1887

Abstract

A polyhydroxybutyrate (PHB)-degrading actinomycete, strain SFB5A, was identified as a species of based on its membrane fatty acid profile and the presence of -diaminopimelic acid in the cell wall. It formed sporulating mycelia on most agar media, but flat or wrinkled, moist colonies on trypticase soy agar. Spores were smooth, cylindrical, and borne on long, straight to flexuous chains. It produced a light brown diffusible pigment, but not melanin. Comparison of genomic digital DNA–DNA hybridization (dDDH) and average nucleotide identity (ANI) values indicated that strain SFB5A was related to JCM 4394, GIMV4.0001, JCM 4498 and JCM 4086, plus 11 other species. However, the dDDH and ANI values were well below the species differentiation thresholds of <70 and <95 %, respectively; also, multilocus sequence analysis distances exceeded the species threshold of 0.007. Moreover, strain SFB5A differed from the other species in pigmentation and its ability to catabolize arabinose. Strain SFB5A and 11 of its 15 closest relatives degraded PHB and have genes for extracellular, short-chain-length denatured polyhydroxyalkanoate depolymerases. These enzymes from strain SFB5A and its closest relatives had a type 1 catalytic domain structure, while those from other relatives had a type 2 structure, which differs from type one in the position of a consensus histidine in the active site. Thus, phenotypic and genotypic differences suggest that strain SFB5A represents a new species of for which we propose the name sp. nov. The type strain is SFB5A (=NRRL B-65520=DSM 112030).

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2022-03-08
2024-04-18
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References

  1. Becker B, Lechevalier MP, Lechevalier HA. Chemical composition of cell-wall preparations from strains of various form-genera of aerobic actinomycetes. Appl Microbiol 1965; 13:236–243 [View Article]
    [Google Scholar]
  2. Holt JG, Krieg NR, Sneath PH, Staley JT, Williams ST. Bergey’s Manual of Determinative Bacteriology, 9th edn. Philadelphia, Pennsylvania, USA: Lippincott, Williams and Wilkins; 2000
    [Google Scholar]
  3. Peczynska-Czoch W, Mordarski M. Actinomycete enzymes. In Goodfellow M, Williams ST, Mordarski M. eds Actinomycetes in Biotechnology London, UK: Academic Press; 1988 pp 219–284
    [Google Scholar]
  4. Anderson AJ, Dawes EA. Occurrence, metabolism, metabolic role, and industrial uses of bacterial polyhydroxyalkanoates. Microbiol Rev 1990; 54:450–472 [View Article]
    [Google Scholar]
  5. Jendrossek D, Handrick R. Microbial degradation of polyhydroxyalkanoates. Annu Rev Microbiol 2002; 56:403–432 [View Article] [PubMed]
    [Google Scholar]
  6. Mergaert JA, Webb A, Anderson C, Wouters A, Swings J. Microbial degradation of poly(3-hydroxybutyrate) and poly(3-hydroxybutyrate-co-3-hydroxyvalerate) in soils. Appl Environ Microbiol 1993; 59:3233–3238 [View Article] [PubMed]
    [Google Scholar]
  7. García-Hidalgo J, Hormigo D, Arroyo M, de la Mata I. Novel extracellular PHB depolymerase from Streptomyces ascomycinicus: PHB copolymers degradation in acidic conditions. PLoS One 2013; 8:e71699 [View Article] [PubMed]
    [Google Scholar]
  8. Hsu KJ, Tseng M, Don TM, Yang MK. Biodegradation of poly(β-hydroxybutyrate) by a novel isolate of Streptomyces bangladeshensis 77t-4. Bot Stud 2012; 53:307–313
    [Google Scholar]
  9. Klingbeil B, Kroppenstedt RM, Jendrossek D. Taxonomic identification of Streptomyces exfoliatus K10 and characterization of its poly(3-hydroxybutyrate) depolymerase gene. FEMS Microbiol Lett 1996; 142:215–221 [View Article] [PubMed]
    [Google Scholar]
  10. Martínez V, de Santos PG, García-Hidalgo J, Hormigo D, Prieto MA et al. Novel extracellular medium-chain-length polyhydroxyalkanoate depolymerase from Streptomyces exfoliatus K10 DSMZ 41693: a promising biocatalyst for the efficient degradation of natural and functionalized mcl-PHAs. Appl Microbiol Biotechnol 2015; 99:9605–9615 [View Article] [PubMed]
    [Google Scholar]
  11. Aly M, Tork S, A. Qari H, N. Al-Seeni M. Poly-β-hydroxybutyrate depolymerase from Streptomyces lydicus MM10, isolated from wastewater sample. IJAB 2015; 17:891–900 [View Article]
    [Google Scholar]
  12. Gangoiti J, Santos M, Prieto MA, de la Mata I, Serra JL et al. Characterization of a novel subgroup of extracellular medium-chain-length polyhydroxyalkanoate depolymerases from actinobacteria. Appl Environ Microbiol 2012; 78:7229–7237 [View Article] [PubMed]
    [Google Scholar]
  13. Yashchuk O, Miyazaki SS, Hermida EB. Isolation, purification and some properties of an extracellular phbv depolymerase from streptomyces sp. ssm 5670. Asian J Microbiol Biotech Env Sci 2014; 16:29–33
    [Google Scholar]
  14. Akbar S, Hasan F, Nadhman A, Khan S, Shah AA et al. Production and purification of poly(3-hydroxybutyrate-co-3-hydroxyvalerate) degrading enzyme from Streptomyces sp. AF-111. J Polym Environ 2013; 21:1109–1116 [View Article]
    [Google Scholar]
  15. Allen AD, Anderson WA, Ayorinde F, Eribo BE. Isolation and characterization of an extracellular thermoalkanophilic P(3HB-co-3HV) depolymerase from Streptomyces sp. IN1. Int Biodeterior Biodegrad 2011; 65:777–785 [View Article]
    [Google Scholar]
  16. Kim HJ, Kim DY, Nam JS, Bae KS, Rhee YH. Characterization of an extracellular medium-chain-length poly(3-hydroxyalkanoate) depolymerase from Streptomyces sp. KJ-72. Antonie van Leeuwenhoek 2003; 83:183–189 [View Article] [PubMed]
    [Google Scholar]
  17. Calabia BP, Tokiwa Y. A novel PHB depolymerase from a thermophilic Streptomyces sp. Biotechnol Lett 2006; 28:383–388 [View Article] [PubMed]
    [Google Scholar]
  18. Blevins HM, Blue MkD, Cobbs BD, Ricotilli TA, Kyler SL et al. Characterization of an extracellular polyhydroxyalkanoate depolymerase from Streptomyces sp. SFB5A. J Bioremediat Biodegrad 2018; 09:425 [View Article]
    [Google Scholar]
  19. Mabrouk MM, Sabry SA. Degradation of poly (3-hydroxybutyrate) and its copolymer poly (3-hydroxybutyrate-co-3-hydroxyvalerate) by a marine Streptomyces sp. SNG9. Microbiol Res 2001; 156:323–335 [View Article] [PubMed]
    [Google Scholar]
  20. Yashchuk O, Miyazaki SS. PHB-degrading Streptomyces sp. ssm 5670: isolation, characterization and phb-accumulation. J Pure Appl Microbiol 2014; 8:2823–2830
    [Google Scholar]
  21. Hoang K-C, Lee C-Y, Lai Y-C, Liau C-Y. TH-11, a Streptomyces sp. strain that degrades poly(3-hydroxybutyrate) and poly(ethylene succinate. J Chinese Chem Soc 2008; 55:1214–1220 [View Article]
    [Google Scholar]
  22. Santos M, Gangoiti J, Keul H, Möller M, Serra JL et al. Polyester hydrolytic and synthetic activity catalyzed by the medium-chain-length poly(3-hydroxyalkanoate) depolymerase from Streptomyces venezuelae SO1. Appl Microbiol Biotechnol 2013; 97:211–222 [View Article] [PubMed]
    [Google Scholar]
  23. Knoll M, Hamm TM, Wagner F, Martinez V, Pleiss J. The PHA depolymerase engineering database: a systematic analysis tool for the diverse family of polyhydroxyalkanoate (PHA) depolymerases. BMC Bioinformatics 2009; 10:89 [View Article] [PubMed]
    [Google Scholar]
  24. Viljakainen VR, Hug LA. The phylogenetic and global distribution of bacterial polyhydroxyalkanoate bioplastic-degrading genes. Environ Microbiol 2021; 23:1717–1731 [View Article] [PubMed]
    [Google Scholar]
  25. Schlegel HG, Kaltwasser H, Gottschalk G. A submersion method for culture of hydrogen-oxidizing bacteria: growth physiological studies. Arch Mikrobiol 1961; 38:209–222 [View Article]
    [Google Scholar]
  26. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA. Practical Streptomyces Genetics Norwich, UK: John Innes Centre; 2000
    [Google Scholar]
  27. Edwards U, Rogall T, Blöcker H, Emde M, Böttger EC. Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 1989; 17:7843–7853 [View Article] [PubMed]
    [Google Scholar]
  28. Inoue H, Nojima H, Okayama H. High efficiency transformation of Escherichia coli with plasmids. Gene 1990; 96:23–28 [View Article] [PubMed]
    [Google Scholar]
  29. Rintala H, Nevalainen A, Rönkä E, Suutari M. PCR primers targeting the 16S rRNA gene for the specific detection of streptomycetes. Mol Cell Probes 2001; 15:337–347 [View Article] [PubMed]
    [Google Scholar]
  30. Huang X, Madan A. CAP3: A DNA sequence assembly program. Genome Res 1999; 9:868–877 [View Article] [PubMed]
    [Google Scholar]
  31. 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]
  32. 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]
  33. 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 [View Article] [PubMed]
    [Google Scholar]
  34. 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]
  35. Fitch WM. Toward defining the course of evolution: minimum change for a specific tree topology. Systematic Zoology 1971; 20:406 [View Article]
    [Google Scholar]
  36. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article] [PubMed]
    [Google Scholar]
  37. Labeda DP, Goodfellow M, Brown R, Ward AC, Lanoot B et al. Phylogenetic study of the species within the family Streptomycetaceae. Antonie van Leeuwenhoek 2012; 101:73–104 [View Article] [PubMed]
    [Google Scholar]
  38. Whitman WB, Woyke T, Klenk H-P, Zhou Y, Lilburn TG et al. Genomic encyclopedia of bacterial and archaeal type strains, Phase III: the genomes of soil and plant-associated and newly described type strains. Stand Genomic Sci 2015; 10:26 [View Article] [PubMed]
    [Google Scholar]
  39. Bennett S. Solexa Ltd. Pharmacogenomics 2004; 5:433–438 [View Article]
    [Google Scholar]
  40. Yoon SH, Ha SM, Lim JM, Kwon SJ, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article] [PubMed]
    [Google Scholar]
  41. 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]
  42. 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]
  43. Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH et al. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol 2016; 17:1–14 [View Article] [PubMed]
    [Google Scholar]
  44. Lagesen K, Hallin P, Rødland EA, Staerfeldt H-H, Rognes T et al. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007; 35:3100–3108 [View Article] [PubMed]
    [Google Scholar]
  45. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:421 [View Article] [PubMed]
    [Google Scholar]
  46. 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 [View Article]
    [Google Scholar]
  47. 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]
    [Google Scholar]
  48. Farris JS. Estimating phylogenetic trees from distance matrices. Am Nat 1972; 106:645–668 [View Article]
    [Google Scholar]
  49. Kreft L, Botzki A, Coppens F, Vandepoele K, Van Bel M. PhyD3: a phylogenetic tree viewer with extended phyloXML support for functional genomics data visualization. Bioinformatics 2017; 33:2946–2947 [View Article]
    [Google Scholar]
  50. 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]
  51. Moore WEC, Stackebrandt E, Kandler O, Colwell RR, Krichevsky MI et al. Report of the Ad Hoc Committee on Reconciliation of Approaches to Bacterial Systematics. Int J Syst Evol Microbiol 1987; 37:463–464 [View Article]
    [Google Scholar]
  52. 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]
    [Google Scholar]
  53. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol 1966; 16:313–340 [View Article]
    [Google Scholar]
  54. Williams ST, Davies FL. Use of scanning electron microscope for the examination of actinomycetes. J Gen Microbiol 1967; 48:171–177 [View Article] [PubMed]
    [Google Scholar]
  55. Gerhardt P. Manual of Methods for General Bacteriology Washington, DC, USA: American Society for Microbiology; 1981 pp 409–443
    [Google Scholar]
  56. Balouiri M, Sadiki M, Ibnsouda SK. Methods for in vitro evaluating antimicrobial activity: a review. J Pharm Anal 2016; 6:71–79 [View Article]
    [Google Scholar]
  57. Baron SF, Crossman AN, Malik S, Sidhu P, Nehra K et al. Complete genome sequence of the Streptomyces-specific bacteriophage BRock. Microbiol Resour Announc 2020; 9:e00624-20 [View Article] [PubMed]
    [Google Scholar]
  58. Hasegawa T, Takizawa M, Tanida S. A rapid analysis for chemical grouping of aerobic actinomycetes. J Gen Appl Microbiol 1983; 29:319–322 [View Article]
    [Google Scholar]
  59. 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]
  60. Bryson JL, Mitchell TJ. Improved spraying reagents for the detection of sugars on paper chromatograms. Nature 1951; 167:864 [View Article] [PubMed]
    [Google Scholar]
  61. Nguyen TM, Kim J. A rapid and simple method for identifying bacterial polar lipid components in wet biomass. J Microbiol 2017; 55:635–639 [View Article] [PubMed]
    [Google Scholar]
  62. Sasser M. Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids, MIDI Technical Note 101 Newark, DE, USA: Microbial ID Inc; 1990
    [Google Scholar]
  63. Zhu H-H, Guo J, Yao Q, Yang S-Z, Deng M-R et al. Streptomyces vietnamensis sp. nov., a streptomycete with violet blue diffusible pigment isolated from soil in Vietnam. Int J Syst Evol Microbiol 2007; 57:1770–1774 [View Article] [PubMed]
    [Google Scholar]
  64. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389–3402 [View Article] [PubMed]
    [Google Scholar]
  65. Kimura M. The Neutral Theory of Molecular Evolution Cambridge, UK: Cambridge University Press; 1983 [View Article]
    [Google Scholar]
  66. Holland BR, Huber KT, Dress A, Moulton V. Delta plots: a tool for analyzing phylogenetic distance data. Mol Biol Evol 2002; 19:2051–2059 [View Article] [PubMed]
    [Google Scholar]
  67. Shirling EB, Gottlieb D. Cooperative description of type cultures of Streptomyces.: II. Species descriptions from first study. Int J Syst Bacteriol 1968; 18:69–189 [View Article]
    [Google Scholar]
  68. Shirling EB, Gottlieb D. Cooperative description of type cultures of Streptomyces III. Additional species descriptions from first and second studies. Int J Syst Bacteriol 1968; 18:279–392 [View Article]
    [Google Scholar]
  69. Shirling EB, Gottlieb D. Cooperative description of type cultures of Streptomyces. IV. Species descriptions from the second, third and fourth studies. Int J Syst Bacteriol 1969; 19:391–512 [View Article]
    [Google Scholar]
  70. Shirling EB, Gottlieb D. Cooperative description of type strains of Streptomyces: V. Additional descriptions. Int J Syst Bacteriol 1972; 22:265–394 [View Article]
    [Google Scholar]
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