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INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 72, Issue 10

sp. nov., a new cold-adapted member of the family Micrococcaceae isolated from Antarctic fellfield soil No Access

Abstract

An aerobic, Gram-stain-positive and non-spore-forming strain, designated C1-1, was isolated from a fellfield soil sample collected from frost-sorted polygons on Jane Col, Signy Island, Maritime Antarctic. Cells with a size of 0.65–0.9×1.2–1.7 µm have a flagellar motile apparatus and exhibit a rod–coccus growth cycle. Optimal growth conditions were observed at 15–20 °C, pH 7.0 and NaCl concentration up to 0.5 % (w/v) in the medium. The 16S rRNA gene sequence of C1-1 showed the highest pairwise similarity of 98.77 % to NBRC 113092. Phylogenetic trees based on the 16S rRNA and whole-genome sequences revealed that strain C1-1 belongs to the genus and is most closely related to members of the ‘ group’. The G+C content of genomic DNA was 58.95 mol%. The original and orthologous average nucleotide identities between strain C1-1 and NBRC 113092 were 77.15 % and 77.38 %, respectively. The digital DNA–DNA relatedness values between strain C1-1 and NBRC 113092 was 21.6 %. The polar lipid profile was composed mainly of diphosphatidylglycerol, phosphatidylglycerol, phosphatidylinositol and an unidentified glycolipid. The predominant cellular fatty acids were anteiso-C (75 %) and anteiso-C (15.2 %). Menaquinone MK-9(H) (86.4 %) was the major respiratory quinone in strain C1-1. The peptidoglycan type was determined as A3α (-Lys–-Ala; A11.6). Based on all described phylogenetic, physiological and chemotaxonomic characteristics, we propose that strain C1-1 (=DSM 112353=CCM 9148) is the type strain of a novel species sp. nov.

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  • Accepted:
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Keyword(s): Antarctica , Arthrobacter , cold-adapted microorganisms , Micrococcaceae and whole-genome sequencing
Funding
This study was supported by the:
  • Center for Geosphere Dynamics, Charles University (Award UNCE/SCI/006)
    • Principle Award Recipient: CajthamlTomas
  • Ministerstvo Školství, Mládeže a Tělovýchovy (Award LM2018131)
    • Principle Award Recipient: UhlikOndrej
  • Ministerstvo Školství, Mládeže a Tělovýchovy (Award LTAUSA19028)
    • Principle Award Recipient: UhlikOndrej
  • Ministerstvo Školství, Mládeže a Tělovýchovy (Award MSMT No 21-SVV/2020)
    • Principle Award Recipient: VodickovaPatricie
  • Ministerstvo Obrany České Republiky (Award 907930101413)
    • Principle Award Recipient: PajerPetr
© 2022 The Authors
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2024-05-05
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References

  1. Conn HJ, Dimmick I. Soil bacteria similar in morphology to Mycobacterium and Corynebacterium. J Bacteriol 1947; 54:291–303
     [Google Scholar]
  2. Busse H, Arthrobacter WM. Bergey’s man. Syst Archaea Bact 20181–43 [View Article]
     [Google Scholar]
  3. Busse HJ. Review of the taxonomy of the genus Arthrobacter, emendation of the genus arthrobacter sensu lato, proposal to reclassify selected species of the genus Arthrobacter in the novel genera Glutamicibacter gen nov., Paeniglutamicibacter gen. nov., Pseudoglutamicibacter gen. nov., Paenarthrobacter gen. nov. and Pseudarthrobacter gen. nov., and emended description of Arthrobacter. Int J Syst Evol Microbiol 2016; 66:9–37
     [Google Scholar]
  4. Hu Q-W, Chu X, Xiao M, Li C-T, Yan Z-F et al. Arthrobacter deserti sp. nov., isolated from a desert soil sample. Int J Syst Evol Microbiol 2016; 66:2035–2040 [View Article] [PubMed]
     [Google Scholar]
  5. Huang Z, Bao YY, Yuan TT, Wang GX, He LY et al. Arthrobacter nanjingensis sp. nov., a mineral-weathering bacterium isolated from forest soil. Int J Syst Evol Microbiol 1947; 65:365–369 [View Article] [PubMed]
     [Google Scholar]
  6. Kageyama A, Morisaki K, Omura S, Takahashi Y. Arthrobacter oryzae sp. nov. and Arthrobacter humicola sp. nov. Int J Syst Evol Microbiol 2008; 58:53–56 [View Article] [PubMed]
     [Google Scholar]
  7. Lee JS, Lee KC, Pyun YR, Bae KS. Arthrobacter koreensis sp. nov., a novel alkalitolerant bacterium from soil. Int J Syst Evol Microbiol 2003; 53:1277–1280 [View Article] [PubMed]
     [Google Scholar]
  8. Lee SA, Kim JM, Cho H, Kim S-J, Ahn J-H et al. Arthrobacter silviterrae sp. nov., isolated from forest soil. Int J Syst Evol Microbiol 2017; 67:4546–4551 [View Article] [PubMed]
     [Google Scholar]
  9. Park Y, Kook M, Ngo HTT, Kim K-Y, Park S-Y et al. Arthrobacter bambusae sp. nov., isolated from soil of a bamboo grove. Int J Syst Evol Microbiol 2014; 64:3069–3074 [View Article] [PubMed]
     [Google Scholar]
  10. Yan R, Fu Y, Liu D, Jiang S, Ju H et al. Arthrobacter silvisoli sp. nov., isolated from forest soil. Int J Syst Evol Microbiol 2018; 68:3892–3896 [View Article] [PubMed]
     [Google Scholar]
  11. Yan R, Liu D, Fu Y, Zhang Y, Ju H et al. Arthrobacter celericrescens sp. nov., isolated from forest soil. Int J Syst Evol Microbiol 2019; 69:3093–3099 [View Article]
     [Google Scholar]
  12. Yu X-Y, Zhang L, Ren B, Yang N, Liu M et al. Arthrobacter liuii sp. nov., resuscitated from Xinjiang desert soil. Int J Syst Evol Microbiol 2015; 65:896–901 [View Article] [PubMed]
     [Google Scholar]
  13. Zhang D-C, Schumann P, Liu H-C, Xin Y-H, Zhou Y-G et al. Arthrobacter alpinus sp. nov., a psychrophilic bacterium isolated from Alpine soil. Int J Syst Evol Microbiol 2010; 60:2149–2153 [View Article] [PubMed]
     [Google Scholar]
  14. Chang H-W, Bae J-W, Nam Y-D, Kwon H-Y, Park JR et al. Arthrobacter subterraneus sp. nov., isolated from deep subsurface water of the South Coast of Korea. J Microbiol Biotechnol 2007; 17:1875–1879 [PubMed]
     [Google Scholar]
  15. Chen Y-G, Tang S-K, Zhang Y-Q, Li Z-Y, Yi L-B et al. Arthrobacter halodurans sp. nov., a new halotolerant bacterium isolated from sea water. Antonie van Leeuwenhoek 2009; 96:63–70 [View Article] [PubMed]
     [Google Scholar]
  16. Reddy GSN, Aggarwal RK, Matsumoto GI, Shivaji S. Arthrobacter flavus sp. nov., a psychrophilic bacterium isolated from a pond in McMurdo Dry Valley, Antarctica. Int J Syst Evol Microbiol 2000; 50 Pt 4:1553–1561 [View Article] [PubMed]
     [Google Scholar]
  17. Zhang Q, Oh M, Kim JH, Kanjanasuntree R, Konkit M et al. Arthrobacter paludis sp nov., isolated from a marsh. Int J Syst Evol Microbiol 2018; 68:47–51
     [Google Scholar]
  18. Hoang VA, Kim YJ, Nguyen NL, Yang DC. Arthrobacter gyeryongensis sp. nov., isolated from soil of a Gynostemma pentaphyllum field. Int J Syst Evol Microbiol 2014; 64:420–425 [View Article] [PubMed]
     [Google Scholar]
  19. Cheng J, Zhang M-Y, Zhao J-C, Xu H, Zhang Y et al. Arthrobacter ginkgonis sp. nov., an actinomycete isolated from rhizosphere of Ginkgo biloba L. Int J Syst Evol Microbiol 2017; 67:319–324 [View Article] [PubMed]
     [Google Scholar]
  20. Krishnan R, Menon RR, Tanaka N, Busse HJ, Krishnamurthi S et al. Arthrobacter pokkalii sp nov, a novel plant associated actinobacterium with plant beneficial properties, isolated from saline tolerant pokkali rice, Kerala, India. PLoS One 2016; 11:e0150322 [View Article] [PubMed]
     [Google Scholar]
  21. Zhang J, Ma Y, Yu H. Arthrobacter cupressi sp. nov., an actinomycete isolated from the rhizosphere soil of Cupressus sempervirens. Int J Syst Evol Microbiol 2012; 62:2731–2736 [View Article] [PubMed]
     [Google Scholar]
  22. İnce İA, Demirbağ Z, Katı H. Arthrobacter pityocampae sp. nov., isolated from Thaumetopoea pityocampa (Lep., Thaumetopoeidae). Int J Syst Evol Microbiol 2014; 64:3384–3389 [View Article] [PubMed]
     [Google Scholar]
  23. Lee J-Y, Hyun D-W, Soo Kim P, Sik Kim H, Shin N-R et al. Arthrobacter echini sp. nov., isolated from the gut of a purple sea urchin, Heliocidaris crassispina. Int J Syst Evol Microbiol 2016; 66:1887–1893 [View Article] [PubMed]
     [Google Scholar]
  24. Storms V, Devriese LA, Coopman R, Schumann P, Vyncke F et al. Arthrobacter gandavensis sp. nov., for strains of veterinary origin. Int J Syst Evol Microbiol 2003; 53:1881–1884 [View Article] [PubMed]
     [Google Scholar]
  25. Funke G, Hutson RA, Bernard KA, Pfyffer GE, Wauters G et al. Isolation of Arthrobacter spp. from clinical specimens and description of Arthrobacter cumminsii sp. nov. and Arthrobacter woluwensis sp. nov. J Clin Microbiol 1996; 34:2356–2363 [View Article] [PubMed]
     [Google Scholar]
  26. Janssens LE, Wauters G, Charlier J. Identification of Arthrobacter oxydans, Arthrobacter luteolus sp. nov., and Arthrobacter albus sp. nov., isolated from human clinical specimens. Society 2000; 38:2412–2415
     [Google Scholar]
  27. Heyrman J, Verbeeren J, Schumann P, Swings J, De Vos P. Six novel Arthrobacter species isolated from deteriorated mural paintings. Int J Syst Evol Microbiol 2005; 55:1457–1464 [View Article]
     [Google Scholar]
  28. Li Y, Kawamura Y, Fujiwara N, Naka T, Lui H et al. Rhodococcus baikonurensis sp. nov. and Arthrobacter russicus sp. nov.,isolated from air in the Russian space laboratory Mir. Int J Syst Evol Microbiol 2004; 54:827–835
     [Google Scholar]
  29. Liu Q, Xin YH, Chen XL, Liu HC, Zhou YG et al. Arthrobacter ruber sp. nov., isolated from glacier ice. Int J Syst Evol Microbiol 2018; 68:1616–1621 [View Article] [PubMed]
     [Google Scholar]
  30. Liu Q, Liu HC, Zhou YG, Xin YH. Genetic diversity of glacier-inhabiting Cryobacterium bacteria in China and description of Cryobacterium zongtaii sp. nov. and Arthrobacter glacialis sp. nov. Syst Appl Microbiol 2000; 42:168–177 [View Article]
     [Google Scholar]
  31. Margesin R, Schumann P, Zhang D-C, Redzic M, Zhou Y-G et al. Arthrobacter cryoconiti sp. nov., a psychrophilic bacterium isolated from Alpine glacier cryoconite. Int J Syst Evol Microbiol 2012; 62:397–402 [View Article] [PubMed]
     [Google Scholar]
  32. Ganzert L, Bajerski F, Mangelsdorf K, Lipski A, Wagner D. Arthrobacter livingstonensis sp. nov. and Arthrobacter cryotolerans sp. nov., salt-tolerant and psychrotolerant species from Antarctic soil. Int J Syst Evol Microbiol 2012; 61:979–984 [View Article] [PubMed]
     [Google Scholar]
  33. Loveland-Curtze J, Sheridan PP, Gutshall KR, Brenchley JE. Biochemical and phylogenetic analyses of psychrophilic isolates belonging to the Arthrobacter subgroup and description of Arthrobacter psychrolactophilus, sp. nov. Arch Microbiol 2012; 171:355–363 [View Article] [PubMed]
     [Google Scholar]
  34. Reddy GSN, Prakash JSS, Matsumoto GI, Stackebrandt E. Arthrobacter roseus sp. nov., a psychrophilic bacterium isolated from an Antarctic cyanobacterial mat sample. Int J Syst Evol Microbiol 2002; 52:1017–1021 [View Article] [PubMed]
     [Google Scholar]
  35. Wang F, Gai Y, Chen M, Xiao X. Arthrobacter psychrochitiniphilus sp. nov., a psychrotrophic bacterium isolated from Antarctica. Int J Syst Evol Microbiol 2012; 59:2759–2762 [View Article] [PubMed]
     [Google Scholar]
  36. White PL, Wynn-Williams DD, Russell NJ. Diversity of thermal responses of lipid composition in the membranes of the dominant culturable members of an Antarctic fellfield soil bacterial community. Antartic science 2000; 12:386–393 [View Article]
     [Google Scholar]
  37. Kim M, Oh HS, Park SC, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article]
     [Google Scholar]
  38. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article] [PubMed]
     [Google Scholar]
  39. Jeon Y-S, Lee K, Park S-C, Kim B-S, Cho Y-J et al. EzEditor: a versatile sequence alignment editor for both rRNA- and protein-coding genes. Int J Syst Evol Microbiol 2014; 64:689–691 [View Article] [PubMed]
     [Google Scholar]
  40. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article]
     [Google Scholar]
  41. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article] [PubMed]
     [Google Scholar]
  42. Fitch WM. Toward defining the course of evolution: minimum change for a specific tree topology. Syst Biol 1971; 20:406–416 [View Article]
     [Google Scholar]
  43. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing latforms. Mol Biol Evol 2018; 35:1547–1549 [View Article]
     [Google Scholar]
  44. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16:111–120 [View Article]
     [Google Scholar]
  45. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783 [View Article] [PubMed]
     [Google Scholar]
  46. Lopez-Echartea E, Suman J, Smrhova T, Ridl J, Pajer P et al. Genomic analysis of dibenzofuran-degrading Pseudomonas veronii strain pvy reveals its biodegradative versatility. G3 2020; 11:jkaa030 [View Article]
     [Google Scholar]
  47. Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH et al. Canu: scalable and accurate long-read assembly via adaptive k -mer weighting and repeat separation. Genome Res 1985; 27:722–736 [View Article]
     [Google Scholar]
  48. Vaser R, Sović I, Nagarajan N, Šikić M. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res 2017; 27:737–746 [View Article]
     [Google Scholar]
  49. Loman NJ, Quick J, Simpson JT. A complete bacterial genome assembled de novo using only nanopore sequencing data. Nat Methods 2017; 12:733–735 [View Article]
     [Google Scholar]
  50. Arumugam K, Bağcı C, Bessarab I, Beier S, Buchfink B et al. Annotated bacterial chromosomes from frame-shift-corrected long-read metagenomic data. Microbiome 2019; 7:61 [View Article]
     [Google Scholar]
  51. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods 2015; 12:59–60 [View Article]
     [Google Scholar]
  52. O’Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res 2016; 44:D733–45 [View Article]
     [Google Scholar]
  53. Lee I, Ouk Kim Y, Park S-C, Chun J. OrthoANI: n improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66:1100–1103 [View Article]
     [Google Scholar]
  54. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009; 106:19126–19131 [View Article]
     [Google Scholar]
  55. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article]
     [Google Scholar]
  56. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [View Article]
     [Google Scholar]
  57. Bartholomew JW. Variables influencing results, and the precise definition of steps in Gram staining as a means of standardizing the results obtained. Stain Technol 1962; 37:139–155 [View Article]
     [Google Scholar]
  58. Gregersen T. Rapid method for distinction of gram-negative from Gram-positive bacteria. European J Appl Microbiol Biotechnol 1978; 5:123–127 [View Article]
     [Google Scholar]
  59. Jain A, Jain R, Jain S. Motility testing – hanging drop method and stab. In Basic Techniques in Biochemistry, Microbiology and Molecular Biology Humana, New York, NY: Springer Protocols Handbooks; 2020 pp 121–122 [View Article]
     [Google Scholar]
  60. Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M et al. An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 1984; 2:233–241 [View Article]
     [Google Scholar]
  61. Dyńska-Kukulska K, Ciesielski W, Zakrzewski R. The use of a new, modified Dittmer–Lester spray reagent for phospholipid determination by the TLC image analysis technique. Biomed Chromatogr 2013; 27:458–465 [View Article]
     [Google Scholar]
  62. Řezanka T, Nedbalová L, Elster J, Cajthaml T, Sigler K. Very-long-chain iso and anteiso branched fatty acids in N-acylphosphatidylethanolamines from a natural cyanobacterial mat of Calothrix sp. Phytochemistry 2013; 70:655–663 [View Article]
     [Google Scholar]
  63. Schumann P. Peptidoglycan structure. In Methods in Microbiology vol 38 Elsevier Ltd; 2011 pp 101–129 [View Article]
     [Google Scholar]
  64. Tindall BJ. Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol Lett 1990; 66:199–202 [View Article]
     [Google Scholar]
  65. Vieira S, Huber KJ, Neumann-Schaal M, Geppert A, Luckner M et al. Usitatibacter rugosus gen nov., sp. nov. and Usitatibacter palustris sp. nov., novel members of Usitatibacteraceae fam. nov. within the order Nitrosomonadales isolated from soil. Int J Syst Evol Microbiol 2021; 71:
     [Google Scholar]
  66. Schleifer KH, Kandler O. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 1972; 36:407–477 [View Article]
     [Google Scholar]
  67. DSMZ Nomenclature of peptidoglycan structures of cross-linkage types A and B, with examples of DSMZ strains having specific peptidoglycan types; 2022 www.dsmz.de/collection/catalogue/microorganisms/special-groups-of-organisms/peptidoglycans
  68. Tvrzová L, Schumann P, Spröer C, Sedláček I, Verbarg S et al. Polyphasic taxonomic study of strain CCM 2783 resulting in the description of Arthrobacter stackebrandtii sp. nov. Int J Syst Evol Microbiol 2005; 55:805–808 [View Article] [PubMed]
     [Google Scholar]
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Arthrobacter polaris sp. nov., a new cold-adapted member of the family Micrococcaceae isolated from Antarctic fellfield soil
Int J Syst Evol Microbiol 72, 005541 (2022); https://doi.org/10.1099/ijsem.0.005541
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