-14T was observed to grow at 25–35 °C, pH 7.0–11.0, in the presence of 0–6.0% (w/v) NaCl. The predominant respiratory quinone was MK-8 (H4) and LL-diaminopimelic acid was the diagnostic diamino acid in the cell-wall peptidoglycan. The major fatty acids were identified as iso-C16:0 and C18:1 ω9c. It contained diphosphatidylglycerol, phosphatidylglycerol and phosphatidylinositol as the polar lipids. The genome (3,722,608 bp), composed of 24 contigs, had a G + C content of 69.6 mol%. Out of the 3667 predicted genes, 3618 were protein-coding genes, and 49 were ncRNAs. Digital DNA–DNA hybridization (dDDH) estimation and average nucleotide identity (ANI) of strain DJM-14T against genomes of the type strains of related species in the same family ranged between 18.7% and 20.0%; 68.8% and 73.6%, respectively. According to phenotypic, genotypic and phylogenetic data, strain DJM-14T represents a novel species in the genus Nocardioides, for which the name Nocardioides limicola sp. nov. is proposed and the type strain is DJM-14T (= CGMCC 4.7593T, =JCM 33,692T). In addition, novel strains were able to grow with n-alkane (C24-C36) as the sole carbon source. Multiple copies of alkane 1-monooxygenase (alkB) gene, as well as alcohol dehydrogenase gene and aldehyde dehydrogenase gene involved in the alkane assimilation were annotated in the genome of type strain DJM-14T.
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References
Auch AF, Klenk HP, Göker M (2010) Standard operating procedure for calculating genome-to-genome distances based on high-scoring segment pairs. Stand Genomic Sci 2:142–148. https://doi.org/10.4056/sigs.541628
Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, Costa MS, Rooney AP, Yi HN, Xu XW, Meyer SD, Trujillo ME (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68:461–466. https://doi.org/10.1099/ijsem.1090.002516
Collins MD, Goodfellow M, Minnikin DE, Alderson G (1985) Menaquinone composition of mycolic acid-containing actinomycetes and some sporoactinomycetes. J Appl Bacteriol 58(1):77–86. https://doi.org/10.1111/j.1365-2672.1985.tb01431.x
Dastager SG, Lee JC, Ju YJ, Park DJ, Kim CJ (2008) 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. https://doi.org/10.1099/ijs.0.65566-0
Dong C, Lai Q, Liu X, Gu L, Zhang Y, Xie Z, Wang D, Shao Z (2021) Alcanivorax profundimaris sp. nov., a novel marine hydrocarbonoclastic bacterium isolated from seawater and deep-ea sediment. Curr Microbiol 78:1053–1060. https://doi.org/10.1007/s00284-020-02322-7
Duan M, Wang X, Fang S, Zhao B, Li C, Xiong Y (2018) Treatment of Daqing oily sludge by thermochemical cleaning method. Colloids Surf a Physicochem Eng Aspects 554:272–278. https://doi.org/10.1016/j.colsurfa.2018.06.046
Ehiosun K, Iyere et al (2022) Degradation of long-chain alkanes through biofilm formation by bacteria isolated from oil-polluted soil. Int Biodeterior Biodegrad 175:105508
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376. https://doi.org/10.1007/BF01734359
Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125(1):1–15
Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Biol 20:406–416. https://doi.org/10.2307/2412116
Gao RX, Liu CX, Zhao JW, Jia FY, Yu C, Yang LY, Wang XJ, Xiang WS (2014) Micromonospora jinlongensis sp. nov., isolated from muddy soil in China and emended description of the genus Micromonospora. Antonie Van Leeuwenhoek 105:307–315. https://doi.org/10.1007/s10482013-0074-3
Gregersen T (1978) Rapid method for distinction of gram-negative from gram-positive bacteria. Eur J Appl Microbiol Biotechnol 5:123–127. https://doi.org/10.1007/BF00498806
Gu YF, Liang J, Xiao H et al (2007) Research of soil pollution by ground crude oil of the daqing oil filed. Environ Sci Manag 9:50–52
Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinf 11:11. https://doi.org/10.1186/1471-2105-11-119
Hyun DW, Jeong YS, Lee JY et al (2021) Description of Nocardioides piscis sp. nov., Sphingomonas piscis sp. nov. and Sphingomonas sinipercae sp. nov., isolated from the intestine of fish species Odontobutis interrupta (Korean spotted sleeper) and Siniperca scherzeri (leopard mandarin fish). J Microbiol 59:552–562
Jung CM, Broberg C, Giuliani J et al (2002) Characterization of JP-7 jet fuel degradation by the bacterium Nocardioides luteus strain BAFB. J Basic Microbiol Int J Biochem Physiol Genetics Morphol Ecol Microorg 42(2):127–131
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 Ez Taxone: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62(3):716–721. https://doi.org/10.1099/ijs.0.038075-0
Komagata K, Suzuki K (1988) Lipid and cell-wall analysis in bacterial systematics. Methods Microbiol 19:161–207. https://doi.org/10.1016/S0580-9517(08)70410-0
Kovacs N (1956) Identification of Pseudomonas pyocyanea by the oxidase reaction. Nature 178:703–703. https://doi.org/10.1038/178703a178700
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 5:122359–122367. https://doi.org/10.1080/01483918208067640
Kubota M, Kawahara K, Sekiya K et al (2005) Nocardioides aromaticivorans sp. nov., a dibenzofuran-degrading bacterium isolated from dioxin-polluted environments. Syst Appl Microbiol 28(2):165–174. https://doi.org/10.1016/j.syapm.2004.10.002
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 70 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw1054
Li LC (2007) Designing PCR primer for DNA methylation mapping. Methods mol biol (Clifton, N.J.) 402:371–384. https://doi.org/10.1007/978-1-59745-528-2_19
Liao X, Lai Q, Yang J, Dong C, Li D, Shao Z (2020) Alcanivorax sediminis sp. nov., isolated from deep-sea sediment of the Pacific Ocean. Int J Syst Evol Microbiol 70:4280–4284. https://doi.org/10.1099/ijsem.0.004285
Lin SY, Wen CZ, Hameed A, Liu YC (2015) Nocardioides Echinoideorum sp. nov., isolated from sea urchins (Tripneustes gratilla). Int J Syst Evol Microbiol 65:1953–1958. https://doi.org/10.1099/ijs.0.000206
Liu Q, Xin YH, Liu HC, Zhou YG, Wen Y (2013) Nocardioides szechwanensis sp. nov. and Nocardioides psychrotolerans sp. nov., isolated from a glacier. Int J Syst Evol Microbiol 63:129–133. https://doi.org/10.1099/ijs.0.038091-0
Luo C, Rodriguez-r LM, Konstantinidis KT (2014) MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences. Nucl Acids Res 42(8):e73–e73
Meier-Kolthoff JP, Klenk H, Göker M (2014) Taxonomic use of DNA G + C content and DNA–DNA hybridization in the genomic age. Int J Syst Evol Microbiol 64:352–356
Minnikin DE, Collins MD, Goodfellow M (1979) Fatty acid and polar lipid composition in the classification of Cellulomonas, Oerskovia and related taxa. J Appl Bacteriol 47:87–95. https://doi.org/10.1111/j.1365-2672.1979.tb01172.x
Minnikin DE, Hutchinson IG, Caldicott AB, Goodfellow M (1980) Thin layer chromatography of methanolysates of mycolic acid-containing bacteria. J Chromatogr 188:221–233
Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M, Schaala A, Parletta JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241. https://doi.org/10.1016/0167-7012(84)90018-6
Park YJ, Jeong SE, Jung HS, Park SY, Jeon CO (2018) Nocardioides currus sp. nov., isolated from a mobile car air-conditioning system. Int J Syst Evol Microbiol 68:2977–2982. https://doi.org/10.1099/ijsem.0.002933
Prauser H (1976) Nocardioides, a new genus of the order Actinomycetales. Int J Syst Evol Microbiol 26:58–65. https://doi.org/10.1099/00207713-26-1-58
Qi J, Wang B, Hao B-I (2004) Whole proteome prokaryote phylogeny without sequence alignment: a K-string composition approach. J Mol Evol 58:1–11. https://doi.org/10.1007/s00239-003-2493-7
Richter M, Rossellómóra R, Glöckner FO, Peplies J (2015) JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32:929. https://doi.org/910.1093/bioinformatics/btv1681
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Schippers A, Schumann P, Spröer C (2005) Nocardioides oleivorans sp. nov., a novel crude-oil-degrading bacterium. Int J Syst Evol Microbiol 55(4):1501–1504. https://doi.org/10.1099/ijs.0.63500-0
Suh MK, Lee KC, Kim JS, Han IL, Kim HS, Eom MK, Shin YK, Lee JS (2021) Nocardioides cynanchi sp. nov., isolated from soil of rhizosphere of Cynanchum Wilfordii. Int J Syst Evol Microbiol 71(2):004640. https://doi.org/10.1099/ijsem.0.004640
Tamura K et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739
Wu S, Zhou Z, Wang D, Wang G (2019) Nocardioides gansuensis sp. nov., isolated from geopark soil. Int J Syst Evol Microbiol 69(2):390–396
Xiang W, Liu C, Wang X, Du J, Xi L, Huang Y (2011) Actinoalloteichus nanshanensis sp. nov., isolated from the rhizosphere of a fig tree (Ficus religiosa). IntJ Syst Evol Microbiol 61:1165–1169. https://doi.org/10.1099/ijs.0.023283-0
Xu P, Li WJ, Tang SK, Zhang YQ, Chen GZ, 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. https://doi.org/10.1099/ijs.0.63407-0
Yi H, Chun J (2004) Nocardioides aestuarii sp. nov., isolated from tidal flat sediment. Int J Syst Evol Microbiol 54:2151–2154. https://doi.org/10.1099/ijs.0.63192-0
Yokota A, Tamura T, Hasegawa T, Huang LH (1993) Catenuloplanes japonicus gen. nov., sp. nov., nom. rev., a new genus of the order Actinomycetales. Int J Syst Evol Microbiol 43:805–812
Yoon JH, Cho YG, Lee ST et al (1999) Nocardioides nitrophenolicus sp. nov., a p-nitrophenol-degrading bacterium. Int J Syst Evol Microbiol 49(2):675–680. https://doi.org/10.1099/00207713-49-2-675
Yoon JH, Kang SJ, Park S, Oh TK (2007) Devosia insulae sp. nov., isolated from soil, and emended description of the genus Devosia. Int J Syst Evol Microbiol 57:1310–1314. https://doi.org/10.1099/ijs.0.65028-0
Yousaf S, Afzal M, Reichenauer TG, Brady CL, Sessitsch A (2011) Hydrocarbon degradation, plant colonization and gene expression of alkane degradation genes by endophytic Enterobacter ludwigii strains. Environ Pollut 159(10):2675–2683
Yuan L, Wu Y, Fan Q et al (2023) Remediating petroleum hydrocarbons in highly saline–alkali soils using three native plant species. J Environ Manag 339:117928
Zhang HX, Wang K, Xu ZX, Chen GJ, Du ZJ (2016) Nocardioides gilvus sp. nov., isolated from Namtso Lake. Antonie Van Leeuwenhoek 109:1367–1374. https://doi.org/10.1007/s10482-016-0735-0
Zhang LY, Ming H, Zhao ZL, Ji WL, Salam N, Jiao JY, Fang BZ, Li WJ, Nie GX (2018) Nocardioides allogilvus sp. nov., a novel actinobacterium isolated from a karst cave. Int J Syst Evol Microbiol 68:2485–2490. https://doi.org/10.1099/ijsem.0.002863
Zhu L, Wang Y, Ding Y, Luo K, Yang B, Yang S, Liu S, Cui H, Wei W (2022) Alcanivorax limicola sp. nov., isolated from a soda alkali-saline soil. Arch Microbiol 204(1):106. https://doi.org/10.1007/s00203-021-02638-3
Acknowledgements
We thank all the laboratory members for their critical reviews and comments on this manuscript, and we thank Sai Yang for the sample collection and Xin Zhang for the help during the experiment.
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This work was financially supported by the National Natural Science Foundation of China [31770543, 41503068, 31600069], Priority Academic Program Development of Jiangsu Higher Education Institutions [PAPD-2018-87] and the Natural Science Foundation of Jiangsu Province of China [BK20150496, BK20150497].
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This study was conceived and designed by LZ and WW, BYY and WJG performed the experiments. XX and SKL provided guidance on data analysis. XYH analyzed the data and drafted the manuscript. All authors reviewed this manuscript.
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Zhu, L., Yang, B., Guo, W. et al. Nocardioides limicola sp. nov., an alkaliphilic alkane degrading bacterium isolated from oilfield alkali-saline soil. Antonie van Leeuwenhoek 117, 14 (2024). https://doi.org/10.1007/s10482-023-01907-z
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DOI: https://doi.org/10.1007/s10482-023-01907-z