1887

Abstract

A pink-coloured bacterium (strain KR32) was isolated from cheese and assigned to the ‘ group’. Members of the ‘pink group’ form a stable clade (100 % bootstrap value) and contain the species , and , which share ≥99.0 % 16S rRNA gene sequence similarity. Isolate KR32 showed highest 16S rRNA gene sequence similarity (99.9 %) to DSM 20550. Additional multilocus sequence comparison confirmed the assignment of strain KR32 to the clade ‘pink group’. Average nucleotide identity and digital DNA–DNA hybridization values between isolate KR32 and DSM 20550 were 82.85 and 26.30 %, respectively. The G+C content of the genomic DNA of isolate KR32 was 69.14 mol%. Chemotaxonomic analysis determined anteiso-C as the predominant fatty acid and MK-9(H) as the predominant menaquinone. Polar lipids were diphosphatidylglycerol, phosphatidylglycerol, phosphatidylinositol and monoacyldimannosyl-monoacylglycerol. The peptidoglycan type of the isolate was A3α. The carotenoid bacterioruberin was detected as the major pigment. At 10 °C, strain KR32 grew with increased concentrations of bacterioruberin and production of unsaturated fatty acids. Strain KR32 was a Gram-stain-positive, catalase-positive, oxidase-positive and coccus-shaped bacterium with optimal growth at 27–30 °C and pH 8. The results of phylogenetic and phenotypic analyses enabled the differentiation of the isolate from other closely related species of the ‘pink group’. Therefore, strain KR32 represents a novel species for which the name sp. nov. is proposed. The type strain is KR32 (=DSM 109896=LMG 31480=NCCB 100733).

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2020-03-30
2020-06-04
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References

  1. Harrison FC, Kennedy ME. The red discoloration of cured codfish. Trans R Soc Can 1922; 16:101–152
    [Google Scholar]
  2. Merlino CP. Bartolomeo Bizio's letter to the most Eminent Priest, Angelo Bellani, concerning the phenomenon of the red colored polenta. J Bacteriol 1924; 9:527–543 [CrossRef][PubMed]
    [Google Scholar]
  3. Seel W, Baust D, Sons D, Albers M, Etzbach L et al. Carotenoids are used as regulators for membrane fluidity by Staphylococcus xylosus . Sci Rep 2020; 10:330 [CrossRef][PubMed]
    [Google Scholar]
  4. Conn HJ, Dimmick I. Soil bacteria similar in morphology to Mycobacterium and Corynebacterium . J Bacteriol 1947; 54:291–303 [CrossRef][PubMed]
    [Google Scholar]
  5. Busse H-J, Family I et al. Micrococcaceae Pribram 1929, 361AL emend. In Goodfellow M, Kämpfer P. (editors) Bergey’s Manual of Systematic Bacteriology 5, 2nd ed. New York: Springer; 2012 p 571
    [Google Scholar]
  6. Busse H-J. 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 roseus. Int J Syst Evol Microbiol 2016; 66:9–37 [CrossRef][PubMed]
    [Google Scholar]
  7. Nouioui I, Carro L, García-López M, Meier-Kolthoff JP, Woyke T et al. Genome-Based Taxonomic Classification of the Phylum Actinobacteria . Front Microbiol 2018; 9:2007 [CrossRef][PubMed]
    [Google Scholar]
  8. Bockelmann W, Hoppe-Seyler T. The surface flora of bacterial smear-ripened cheeses from cow's and goat's milk. Int Dairy J 2001; 11:307–314 [CrossRef]
    [Google Scholar]
  9. Delbès C, Ali-Mandjee L, Montel M-C. Monitoring bacterial communities in RAW milk and cheese by culture-dependent and -independent 16S rRNA gene-based analyses. Appl Environ Microbiol 2007; 73:1882–1891 [CrossRef][PubMed]
    [Google Scholar]
  10. Irlinger F, Bimet F, Delettre J, Lefèvre M, Grimont PAD. Arthrobacter bergerei sp. nov. and Arthrobacter arilaitensis sp. nov., novel coryneform species isolated from the surfaces of cheeses. Int J Syst Evol Microbiol 2005; 55:457–462 [CrossRef][PubMed]
    [Google Scholar]
  11. Monnet C, Loux V, Gibrat J-F, Spinnler E, Barbe V et al. The Arthrobacter arilaitensis Re117 genome sequence reveals its genetic adaptation to the surface of cheese. PLoS One 2010; 5:e15489 [CrossRef][PubMed]
    [Google Scholar]
  12. Valdes-Stauber N, Götz H, Busse M. Antagonistic effect of coryneform bacteria from red smear cheese against Listeria species. Int J Food Microbiol 1991; 13:119–130 [CrossRef][PubMed]
    [Google Scholar]
  13. Liu Q, Xin Y-H, Chen X-L, Liu H-C, Zhou Y-G et al. Arthrobacter ruber sp. nov., isolated from glacier ice. Int J Syst Evol Microbiol 2018; 68:1616–1621 [CrossRef][PubMed]
    [Google Scholar]
  14. Dieser M, Greenwood M, Foreman CM. Carotenoid pigmentation in Antarctic heterotrophic bacteria as a strategy to withstand environmental stresses. Arct Antarct Alp Res 2010; 42:396–405 [CrossRef]
    [Google Scholar]
  15. Bowman JP, McCammon SA, Brown MV, Nichols DS, McMeekin TA. Diversity and association of psychrophilic bacteria in Antarctic sea ice. Appl Environ Microbiol 1997; 63:3068–3078 [CrossRef][PubMed]
    [Google Scholar]
  16. Parte AC. LPSN - List of Prokaryotic names with Standing in Nomenclature (bacterio.net), 20 years on. Int J Syst Evol Microbiol 2018; 68:1825–1829 [CrossRef][PubMed]
    [Google Scholar]
  17. Sutthiwong N, Fouillaud M, Valla A, Caro Y, Dufossé L. Bacteria belonging to the extremely versatile genus Arthrobacter as novel source of natural pigments with extended hue range. Food Res Int 2014; 65:156–162 [CrossRef]
    [Google Scholar]
  18. Mandelli F, Miranda VS, Rodrigues E, Mercadante AZ. Identification of carotenoids with high antioxidant capacity produced by extremophile microorganisms. World J Microbiol Biotechnol 2012; 28:1781–1790 [CrossRef][PubMed]
    [Google Scholar]
  19. Fong NJ, Burgess ML, Barrow KD, Glenn DR. Carotenoid accumulation in the psychrotrophic bacterium Arthrobacter agilis in response to thermal and salt stress. Appl Microbiol Biotechnol 2001; 56:750–756 [CrossRef][PubMed]
    [Google Scholar]
  20. Chattopadhyay MK, Jagannadham MV, Vairamani M, Shivaji S. Carotenoid pigments of an antarctic psychrotrophic bacterium Micrococcus roseus: temperature dependent biosynthesis, structure, and interaction with synthetic membranes. Biochem Biophys Res Commun 1997; 239:85–90 [CrossRef][PubMed]
    [Google Scholar]
  21. Wiertz R, Schulz SC, Müller U, Kämpfer P, Lipski A. Corynebacterium frankenforstense sp. nov. and Corynebacterium lactis sp. nov., isolated from raw cow milk. Int J Syst Evol Microbiol 2013; 63:4495–4501 [CrossRef][PubMed]
    [Google Scholar]
  22. 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 [CrossRef][PubMed]
    [Google Scholar]
  23. Zimmermann J, Rückert C, Kalinowski J, Lipski A. Corynebacterium crudilactis sp. nov., isolated from raw cow's milk. Int J Syst Evol Microbiol 2016; 66:5288–5293 [CrossRef][PubMed]
    [Google Scholar]
  24. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [CrossRef][PubMed]
    [Google Scholar]
  25. Edgar RC. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [CrossRef][PubMed]
    [Google Scholar]
  26. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 1993; 10:512–526 [CrossRef][PubMed]
    [Google Scholar]
  27. Tavaré S. Some probabilistic and statistical problems in the analysis of DNA sequences. In Miura RM. editor Some Mathematical Questions in Biology: DNA Sequence Analysis 17 Providence: Am Math Soc; 1986 pp 57–86
    [Google Scholar]
  28. Shoemaker JS, Fitch WM. Evidence from nuclear sequences that invariable sites should be considered when sequence divergence is calculated. Mol Biol Evol 1989; 6:270–289 [CrossRef][PubMed]
    [Google Scholar]
  29. Yang Z. Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J Mol Evol 1994; 39:306–314 [CrossRef][PubMed]
    [Google Scholar]
  30. Reddy GS, 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; 50:1553–1561 [CrossRef][PubMed]
    [Google Scholar]
  31. 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 [CrossRef][PubMed]
    [Google Scholar]
  32. Weber M, Schünemann W, Fuß J, Kämpfer P, Lipski A. Stenotrophomonas lactitubi sp. nov. and Stenotrophomonas indicatrix sp. nov., isolated from surfaces with food contact. Int J Syst Evol Microbiol 2018; 68:1830–1838 [CrossRef][PubMed]
    [Google Scholar]
  33. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [CrossRef][PubMed]
    [Google Scholar]
  34. Lee I, Chalita M, Ha S-M, Na S-I, Yoon S-H et al. ContEst16S: an algorithm that identifies contaminated prokaryotic genomes using 16S RNA gene sequences. Int J Syst Evol Microbiol 2017; 67:2053–2057 [CrossRef][PubMed]
    [Google Scholar]
  35. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [CrossRef][PubMed]
    [Google Scholar]
  36. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [CrossRef][PubMed]
    [Google Scholar]
  37. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [CrossRef][PubMed]
    [Google Scholar]
  38. Liu Q, Xin Y-H, Zhou Y-G, Chen W-X. Multilocus sequence analysis of homologous recombination and diversity in Arthrobacter sensu lato named species and glacier-inhabiting strains. Syst Appl Microbiol 2018; 41:23–29 [CrossRef][PubMed]
    [Google Scholar]
  39. Gerhardt P. Manual of Methods for General Bacteriology Washington, DC: Am Soc Microbiol; 1984
    [Google Scholar]
  40. Harrigan WF. Laboratory Methods in Food Microbiology San Diego: AP; 1998
    [Google Scholar]
  41. Kolari M, Nuutinen J, Salkinoja-Salonen MS. Mechanisms of biofilm formation in paper machine by Bacillus species: the role of Deinococcus geothermalis . J Ind Microbiol Biotechnol 2001; 27:343–351 [CrossRef][PubMed]
    [Google Scholar]
  42. 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 [CrossRef][PubMed]
    [Google Scholar]
  43. Nichols PD, Guckert JB, White DC. Determination of monosaturated fatty acid double-bond position and geometry for microbial monocultures and complex consortia by capillary GC-MS of their dimethyl disulphide adducts. J Microbiol Methods 1986; 5:49–55 [CrossRef]
    [Google Scholar]
  44. White T, Bursten S, Federighi D, Lewis RA, Nudelman E. High-Resolution separation and quantification of neutral lipid and phospholipid species in mammalian cells and sera by multi-one-dimensional thin-layer chromatography. Anal Biochem 1998; 258:109–117 [CrossRef][PubMed]
    [Google Scholar]
  45. Hölzl G, Sohlenkamp C, Vences-Guzmán MA, Gisch N. Headgroup hydroxylation by OlsE occurs at the C4 position of ornithine lipid and is widespread in proteobacteria and bacteroidetes. Chem Phys Lipids 2018; 213:32–38 [CrossRef][PubMed]
    [Google Scholar]
  46. Kaiser P, Surmann P, Vallentin G, Fuhrmann H. A small-scale method for quantitation of carotenoids in bacteria and yeasts. J Microbiol Methods 2007; 70:142–149 [CrossRef][PubMed]
    [Google Scholar]
  47. Etzbach L, Pfeiffer A, Weber F, Schieber A. Characterization of carotenoid profiles in goldenberry (Physalis peruviana L.) fruits at various ripening stages and in different plant tissues by HPLC-DAD-APCI-MS. Food Chem 2018; 245:508–517 [CrossRef][PubMed]
    [Google Scholar]
  48. Annous BA, Becker LA, Bayles DO, Labeda DP, Wilkinson BJ. Critical role of anteiso-C15:0 fatty acid in the growth of Listeria monocytogenes at low temperatures. Appl Environ Microbiol 1997; 63:3887–3894 [CrossRef][PubMed]
    [Google Scholar]
  49. Paściak M, Sanchez-Carballo P, Duda-Madej A, Lindner B, Gamian A et al. Structural characterization of the major glycolipids from Arthrobacter globiformis and Arthrobacter scleromae . Carbohydr Res 2010; 345:1497–1503 [CrossRef][PubMed]
    [Google Scholar]
  50. Dummer AM, Bonsall JC, Cihla JB, Lawry SM, Johnson GC et al. Bacterioopsin-mediated regulation of bacterioruberin biosynthesis in Halobacterium salinarum . J Bacteriol 2011; 193:5658–5667 [CrossRef][PubMed]
    [Google Scholar]
  51. Saito T, Terato H, Yamamoto O. Pigments of Rubrobacter radiotolerans . Arch Microbiol 1994; 162:414–421 [CrossRef]
    [Google Scholar]
  52. O'Donnell AG, Minnikin DE, Goodfellow M, Parlett JH. The analysis of actinomycete wall amino acids by gas chromatography. FEMS Microbiol Lett 1982; 15:75–78 [CrossRef]
    [Google Scholar]
  53. Schleifer KH, Kandler O. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 1972; 36:407–477 [CrossRef][PubMed]
    [Google Scholar]
  54. Nei M, Kumar S. Molecular Evolution and Phylogenetics New York: Oxford University; 2000
    [Google Scholar]
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