1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 73, Issue 9

sp. nov., a brown-black pigment producing actinomycete isolated from dry mudflat sand No Access

Abstract

A novel Gram-stain-positive, aerobic actinobacterial strain, designated GXMU-J15, was isolated from dry mudflat sand. A polyphasic approach was employed for its taxonomic characterization. The strain developed extensively branched yellowish white to light yellow substrate mycelia and white aerial mycelia, and produced smooth cylindrical spores in a loose straight spore chain on International Project 2–7 agar media. Strain GXMU-J15 grew at 20–50 °C (optimum, 35 °C), at pH 5.0–8.0 (optimum, pH 7.0) and in the presence of 0–8 % (w/v) NaCl. Analysis of 16S rRNA gene sequences indicated that strain GXMU-J15 represents a member of the genus . Strain GXMU-J15 showed the highest 16S rRNA gene sequence similarity to CGMCC 4.1745 (99.1 %) and CGMCC 4.1883 (98.8 %). Phylogenetic tree analysis based on multilocus sequence analysis (MLSA) and whole genome sequence construction revealed that strain GXMU-J15 was most closely related to PSKA01, DSM 40467 and JCM 4913. The MLSA and genome-to-genome distances between strain GXMU-J15 and its relatives were 0.0418, 0.0443 and 0.0485 and 0.1237, 0.1188 and 0.1179, respectively. The results of orthologous average nucleotide identity and digital DNA–DNA hybridization analysis corroborated the results of the MLSA and whole genome sequence evolution analysis, indicating that the novel isolate represents a distinct species of the genus . The whole-cell sugars of strain GXMU-J15 were xylose, glucose and galactose. The characteristic diamino acid in the cell-wall hydrolysate was -diaminopimelic acid. The lipids contained diphosphatidylglycerol, phosphatidylmethylethanolamine, phosphatidylethanolamine, phosphatidylinositol, phosphatidylglycerol, phosphatidylglycerides, phosphatidylcholine, two phospholipids of an unknown structure containing glucosamine, one unknown phospholipid and two unknown lipids. The major cellular fatty acid components were iso-C, anteiso-C, iso-C and anteiso-C. The main respiratory quinone types were MK-9(H6) and MK-9(H8). The whole genome size of strain GXMU-J15 was 8.68 Mbp, with 71.23 mol% G+C content. Genomic analysis indicated that strain GXMU-J15 has the potential to synthesize polyketides, terpenes and a series of important antibiotics besides the gene cluster for melanin synthesis. Based on these genotypic and phenotypic data, strain GXMU-J15 is proposed to represent a new species of the genus named sp. nov. The type strain is GXMU-J15 (=MCCC 1K08211=JCM 35917).

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): chitinase , melanin , polyphasic taxonomy and Streptomyces fuscus
Funding
This study was supported by the:
  • Innovation Group of Xiangsihu Youth Scholar of Guangxi Minzu University (Award 201706)
    • Principle Award Recipient: NaikunShen
  • Guangxi Key Laboratory of Automatic Detection Technology and Instrument Foundation (Award GXMNPCBC-2022-01)
    • Principle Award Recipient: NaikunShen
  • Scientific Research Project for Introducing High-level Talents of Guangxi Minzu University (Award 2018KJQD17)
    • Principle Award Recipient: NaikunShen
  • Natural Science Foundation of China (Award 32160017, 32060020)
    • Principle Award Recipient: ShenNaikun
  • Science and Technology Major Project of Guangxi Province (Award AB21220020)
    • Principle Award Recipient: HongyanZhang
  • Science and Technology Major Project of Guangxi Province (Award AB21196019)
    • Principle Award Recipient: NaikunShen
© 2023 The Authors
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.006047
2023-09-27
2024-05-08
Loading full text...

Full text loading...

References

  1. Alimi BA, Pathania S, Wilson J, Duffy B, Frias JMC. Extraction, quantification, characterization, and application in food packaging of chitin and chitosan from mushrooms: a review. Int J Biol Macromol 2023; 237:124195 [View Article] [PubMed]
     [Google Scholar]
  2. Amiri H, Aghbashlo M, Sharma M, Gaffey J, Manning L et al. Chitin and chitosan derived from crustacean waste valorization streams can support food systems and the UN sustainable development goals. Nat Food 2022; 3:822–828 [View Article] [PubMed]
     [Google Scholar]
  3. Kobayashi H, Sagawa T, Fukuoka A. Catalytic conversion of chitin as a nitrogen-containing biomass. Chem Commun 2023; 59:6301–6313 [View Article] [PubMed]
     [Google Scholar]
  4. Zhang Y, Luo X, Yin L, Yin F, Zheng W et al. Isolation and screening of a chitin deacetylase producing Bacillus cereus and its potential for chitosan preparation. Front Bioeng Biotechnol 2023; 11:1183333 [View Article]
     [Google Scholar]
  5. Gîjiu CL, Isopescu R, Dinculescu D, Memecică M, Apetroaei M-R et al. Crabs marine waste-a valuable source of chitosan: tuning chitosan properties by chitin extraction optimization. Polymers 2022; 14:21 [View Article] [PubMed]
     [Google Scholar]
  6. Said Al Hoqani HA, Al-Shaqsi N, Hossain MA, Al Sibani MA. Isolation and optimization of the method for industrial production of chitin and chitosan from Omani shrimp shell. Carbohydr Res 2020; 492:108001 [View Article] [PubMed]
     [Google Scholar]
  7. Dwyer K, Bentley IS, Fitzpatrick DA, Saleh AA, Tighe E et al. Recombinant production, characterization and industrial application testing of a novel acidic exo/endo-chitinase from Rasamsonia emersonii. Extremophiles 2023; 27:10 [View Article] [PubMed]
     [Google Scholar]
  8. Li RK, Hu YJ, He YJ, Ng TB, Zhou ZM et al. A thermophilic chitinase 1602 from the marine bacterium Microbulbifer sp. BN3 and its high-level expression in Pichia pastoris. Biotechnol Appl Biochem 2021; 68:1076–1085 [View Article] [PubMed]
     [Google Scholar]
  9. Xie J, Zhang H, Xu X, Li S, Jiang M et al. Streptomyces beihaiensis sp. nov., a chitin-degrading actinobacterium, isolated from shrimp pond soil. Int J Syst Evol Microbiol 2023; 73: [View Article] [PubMed]
     [Google Scholar]
  10. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol 1966; 16:313–340 [View Article]
     [Google Scholar]
  11. O’Donnell AG, Falconer C, Goodfellow M, Ward AC, Williams E. Biosystematics and diversity amongst novel carboxydotrophic actinomycetes. Antonie van Leeuwenhoek 1993; 64:325–340 [View Article] [PubMed]
     [Google Scholar]
  12. Abildgren MP, Lund F, Thrane U, Elmholt S. Czapek-Dox agar containing iprodione and dicloran as a selective medium for the isolation of Fusarium species. Lett Appl Microbiol 1987; 5:83–86 [View Article]
     [Google Scholar]
  13. Waksman SA. The Actinomycetes. Vol. II. Classification, Identification and Descriptions of Genera and Species Baltimore: Williams and Wilkins; 1961
     [Google Scholar]
  14. Abdukhakimova D, Markhametova Z, Shamkeeva S, Zhulamanova A, Trenozhnikova L et al. Characterizationharacterization of extremophilic actinomycetes strains as sources of antimicrobial agents. Methods Mol Biol 2021; 2296:59–75 [View Article] [PubMed]
     [Google Scholar]
  15. Tripathi N, Sapra A. Gram staining. In StatPearls Treasure Island (FL): 2023
     [Google Scholar]
  16. Kelly K. Inter-Society Color Council-National Bureau of Standards Color Name Charts Illustrated with Centroid Colors Washington, DC: US Government Printing Office; 1964
     [Google Scholar]
  17. Klanbut K, Rattanakavil T, Duangupama T, Suriyachadkun C, Herron PR et al. Streptomyces salinarius sp. nov., an actinomycete isolated from solar saltern soil. Int J Syst Evol Microbiol 2023; 73: [View Article] [PubMed]
     [Google Scholar]
  18. Pridham TG, Gottlieb D. The utilization of carbon compounds by some actinomycetales as an aid for species determination. J Bacteriol 1948; 56:107–114 [View Article] [PubMed]
     [Google Scholar]
  19. Maiti PK, Mandal S. Lentzea indica sp. nov., a novel actinobacteria isolated from Indian Himalayan-soil. Antonie van Leeuwenhoek 2020; 113:1411–1423 [View Article] [PubMed]
     [Google Scholar]
  20. Maiti PK, Mandal S. Majority of actinobacterial strains isolated from Kashmir Himalaya soil are rich source of antimicrobials and industrially important biomolecules. AiM 2019; 09:220–238 [View Article]
     [Google Scholar]
  21. Williams ST, Goodfellow M, Alderson G, Wellington EMH, Sneath PHA et al. Numerical classification of Streptomyces and related genera. Microbiology 1983; 129:1743–1813 [View Article]
     [Google Scholar]
  22. Staneck JL, Roberts GD. Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 1974; 28:226–231 [View Article] [PubMed]
     [Google Scholar]
  23. Lechevalier HA, Lechevalier MP, Gerber NN. Chemical composition as a criterion in the classification of actinomycetes. Adv Appl Microbiol 1971; 14:47–72 [View Article] [PubMed]
     [Google Scholar]
  24. 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]
  25. Goodfellow M, Collins MD, Minnikin DE. Fatty acid and polar lipid composition in the classification of Kurthia. J Appl Bacteriol 1980; 48:269–276 [View Article] [PubMed]
     [Google Scholar]
  26. Kroppenstedt RM. Separation of bacterial menaquinones by HPLC using Reverse Phase (RP18) and a silver loaded ion exchanger as stationary phases. J Liq Chromatogr 1982; 5:2359–2367 [View Article]
     [Google Scholar]
  27. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. In Usfcc Newsl 1990
     [Google Scholar]
  28. Jiang S, Zhang L, Dai S, Li X. A quick and efficient method for Genomic DNA extraction from actinobacteria. Biotechnology 2007; 17:39–41
     [Google Scholar]
  29. Nakajima Y, Kitpreechavanich V, Suzuki K, Kudo T. Microbispora corallina sp. nov., a new species of the genus Microbispora isolated from Thai soil. Int J Syst Bacteriol 1999; 49 Pt 4:1761–1767 [View Article] [PubMed]
     [Google Scholar]
  30. Wattam AR, Davis JJ, Assaf R, Boisvert S, Brettin T et al. Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center. Nucleic Acids Res 2017; 45:D535–D542 [View Article] [PubMed]
     [Google Scholar]
  31. 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 [View Article] [PubMed]
     [Google Scholar]
  32. 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]
  33. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23:2947–2948 [View Article] [PubMed]
     [Google Scholar]
  34. Tamura K, Stecher G, Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis version 11. Mol Biol Evol 2021; 38:3022–3027 [View Article] [PubMed]
     [Google Scholar]
  35. 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]
  36. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article] [PubMed]
     [Google Scholar]
  37. 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]
  38. 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] [PubMed]
     [Google Scholar]
  39. Tamura K. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol Biol Evol 1992; 9:678–687 [View Article] [PubMed]
     [Google Scholar]
  40. Labeda DP, Dunlap CA, Rong X, Huang Y, Doroghazi JR et al. Phylogenetic relationships in the family Streptomycetaceae using multi-locus sequence analysis. Antonie van Leeuwenhoek 2017; 110:563–583 [View Article] [PubMed]
     [Google Scholar]
  41. Guo Y, Zheng W, Rong X, Huang Y. A multilocus phylogeny of the Streptomyces griseus 16S rRNA gene clade: use of multilocus sequence analysis for streptomycete systematics. Int J Syst Evol Microbiol 2008; 58:149–159 [View Article] [PubMed]
     [Google Scholar]
  42. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article] [PubMed]
     [Google Scholar]
  43. 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] [PubMed]
     [Google Scholar]
  44. Lefort V, Desper R, Gascuel O. FastME 2.0: a comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol 2015; 32:2798–2800 [View Article] [PubMed]
     [Google Scholar]
  45. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article] [PubMed]
     [Google Scholar]
  46. Xu L, Dong Z, Fang L, Luo Y, Wei Z et al. OrthoVenn2: a web server for whole-genome comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res 2019; 47:W52–W58 [View Article] [PubMed]
     [Google Scholar]
  47. Blin K, Shaw S, Augustijn HE, Reitz ZL, Biermann F et al. antiSMASH 7.0: new and improved predictions for detection, regulation, chemical structures and visualisation. Nucleic Acids Res 2023; 51:W46–W50 [View Article] [PubMed]
     [Google Scholar]
  48. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci 2009; 106:19126–19131 [View Article]
     [Google Scholar]
  49. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32:929–931 [View Article] [PubMed]
     [Google Scholar]
  50. 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; 14:1–14 [View Article] [PubMed]
     [Google Scholar]
  51. Pridham TG, Lyons AJ. Streptomyces albus (Rossi-Doria) Waksman et Henrici: taxonomic study of strains labeled Streptomyces albus. J Bacteriol 1961; 81:431–441 [View Article] [PubMed]
     [Google Scholar]
  52. Waksman SA, Henrici AT. The nomenclature and classification of the actinomycetes. J Bacteriol 1943; 46:337–341 [View Article] [PubMed]
     [Google Scholar]
  53. Lechevalier MP, Lechevalier HA. The chemotaxonomy of actinomycetes. In Actinomycete Taxonomy 1980
     [Google Scholar]
  54. Kämpfer P. The family Streptomycetaceae, part I: taxonomy. In The Prokaryotes vol 3 2006 pp 538–604 [View Article]
     [Google Scholar]
  55. Rong X, Huang Y. Taxonomic evaluation of the Streptomyces hygroscopicus clade using multilocus sequence analysis and DNA-DNA hybridization, validating the MLSA scheme for systematics of the whole genus. Syst Appl Microbiol 2012; 35:7–18 [View Article] [PubMed]
     [Google Scholar]
  56. 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 [View Article] [PubMed]
     [Google Scholar]
  57. 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]
  58. Zheng Y, Saitou A, Wang C-M, Toyoda A, Minakuchi Y et al. Genome features and secondary metabolites biosynthetic potential of the class Ktedonobacteria. Front Microbiol 2019; 10:893 [View Article] [PubMed]
     [Google Scholar]
  59. Santhanam R, Rong X, Huang Y, Andrews BA, Asenjo JA et al. Streptomyces bullii sp. nov., isolated from a hyper-arid Atacama Desert soil. Antonie van Leeuwenhoek 2013; 103:367–373 [View Article] [PubMed]
     [Google Scholar]
  60. Kim SB, Falconer C, Williams E, Goodfellow M. Streptomyces thermocarboxydovorans sp. nov. and Streptomyces thermocarboxydus sp. nov., two moderately thermophilic carboxydotrophic species from soil. Int J Syst Bacteriol 1998; 48 Pt 1:59–68 [View Article] [PubMed]
     [Google Scholar]
  61. Maiti PK, Mandal S. Streptomyces cupreus sp. nov., an antimicrobial producing actinobacterium isolated from Himalayan soil. Arch Microbiol 2021; 203:1601–1609 [View Article] [PubMed]
     [Google Scholar]
  62. Kim SB, Goodfellow M. Streptomyces avermitilis sp. nov., nom. rev., a taxonomic home for the avermectin-producing streptomycetes. Int J Syst Evol Microbiol 2002; 52:2011–2014 [View Article] [PubMed]
     [Google Scholar]
  63. Landwehr W, Kämpfer P, Glaeser SP, Rückert C, Kalinowski J et al. Taxonomic analyses of members of the Streptomyces cinnabarinus cluster, description of Streptomyces cinnabarigriseus sp. nov. and Streptomyces davaonensis sp. nov. Int J Syst Evol Microbiol 2018; 68:382–393 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.006047
Loading
Streptomyces fuscus sp. nov., a brown-black pigment producing actinomycete isolated from dry mudflat sand
Int J Syst Evol Microbiol 73, 006047 (2023); https://doi.org/10.1099/ijsem.0.006047
/content/journal/ijsem/10.1099/ijsem.0.006047
/content/journal/ijsem/10.1099/ijsem.0.006047
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error