Abstract
Strain KC13T, a novel desert-adapted, non-motile, Gram-stain-positive, rod-shaped, aerobic bacterium, was isolated from a soil sample collected from the Karakum Desert, Turkmenistan and characterised by a polyphasic approach. Phylogenetic analysis based on 16S rRNA sequences revealed that strain KC13T was a member of the genus Nocardioides, and formed a distinct cluster with Nocardioides luteus DSM 43366T (99.3% sequence identity), Nocardioides albus DSM 43109T (98.9%), Nocardioides panzhihuensis DSM 26487T (98.3%) and Nocardioides albertanoniae DSM 25218T (97.9%). The orthologous average nucleotide identity and digital DNA–DNA hybridization values were in the range of 85.8–91.0% and 30.2–35.9%, respectively, with the type strains of closely related species. The genome size of strain KC13T was 5.3 Mb with a DNA G + C content of 69.7%. Comprehensive genome analyses showed that strain KC13T, unlike its close relatives, had many genes associated with environmental adaptation. Strain KC13T was found to have chemotaxonomic and phenotypic characteristics of members of the genus Nocardioides and some differences from phylogenetic neighbours. Based on the chemotaxonomic, genomic, phenotypic and phylogenetic data, strain KC13T represents a novel species of the genus Nocardioides, for which the name Nocardioides turkmenicus sp. nov. is proposed, and the type strain is KC13T (= JCM 33525T = CGMCC 4.7619T).
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Data availability
The GenBank accession numbers of the 16S rRNA gene sequence and draft genome sequence of strain KC13T are MG770621and JAALAA000000000, respectively.
References
Abdelkader MS, Philippon T, Asenjo JA, Bull AT, Goodfellow M, Ebel R, Jaspars M, Rateb ME (2018) Asenjonamides A-C, antibacterial metabolites isolated from Streptomyces asenjonii strain KNN 42. f from an extreme-hyper arid Atacama desert soil. J Antibiot 71:425–431. https://doi.org/10.1038/s41429-017-0012-0
Atamuradov KI (1994) Paleogeography of turkmenistan. In: Fet V, Atamuradov KI (eds) Biogeography and ecology of Turkmenistan. Springer, pp 49–64
Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9:75. https://doi.org/10.1186/1471-2164-9-75
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021
Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk H-P, Clément C, Ouhdouch Y, van Wezel GP (2016) Taxonomy, physiology, and natural products of Actinobacteria. Microbiol Mol Biol Rev 80:1–43. https://doi.org/10.1128/mmbr.00019-15
Blin K, Shaw S, Augustijn HE, Reitz ZL, Biermann F, Alanjary M, Fetter A, Terlouw BR, Metcalf WW, Helfrich EJ (2023) antiSMASH 7.0: New and improved predictions for detection, regulation, chemical structures and visualisation. Nucleic Acids Res 51:W46–W50. https://doi.org/10.1093/nar/gkad344
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Carro L, Castro JF, Razmilic V, Nouioui I, Pan C, Igual JM, Jaspars M, Goodfellow M, Bull AT, Asenjo JA (2019) Uncovering the potential of novel micromonosporae isolated from an extreme hyper-arid Atacama Desert soil. Sci Rep 9:4678. https://doi.org/10.1038/s41598-019-38789-z
Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, da Costa MS, Rooney AP, Yi H, Xu X-W, De Meyer S (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.0.002516
Collins MD (1985) Analysis of isoprenoid quinones. In: Bergan T (ed) Methods in microbiology. Academic Press, vol. 18, pp 329–366
Evtushenko LI, Krausova VI, Yoon JH (2012) Genus I. Nocardioides Prauser 1976, 61AL. In: Whitman WB, Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Ludwig W, Suzuki K-I, Parte A (eds) Bergey’s manual of systematic bacteriology, vol 5, 2nd edn. Springer, New York, pp 1197–1251
Farris JS (1972) Estimating phylogenetic trees from distance matrices. Am Nat 106:645–668
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Golinska P, del Carmen M-CM, Świecimska M, Yaramis A, Igual JM, Bull AT, Goodfellow M (2020) Modestobacter excelsi sp. nov., a novel actinobacterium isolated from a high altitude Atacama Desert soil. Syst Appl Microbiol 43:126051. https://doi.org/10.1016/j.syapm.2019.126051
Goodfellow M (1971) Numerical taxonomy of some nocardioform bacteria. Microbiology 69:33–80. https://doi.org/10.1099/00221287-69-1-33
Goodfellow M, Nouioui I, Sanderson R, Xie F, Bull AT (2018) Rare taxa and dark microbial matter: novel bioactive actinobacteria abound in Atacama Desert soils. Antonie Van Leeuwenhoek 111:1315–1332. https://doi.org/10.1007/s10482-018-1088-7
Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Suzuki K-i, Ludwig W, Whitman WB (2012) Bergey’s manual of systematic bacteriology, Vol. 5, The Actinobacteria. New York, Springer
Gordon RE, Barnett DA, Handerhan JE, Pang CH-N (1974) Nocardia coeliaca, Nocardia autotrophica, and the nocardin strain. Int J Syst Evol Microbiol 24:54–63. https://doi.org/10.1099/00207713-24-1-54
Han L, Gao C, Jiang Y, Guan P, Liu J, Li L, Xu L, Huang X (2014) Jiangrines A–F and jiangolide from an actinobacterium, Jiangella gansuensis. J Nat Prod 77:2605–2610. https://doi.org/10.1021/np500402a
Heulin T, De Luca G, Barakat M, Gommeaux M, de Groot A, Blanchard L, Ortet P, Achouak W, (2017) In: Stan-Lotter H, Fendrihan S (eds) Bacterial adaptation to hot and dry deserts. Springer Cham
Jones KL (1949) Fresh isolates of actinomycetes in which the presence of sporogenous aerial mycelia is a fluctuating characteristic. J Bacteriol 57:141
Kämpfer P, Kroppenstedt RM (1996) Numerical analysis of fatty acid patterns of coryneform bacteria and related taxa. Can J Microbiol 42:989–1005. https://doi.org/10.1139/m96-128
Kelly K (1964) Color-name charts illustrated with centroid colors. Inter-Society Color Council-National Bureau of Standards, Chicago
Khan IU, Hussain F, Habib N, Xiao M, Ahmed I, Amin A, Zhi X-Y, Li W-J (2017) Nocardioides thalensis sp. nov., isolated from a desert. Int J Syst Evol Microbiol 67:2848–2852. https://doi.org/10.1099/ijsem.0.002032
Kim M, Oh H-S, Park S-C, 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. https://doi.org/10.1099/ijs.0.059774-0
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. https://doi.org/10.1007/BF01731581
Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645. https://doi.org/10.1101/gr.092759.109
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Küster E, Williams S (1964) Selection of media for isolation of streptomycetes. Nature 202:928–929. https://doi.org/10.1038/202928a0
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. John Wiley and Sons, New York, pp 115–175
Lechevalier MP, Lechevalier H (1970) Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J Syst Evol Microbiol 20:435–443. https://doi.org/10.1099/00207713-20-4-435
Lee I, Ouk Kim Y, Park S-C, Chun J (2016) OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 66:1100–1103. https://doi.org/10.1099/ijsem.0.000760
Lefort V, Desper R, Gascuel O (2015) FastME 2.0: a comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol 32:2798–2800. https://doi.org/10.1093/molbev/msv150
Li L-Y, Yang Z-W, Asem MD, Fang B-Z, Salam N, Alkhalifah DHM, Hozzein WN, Nie G-X, Li W-J (2019) Streptomyces desertarenae sp. nov., a novel actinobacterium isolated from a desert sample. Antonie Van Leeuwenhoek 112:367–374. https://doi.org/10.1007/s10482-018-1163-0
Liu S-W, Xue C-M, Li F-N, Sun C-H (2020) Nocardioides vastitatis sp. nov., isolated from Taklamakan desert soil. Int J Syst Evol Microbiol 70:77–82. https://doi.org/10.1099/ijsem.0.003718
Liu S-W, Jadambaa N, Nikandrova AA, Osterman IA, Sun C-H (2022) Exploring the diversity and antibacterial potentiality of cultivable Actinobacteria from the soil of the saxaul forest in Southern Gobi Desert in Mongolia. Microorganisms 10:989. https://doi.org/10.3390/microorganisms10050989
Meier-Kolthoff JP, Göker M (2019) TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 10:2182. https://doi.org/10.1038/s41467-019-10210-3
Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60. https://doi.org/10.1186/1471-2105-14-60
Minnikin D, O’Donnell A, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett J (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
Mohammadipanah F, Wink J (2016) Actinobacteria from arid and desert habitats: diversity and biological activity. Front Microbiol 6:1541. https://doi.org/10.3389/fmicb.2015.01541
Neilson JW, Quade J, Ortiz M, Nelson WM, Legatzki A, Tian F, LaComb M, Betancourt JL, Wing RA, Soderlund CA (2012) Life at the hyperarid margin: novel bacterial diversity in arid soils of the Atacama Desert, Chile. Extremophiles 16:553–566. https://doi.org/10.1007/s00792-012-0454-z
Okoro CK, Brown R, Jones AL, Andrews BA, Asenjo JA, Goodfellow M, Bull AT (2009) Diversity of culturable actinomycetes in hyper-arid soils of the Atacama Desert, Chile. Antonie Van Leeuwenhoek 95:121–133. https://doi.org/10.1007/s10482-008-9295-2
Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M (2020) List of prokaryotic names with standing in nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 70:5607–5612. https://doi.org/10.1099/ijsem.0.004332
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
Quinn GA, Banat AM, Abdelhameed AM, Banat IM (2020) Streptomyces from traditional medicine: sources of new innovations in antibiotic discovery. J Med Microbiol 69:1040. https://doi.org/10.1099/jmm.0.001232
Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci 106:19126–19131. https://doi.org/10.1073/pnas.090641210
Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J (2016) JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32:929–931. https://doi.org/10.1093/bioinformatics/btv681
Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids: MIDI Technical Note 101. DE, MIDI Inc, Newark
Saygin H, Ay H, Guven K, Cetin D, Sahin N (2019) Desertiactinospora gelatinilytica gen. nov., sp. nov., a new member of the family Streptosporangiaceae isolated from the Karakum Desert. Antonie Van Leeuwenhoek 112:409–423. https://doi.org/10.1007/s10482-018-1169-7
Saygin H, Ay H, Guven K, Cetin D, Sahin N (2021a) Comprehensive genome analysis of a novel actinobacterium with high potential for biotechnological applications, Nonomuraea aridisoli sp. nov., isolated from desert soil. Antonie Van Leeuwenhoek 114:1963–1975. https://doi.org/10.1007/s10482-021-01654-z
Saygin H, Ay H, Guven K, Inan-Bektas K, Cetin D, Sahin N (2021b) Saccharopolyspora karakumensis sp. nov., Saccharopolyspora elongata sp. nov., Saccharopolyspora aridisoli sp. nov., Saccharopolyspora terrae sp. nov. and their biotechnological potential revealed by genome analysis. Syst Appl Microbiol 44:126270. https://doi.org/10.1016/j.syapm.2021.126270
Shirling ET, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340
Staneck JL, Roberts GD (1974) Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Environ Microbiol 28:226–231. https://doi.org/10.1128/am.28.2.226-231.1974
Sun Y, Shi Y-L, Wang H, Zhang T, Yu L-Y, Sun H, Zhang Y-Q (2018) Diversity of bacteria and the characteristics of actinobacteria community structure in Badain Jaran Desert and Tengger Desert of China. Front Microbiol 9:1068. https://doi.org/10.3389/fmicb.2018.01068
Tuo L, Dong Y-P, Habden X, Liu J-M, Guo L, Liu X-F, Chen L, Jiang Z-K, Liu S-W, Zhang Y-B (2015) Nocardioides deserti sp. nov., an actinobacterium isolated from desert soil. Int J Syst Evol Microbiol 65:1604–1610. https://doi.org/10.1099/ijs.0.000147
Waitz JA, Horan AC, Kalyanpur M, Lee BK, Loebenberg D, Marquez JA, Miller G, Patel MG (1981) Kijanimicin (Sch 25663), a novel antibiotic produced by Actinomadura kijaniata SCC 1256. J Antibiot 34:1101–1106. https://doi.org/10.7164/antibiotics.34.1101
Waksman SA (1967) The actinomycetes. A summary of current knowledge. Ronald Press, NewYork
Waksman SA (1961) The Actinomycetes. Vol. II. Classification, identification and descriptions of genera and species. Baltimore, Williams & Wilkins
Wattam AR, Davis JJ, Assaf R, Boisvert S, Brettin T, Bun C, Conrad N, Dietrich EM, Disz T, Gabbard JL, Gerdes S, Henry CS, Kenyon RW, Machi D, Mao C, Nordberg EK, Olsen GJ, Murphy-Olson DE, Olson R, Overbeek R, Parrello B, Pusch GD, Shukla M, Vonstein V, Warren A, Xia F, Yoo H, Stevens RL (2017) Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center. Nucleic Acids Res 45:D535–D542. https://doi.org/10.1093/nar/gkw1017
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703. https://doi.org/10.1128/jb.173.2.697-703.1991
White D, Drummond J, Fuqua C (2012) The physiology and biochemistry of prokaryotes. Oxford University Press, New York
Wichner D, Idris H, Houssen WE, McEwan AR, Bull AT, Asenjo JA, Goodfellow M, Jaspars M, Ebel R, Rateb ME (2017) Isolation and anti-HIV-1 integrase activity of lentzeosides A-F from extremotolerant lentzea sp. H45, a strain isolated from a high-altitude Atacama Desert soil. J Antibiot 70:448–453. https://doi.org/10.1038/ja.2016.78
Williams S, Goodfellow M, Alderson G, Wellington E, Sneath P, Sackin M (1983) Numerical classification of Streptomyces and related genera. Microbiology 129:1743–1813. https://doi.org/10.1099/00221287-129-6-1743
Xie F, Rangseekaew P, Pathom-aree W (2022) Actinobacteria from arid environments and their biotechnological applications. In: Rai RV, Bai JA (eds) Natural products from actinomycetes: diversity, ecology and drug discovery. Springer, Singapore, pp 91–118
Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, 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. https://doi.org/10.1099/ijsem.0.001755
Zonn IS, Esenov PE (2014) The Karakum Desert. In: Zonn IS, Kostianoy AG (eds) The turkmen lake altyn asyr and water resources in turkmenistan. Springer, Berlin, Heidelberg, pp 23–37
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This research was supported by Ondokuz Mayis University (OMU), project no. PYO.FEN.1901.16.001.
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HS and NS designed the research. HS performed the genomic data analysis. HS, KG, DC and NS performed the polyphasic taxonomic experiments. HS drafted the manuscript. All authors have read and approved the final version of the manuscript.
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Saygin, H., Guven, K., Cetin, D. et al. Polyphasic characterization and genomic insights into Nocardioides turkmenicus sp. nov. isolated from a desert soil. Antonie van Leeuwenhoek 117, 25 (2024). https://doi.org/10.1007/s10482-023-01920-2
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DOI: https://doi.org/10.1007/s10482-023-01920-2