1887

Abstract

Three chitinolytic, Gram-negative, light pink, capsule-forming, rod-shaped bacterial strains with gliding motion (MYSH2, MJ1a and dk17) were isolated from seashells, soil and foxtail, respectively. Phylogenetic analysis of the 16S rRNA gene sequences and concatenated alignment of 92 core genes indicated that strains MYSH2, MJ1a and dk17 were novel species of the genus and exhibited a high 16S rRNA sequence similarity (i.e. more than 97.2 %) among each other. These novel strains contained summed feature 3 (C ω7 and/or C ω6), iso-C and MK-7 as the predominant fatty acids and menaquinone. According to the CAZys coding gene of KAAS, MYSH2 and MJ1a were interpreted as strains containing both GH18 and 19 family coding genes, except for dk17, which shows only GH19 family genes. These strains likely degrade chitin to chitobiose or directly to -acetyl--glucosamine, which may enhance their chitinolytic capacity, thus making these stains potentially useful for industrial chitin degradation. Based on distinct morphological, physiological, chemotaxonomic and phylogenetic differences from their closest phylogenetic neighbours, we propose that strains MYSH2, MJ1a and dk17 represent three novel species in the genus , for which the names sp. nov. (=KACC 19716=JCM 32787), sp. nov. (=KACC 19906=NBRC 113667) and sp. nov. (=KACC 19907=NBRC 113666) are proposed. An emended description of the genus is proposed.

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2022-06-14
2022-06-28
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References

  1. Rinaudo M. Chitin and chitosan: Properties and applications. Prog Polym Sci 2006; 31:603–632 [View Article]
    [Google Scholar]
  2. Das SN, Madhuprakash J, Sarma PVSRN, Purushotham P, Suma K et al. Biotechnological approaches for field applications of chitooligosaccharides (COS) to induce innate immunity in plants. Crit Rev Biotechnol 2015; 35:29–43 [View Article] [PubMed]
    [Google Scholar]
  3. Purushotham P, Podile AR. Synthesis of long-chain chitooligosaccharides by a hypertransglycosylating processive endochitinase of Serratia proteamaculans 568. J Bacteriol 2012; 194:4260–4271 [View Article] [PubMed]
    [Google Scholar]
  4. Aam BB, Heggset EB, Norberg AL, Sørlie M, Vårum KM et al. Production of chitooligosaccharides and their potential applications in medicine. Mar Drugs 2010; 8:1482–1517 [View Article] [PubMed]
    [Google Scholar]
  5. Madhuprakash J, El Gueddari NE, Moerschbacher BM, Podile AR. Production of bioactive chitosan oligosaccharides using the hypertransglycosylating chitinase-D from Serratia proteamaculans. Bioresour Technol 2015; 198:503–509 [View Article] [PubMed]
    [Google Scholar]
  6. Jeon YJ, Park PJ, Kim SK. Antimicrobial effect of chitooligosaccharides produced by bioreactor. Carbohydr Polym 2001; 44:71–76 [View Article]
    [Google Scholar]
  7. Wang S-L, Lin H-T, Liang T-W, Chen Y-J, Yen Y-H et al. Reclamation of chitinous materials by bromelain for the preparation of antitumor and antifungal materials. Bioresour Technol 2008; 99:4386–4393 [View Article] [PubMed]
    [Google Scholar]
  8. Ngo DN, Kim MM, Kim SK. Chitin oligosaccharides inhibit oxidative stress in live cells. Carbohydr Polym 2008; 74:228–234 [View Article]
    [Google Scholar]
  9. Hamed I, Özogul F, Regenstein JM. Industrial applications of crustacean by-products (chitin, chitosan, and chitooligosaccharides): a review. Trends Food Sci Technol 2016; 48:40–50 [View Article]
    [Google Scholar]
  10. Mukherjee S, Behera PK, Madhuprakash J. Efficient conversion of crystalline chitin to N-acetylglucosamine and N,N’-diacetylchitobiose by the enzyme cocktail produced by Paenibacillus sp. LS1. Carbohydr Polym 2020; 250:116889 [View Article] [PubMed]
    [Google Scholar]
  11. Pankratov TA, Tindall BJ, Liesack W, Dedysh SN. Mucilaginibacter paludis gen. nov., sp. nov. and Mucilaginibacter gracilis sp. nov., pectin-, xylan- and laminarin-degrading members of the family Sphingobacteriaceae from acidic Sphagnum peat bog. Int J Syst Evol Microbiol 2007; 57:2349–2354 [View Article]
    [Google Scholar]
  12. Joung Y, Kim H, Kang H, Lee B-I, Ahn T-S et al. Mucilaginibacter soyangensis sp. nov., isolated from a lake. Int J Syst Evol Microbiol 2014; 64:413–419 [View Article] [PubMed]
    [Google Scholar]
  13. Baik KS, Park SC, Kim EM, Lim CH, Seong CN. Mucilaginibacter rigui sp. nov., isolated from wetland freshwater, and emended description of the genus Mucilaginibacter. Int J Syst Evol Microbiol 2010; 60:134–139 [View Article] [PubMed]
    [Google Scholar]
  14. Chen XY, Zhao R, Tian Y, Kong BH, Li XD et al. Mucilaginibacter polytrichastri sp. nov., isolated from a moss (Polytrichastrum formosum), and emended description of the genus Mucilaginibacter. Int J Syst Evol Microbiol 2014; 64:1395–1400 [View Article] [PubMed]
    [Google Scholar]
  15. Choi L, Zhao X, Song Y, Wu M, Wang G et al. Mucilaginibacter hurinus sp. nov., isolated from briquette warehouse soil. Arch Microbiol 2020; 202:127–134 [View Article] [PubMed]
    [Google Scholar]
  16. Zhang Z, Sun F, Chen Y, Yao L, Chen Z et al. Mucilaginibacter endophyticus sp. nov., an endophytic polysaccharide-producing bacterium isolated from a stem of Miscanthus sinensis. Antonie van Leeuwenhoek 2019; 112:1087–1094 [View Article]
    [Google Scholar]
  17. Huq MA, Akter S, Lee SY. Mucilaginibacter formosus sp. nov., a bacterium isolated from road-side soil. Antonie van Leeuwenhoek 2018; 112:513–521 [View Article]
    [Google Scholar]
  18. Kim MM, Siddiqi MZ, Im WT. Mucilaginibacter ginsenosidivorans sp. nov., isolated from soil of ginseng field. Curr Microbiol 2017; 74:1382–1388 [View Article]
    [Google Scholar]
  19. Liu Q, Siddiqi MZ, Kim MS, Kim SY, Im WT. Mucilaginibacter hankyongensis sp. nov., isolated from soil of ginseng field Baekdu Mountain. J Microbiol 2017; 55:525–530 [View Article] [PubMed]
    [Google Scholar]
  20. Akter S, Huq MA. Mucilaginibacter corticis sp. nov., isolated from bark of Pinus koraiensis. Antonie van Leeuwenhoek 2019; 113:491–498 [View Article]
    [Google Scholar]
  21. Han SI, Lee HJ, Lee HR, Kim KK, Whang KS. Mucilaginibacter polysacchareus sp. nov., an exopolysaccharide-producing bacterial species isolated from the rhizoplane of the herb Angelica sinensis. Int J Syst Evol Microbiol 2012; 62:632–637 [View Article] [PubMed]
    [Google Scholar]
  22. Madhaiyan M, Poonguzhali S, Lee J-S, Senthilkumar M, Lee KC et al. Mucilaginibacter gossypii sp. nov. and Mucilaginibacter gossypiicola sp. nov., plant-growth-promoting bacteria isolated from cotton rhizosphere soils. Int J Syst Evol Microbiol 2010; 60:2451–2457 [View Article] [PubMed]
    [Google Scholar]
  23. Lee HR, Han SI, Rhee KH, Whang KS. Mucilaginibacter herbaticus sp. nov., isolated from the rhizosphere of the medicinal plant Angelica sinensis. Int J Syst Evol Microbiol 2013; 63:2787–2793 [View Article] [PubMed]
    [Google Scholar]
  24. Paiva G, Abreu P, Proença DN, Santos S, Nobre MF et al. Mucilaginibacter pineti sp. nov., isolated from Pinus pinaster wood from a mixed grove of pines trees. Int J Syst Evol Microbiol 2014; 64:2223–2228 [View Article] [PubMed]
    [Google Scholar]
  25. Wang ZY, Wang RX, Zhou JS, Cheng JF, Li YH. An assessment of the genomics, comparative genomics and cellulose degradation potential of Mucilaginibacter polytrichastri strain RG4-7. Bioresour Technol 2020; 297:122389 [View Article] [PubMed]
    [Google Scholar]
  26. Reasoner DJ, Geldreich EE. A new medium for the enumeration and subculture of bacteria from potable water. Appl Environ Microbiol 1985; 49:1–7 [View Article] [PubMed]
    [Google Scholar]
  27. Chhetri G, Kim J, Kim I, Lee B, Jang W et al. Adhaeribacter rhizoryzae sp. nov., a fibrillar matrix-producing bacterium isolated from the rhizosphere of rice plant. Int J Syst Evol Microbiol 2020; 70:5382–5388 [View Article] [PubMed]
    [Google Scholar]
  28. 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]
  29. Pruesse E, Peplies J, Glöckner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012; 28:1823–1829 [View Article] [PubMed]
    [Google Scholar]
  30. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article] [PubMed]
    [Google Scholar]
  31. Felsenstein J. Evolutionary trees from DNA sequences: A maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article] [PubMed]
    [Google Scholar]
  32. Fitch WM. Toward defining the course of evolution: minimum change for a specific tree topology. Systematic Zoology 1971; 20:406 [View Article]
    [Google Scholar]
  33. 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 [View Article] [PubMed]
    [Google Scholar]
  34. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:1–15 [View Article] [PubMed]
    [Google Scholar]
  35. Tatusov RL, Galperin MY, Natale DA, Koonin EV. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 2000; 28:33–36 [View Article] [PubMed]
    [Google Scholar]
  36. Lee I, Ouk Kim Y, Park S-C, Chun J. OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66:1100–1103 [View Article] [PubMed]
    [Google Scholar]
  37. 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] [PubMed]
    [Google Scholar]
  38. Ezaki T, Hashimoto Y, Yabuuchi E. 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 1989; 39:224–229 [View Article]
    [Google Scholar]
  39. Na S-I, Kim YO, Yoon S-H, Ha S, Baek I et al. UBCG: Up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 2018; 56:280–285 [View Article]
    [Google Scholar]
  40. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 2007; 35:W182–5 [View Article] [PubMed]
    [Google Scholar]
  41. Zhang H, Yohe T, Huang L, Entwistle S, Wu P et al. dbCAN2: A meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 2018; 46:W95–W101 [View Article] [PubMed]
    [Google Scholar]
  42. Buck JD. Nonstaining (KOH) method for determination of Gram reactions of marine bacteria. Appl Environ Microbiol 1982; 44:992–993 [View Article] [PubMed]
    [Google Scholar]
  43. Kim I, Chhetri G, Kim J, Kang M, Seo T. Lewinella aurantiaca sp. nov., a carotenoid pigment-producing bacterium isolated from surface seawater. Int J Syst Evol Microbiol 2020; 70:6180–6187 [View Article] [PubMed]
    [Google Scholar]
  44. Breznak JA, Costilow RN. Physicochemical factors in growth. In Methods for General and Molecular Microbiology Washington, DC, USA: ASM Press; 2014 pp 309–329
    [Google Scholar]
  45. Tindall BJ, Sikorski J, Smibert RA, Krieg NR. Phenotypic characterization and the principles of comparative systematics. In Methods for General and Molecular Microbiology Washington, DC, USA: ASM Press; 2014 pp 330–393
    [Google Scholar]
  46. Kim J, Chhetri G, Kim I, Kim H, Kim MK et al. Methylobacterium terrae sp. nov., a radiation-resistant bacterium isolated from gamma ray-irradiated soil. J Microbiol 2019; 57:959–966 [View Article]
    [Google Scholar]
  47. Sasser M. MIDI Sherlock Microbial Identification System. MIDI Inc Technical Note No.101 2009 pp 1–6
  48. Collins MD, Jones D. Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implication. Microbiol Rev 1981; 45:316–354 [View Article] [PubMed]
    [Google Scholar]
  49. 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]
  50. Komagata K, Suzuki KI. 4 lipid and cell-wall analysis in bacterial systematics. Methods Microbiol 1988; 19:161–207
    [Google Scholar]
  51. Chhetri G, Kim J, Kim I, Kim H, Seo T. Hymenobacter setariae sp. nov., isolated from the ubiquitous weedy grass Setaria viridis. Int J Syst Evol Microbiol 2020; 70:3724–3730 [View Article]
    [Google Scholar]
  52. 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]
  53. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article] [PubMed]
    [Google Scholar]
  54. Oyeleye A, Normi YM. Chitinase: diversity, limitations, and trends in engineering for suitable applications. Biosci Rep 2018; 38:BSR2018032300 [View Article] [PubMed]
    [Google Scholar]
  55. Lacombe-Harvey , Brzezinski R, Beaulieu C. Chitinolytic functions in actinobacteria: ecology, enzymes, and evolution. Appl Microbiol Biotechnol 2018; 102:7219–7230 [View Article] [PubMed]
    [Google Scholar]
  56. Gavriilidou A, Gutleben J, Versluis D, Forgiarini F, van Passel MWJ et al. Comparative genomic analysis of Flavobacteriaceae: insights into carbohydrate metabolism, gliding motility and secondary metabolite biosynthesis. BMC Genomics 2020; 21:569 [View Article] [PubMed]
    [Google Scholar]
  57. Urai M, Aizawa T, Nakagawa Y, Nakajima M, Sunairi M. Mucilaginibacter kameinonensis sp., nov., isolated from garden soil. Int J Syst Evol Microbiol 2008; 58:2046–2050 [View Article] [PubMed]
    [Google Scholar]
  58. Kim D-U, Lee H, Kim H, Kim S-G, Park SY et al. Mucilaginibacter carri sp. nov., isolated from a car air conditioning system. Int J Syst Evol Microbiol 2016; 66:1754–1759 [View Article] [PubMed]
    [Google Scholar]
  59. Yoon JH, Kang SJ, Park S, Oh TK. Mucilaginibacter litoreus sp. nov., isolated from marine sand. Int J Syst Evol Microbiol 2012; 62:2822–2827 [View Article] [PubMed]
    [Google Scholar]
  60. Kim JH, Kang SJ, Jung YT, Oh TK, Yoon JH. Mucilaginibacter lutimaris sp. nov., isolated from a tidal flat sediment. Int J Syst Evol Microbiol 2012; 62:515–519 [View Article] [PubMed]
    [Google Scholar]
  61. Ahn J-H, Kim B-C, Joa J-H, Kim S-J, Song J et al. Mucilaginibacter ginsengisoli sp. nov., isolated from a ginseng-cultivated soil. Int J Syst Evol Microbiol 2015; 65:3933–3937 [View Article] [PubMed]
    [Google Scholar]
  62. Chen WM, Hsieh TY, Sheu SY. Mucilaginibacter amnicola sp. nov., isolated from a freshwater creek. Int J Syst Evol Microbiol 2018; 68:394–401 [View Article] [PubMed]
    [Google Scholar]
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