1887

Abstract

A polyphasic study was undertaken to establish the position of a strain, isolate PRKS01-65, recovered from sand dune soil collected at Parangkusumo, Yogyakarta Province, Java, Indonesia. A combination of chemotaxonomic, cultural and morphological properties confirmed its position in the genus of . Comparative 16S rRNA gene sequence analyses showed that the isolate was most closely related to C34 (99.9 % similarity) and loosely associated with the type strains of (98.7 % similarity) and (98.9 % similarity). Multilocus sequence analyses based on five conserved housekeeping gene alleles confirmed the close relationship between the isolate and C34, although both strains belonged to a well-supported clade that encompassed the type strains of , , , , and . A comparison of the draft genome sequence generated for the isolate with corresponding whole genome sequences of its closest phylogenomic neighbours showed that it formed a well-separated lineage with C34. These strains can also be distinguished using a combination of phenotypic properties and by average nucleotide identity and digital DNA–DNA hybridization similarities of 94.3 and 56 %, values consistent with their classification in different species. Based on this wealth of data it is proposed that isolate PRKS01-65 (=NCIMB 15211=CCMM B1302=ICEBB-03) be classified as sp. nov. The genome of the isolate contains several biosynthetic gene clusters with the potential to produce new natural products.

Funding
This study was supported by the:
  • Indonesia Endowment Fund for Education (LPDP) (Award PhD scholarship)
    • Principle Award Recipient: Ali Budhi Kusuma
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2024-03-28
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References

  1. Waksman SA, Henrici AT. The nomenclature and classification of the actinomycetes. J Bacteriol 1943; 46:337–341 [View Article][PubMed]
    [Google Scholar]
  2. Nouioui I, Carro L, Garcia-Lopez M, Meier-Kolthoff JP, Woyke T et al. Genome-based-taxonomic classification of the phylum Actinobacteria . Front Microbiol 2007; 2018:9
    [Google Scholar]
  3. 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]
  4. 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]
  5. Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C et al. Taxonomy, physiology, and natural products of actinobacteria. Microbiol Mol Biol Rev 2016; 80:1–43 [View Article][PubMed]
    [Google Scholar]
  6. Katz L, Baltz RH. Natural product discovery: past, present, and future. J Ind Microbiol Biotechnol 2016; 43:155–176 [View Article][PubMed]
    [Google Scholar]
  7. Zhu H, Swierstra J, Wu C, Girard G, Choi YH et al. Eliciting antibiotics active against the ESKAPE pathogens in a collection of actinomycetes isolated from mountain soils. Microbiology 2014; 160:1714–1725 [View Article][PubMed]
    [Google Scholar]
  8. van der Aart LT, Nouioui I, Kloosterman A, Igual J-M, Willemse J et al. Polyphasic classification of the gifted natural product producer Streptomyces roseifaciens sp. nov . Int J Syst Evol Microbiol 2019; 69:899–908 [View Article][PubMed]
    [Google Scholar]
  9. Goodfellow M, Fiedler H-P. A guide to successful bioprospecting: informed by actinobacterial Systematics. Antonie van Leeuwenhoek 2010; 98:119–142 [View Article][PubMed]
    [Google Scholar]
  10. Goodfellow M, Nouioui I, Sanderson R, Xie F, Bull AT. Rare taxa and dark microbial matter: novel bioactive actinobacteria abound in Atacama desert soils. Antonie van Leeuwenhoek 2018; 111:1315–1332 [View Article][PubMed]
    [Google Scholar]
  11. Bull AT, Goodfellow M. Dark, rare and inspirational microbial matter in the extremobiosphere: 16 000 M of bioprospecting campaigns. Microbiology 2019; 165:1252–1264 [View Article][PubMed]
    [Google Scholar]
  12. Sayed AM, Hassan MHA, Alhadrami HA, Hassan HM, Goodfellow M et al. Extreme environments: microbiology leading to specialized metabolites. J Appl Microbiol 2020; 128:630–657 [View Article][PubMed]
    [Google Scholar]
  13. Okoro CK, Brown R, Jones AL, Andrews BA, Asenjo JA et al. Diversity of culturable actinomycetes in hyper-arid soils of the Atacama desert, Chile. Antonie van Leeuwenhoek 2009; 95:121–133 [View Article][PubMed]
    [Google Scholar]
  14. Busarakam K, Bull AT, Girard G, Labeda DP, van Wezel GP et al. Streptomyces leeuwenhoekii sp. nov., the producer of chaxalactins and chaxamycins, forms a distinct branch in Streptomyces gene trees. Antonie van Leeuwenhoek 2014; 105:849–861 [View Article][PubMed]
    [Google Scholar]
  15. Abdelkader MSA, Philippon T, Asenjo JA, Bull AT, Goodfellow M et al. Asenjonamides A–C, antibacterial metabolites isolated from Streptomyces asenjonii strain KNN 42.f from an extreme-hyper arid Atacama desert soil. J Antibiot 2018; 71:425–431 [View Article]
    [Google Scholar]
  16. Rateb ME, Ebel R, Jaspars M. Natural product diversity of actinobacteria in the Atacama desert. Antonie van Leeuwenhoek 2018; 111:1467–1477 [View Article][PubMed]
    [Google Scholar]
  17. Baltz RH. Gifted microbes for genome mining and natural product discovery. J Ind Microbiol Biotechnol 2017; 44:573–588 [View Article][PubMed]
    [Google Scholar]
  18. Gomez-Escribano JP, Castro JF, Razmilic V, Chandra G, Andrews B et al. The Streptomyces leeuwenhoekii genome: de novo sequencing and assembly in single contigs of the chromosome, circular plasmid pSLE1 and linear plasmid pSLE2. BMC Genomics 2015; 16:485 [View Article][PubMed]
    [Google Scholar]
  19. Ziemert N, Alanjary M, Weber T. The evolution of genome mining in microbes - a review. Nat Prod Rep 2016; 33:988–1005 [View Article][PubMed]
    [Google Scholar]
  20. Sekurova ON, Schneider O, Zotchev SB. Novel bioactive natural products from bacteria via bioprospecting, genome mining and metabolic engineering. Microb Biotechnol 2019; 12:828–844 [View Article][PubMed]
    [Google Scholar]
  21. Idris H. Actinobacterial Diversity in Atacama Desert Habitats as a Road Map to Biodiscovery. PhD Thesis Newcastle Upon Tyne, UK.: Newcastle University,; 2016
    [Google Scholar]
  22. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol 1966; 16:313–340 [View Article]
    [Google Scholar]
  23. Goodfellow M, Busarakam K, Idris H, Labeda DP, Nouioui I et al. Streptomyces asenjonii sp. nov., isolated from hyper-arid Atacama desert soils and emended description of Streptomyces viridosporus Pridham et al. 1958. Antonie van Leeuwenhoek 2017; 110:1133–1148 [View Article]
    [Google Scholar]
  24. Staneck JL, Roberts GD. Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 1974; 28:226–231 [View Article]
    [Google Scholar]
  25. Lechevalier MP, Lechevalier H. Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J Syst Bacteriol 1970; 20:435–443 [View Article]
    [Google Scholar]
  26. 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]
  27. Sasser M. Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids vol. 101, MIDI Inc Technical Notes. 1990 p 1
    [Google Scholar]
  28. 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]
  29. Kelly K. Color-Name Charts Illustrated with Centroid Colors Chicago: Inter-Society Color Council-National Bureau of Standards; 1953
    [Google Scholar]
  30. Kämpfer P et al. Genus 1. Streptomyces Waksman and Henrici 1943, 339AL emend. Rainey, Ward-Rainey and Stackebrandt, 1997, 486, emend. Kim, Lonsdale, Seong and Goodfellow 2003b, 113, emend. Zhi, Li and Stackebrandt 2009, 600. In Goodfellow M, Kämpfer P, Busse H-J, Trujillo ME, Suzuki K-I et al. (editors) The Actinobacteria Part B. Bergey’s Manual of Systematic Bacteriology volume 5, 2nd edn. New York: Springer; 2012 pp 1455–1767
    [Google Scholar]
  31. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article][PubMed]
    [Google Scholar]
  32. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. 1000 genome project data processing subgroup, the sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079
    [Google Scholar]
  33. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010; 26:841–842 [View Article][PubMed]
    [Google Scholar]
  34. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article][PubMed]
    [Google Scholar]
  35. 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 Compu Biol 2012; 19:455–477 [View Article]
    [Google Scholar]
  36. 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]
  37. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ et al. The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 2014; 42:D206–D214 [View Article]
    [Google Scholar]
  38. 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 [View Article][PubMed]
    [Google Scholar]
  39. 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]
  40. Edgar RC. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article][PubMed]
    [Google Scholar]
  41. 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][PubMed]
    [Google Scholar]
  42. Meier-Kolthoff JP, Göker M, Spröer C, Klenk H-P. When should a DDH experiment be mandatory in microbial taxonomy?. Arch Microbiol 2013; 195:413–418 [View Article][PubMed]
    [Google Scholar]
  43. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article][PubMed]
    [Google Scholar]
  44. Fitch WM. Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 1971; 20:406 [View Article]
    [Google Scholar]
  45. 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]
  46. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article][PubMed]
    [Google Scholar]
  47. 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]
  48. Jukes TH, Cantor CR. Evolution of Protein Molecules 3 London: Academic Press; 1969 pp 21–132
    [Google Scholar]
  49. Gause GF, Preobrazhenskaya TP. Validation List no. 22. Int J Syst Bacteriol 1986; 36:573–576
    [Google Scholar]
  50. Promnuan Y, Kudo T, Ohkuma M, Chantawannakul P. Streptomyces chiangmaiensis sp. nov. and Streptomyces lannensis sp. nov., isolated from the South-East Asian stingless bee (Tetragonilla collina). Int J Syst Evol Microbiol 2013; 63:1896–1901 [View Article][PubMed]
    [Google Scholar]
  51. Meier-Kolthoff JP, Hahnke RL, Petersen J, Scheuner C, Michael V et al. Complete genome sequence of DSM 30083(T), the type strain (U5/41(T)) of Escherichia coli, and a proposal for delineating subspecies in microbial taxonomy. Stand Genomic Sci 2014; 10:2
    [Google Scholar]
  52. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article][PubMed]
    [Google Scholar]
  53. Pattengale ND, Alipour M, Bininda-Emonds ORP, Moret BME, Stamatakis A. How many bootstrap replicates are necessary?. J Comput Biol 2010; 17:337–354 [View Article][PubMed]
    [Google Scholar]
  54. Goloboff PA, Farris JS, Nixon KC. Tnt, a free program for phylogenetic analysis. Cladistics 2008; 24:774–786 [View Article]
    [Google Scholar]
  55. Swofford D. PAUP*: Phylogenetic Analysis Using Parsimony (* and other methods). Version 4.0 B10 Sunderland: Sinauer Associates; 2002
    [Google Scholar]
  56. Rong X, Huang Y. Multi-Locus sequence analysis: taking prokaryotic systematics to the next level. Meth Microbiol 2014; 41:221–251
    [Google Scholar]
  57. Preobrazhenskaya TP, Blinov NO, Ryabova ID. Gauze GF, Preobrazhenskaya TP, Kudirna ES, Blinov NO, Ryabova ID et al. (editors) Problems of Classification of Actinomycetes-Antagonists Medgiz, Moscow: USSR: Government Publishing House of Medical Literature; 1957 pp 1–398
    [Google Scholar]
  58. Pridham TG, Hesseltine CW, Benedict RG. A guide for the classification of streptomycetes according to selected groups; placement of strains in morphological sections. Appl Microbiol 1958; 6:52–79 [View Article][PubMed]
    [Google Scholar]
  59. Johnson LE, Dietz A. Lomofungin, a new antibiotic produced by Streptomyces lomondensis sp. N. Appl Microbiol 1969; 17:755–759 [View Article][PubMed]
    [Google Scholar]
  60. Lacey J. Nomenclature of Saccharopolyspora erythraea Labeda 1987 and Streptomyces erythraeus (Waksman 1923) Waksman and Henrici 1948, and proposals for the alternative epithet Streptomyces labedae sp. nov. Int J Syst Bacteriol 1987; 37:458 [View Article]
    [Google Scholar]
  61. Diab A, Al-Gounaim MY. Streptomyces spinoverrucosus, a new species from the air of Kuwait. Int J Syst Bacteriol 1982; 32:327–331 [View Article]
    [Google Scholar]
  62. 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]
  63. 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]
  64. 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]
  65. Farris JS. Estimating phylogenetic trees from distance matrices. Am Nat 1972; 106:645–668 [View Article]
    [Google Scholar]
  66. 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]
  67. Wayne LG, Moore WEC, Stackebrandt E, Kandler O, Colwell RR 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]
  68. 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][PubMed]
    [Google Scholar]
  69. Chun J, Rainey FA. Integrating genomics into the taxonomy and systematics of the Bacteria and Archaea . Int J Syst Evol Microbiol 2014; 64:316–324 [View Article][PubMed]
    [Google Scholar]
  70. Bentley SD, Chater KF, Cerdeño-Tárraga A-M, Challis GL, Thomson NR et al. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 2002; 417:141–147 [View Article][PubMed]
    [Google Scholar]
  71. Cruz-Morales P, Vijgenboom E, Iruegas-Bocardo F, Girard G, Yáñez-Guerra LA et al. The genome sequence of Streptomyces lividans 66 reveals a novel tRNA-dependent peptide biosynthetic system within a metal-related genomic island. Genome Biol Evol 2013; 5:1165–1175 [View Article][PubMed]
    [Google Scholar]
  72. Williams ST, Goodfellow M, Alderson G, Wellington EM, Sneath PH et al. Numerical classification of Streptomyces and related genera. J Gen Microbiol 1983; 129:1743–1813 [View Article][PubMed]
    [Google Scholar]
  73. Idris H, Labeda DP, Nouioui I, Castro JF, Del Carmen Montero-Calasanz M, Montero-Calasanz MDC et al. Streptomyces aridus sp. nov., isolated from a high altitude Atacama desert soil and emended description of Streptomyces noboritoensis Isono et al. 1957. Antonie van Leeuwenhoek 2017; 110:705–717 [View Article][PubMed]
    [Google Scholar]
  74. Murray P, Barron E, Phaller M, Ternover J, Yolkken R. Manual of clinical microbiology. Mycopathologia 1999; 146:107–108
    [Google Scholar]
  75. Blin K, Shaw S, Steinke K, Villebro R, Ziemert N et al. antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 2019; 47:W81–W87 [View Article]
    [Google Scholar]
  76. Inahashi Y, Iwatsuki M, Ishiyama A, Matsumoto A, Hirose T et al. Actinoallolides A-E, new anti-trypanosomal macrolides, produced by an endophytic actinomycete, Actinoallomurus fulvus MK10-036. Org Lett 2015; 17:864–867 [View Article][PubMed]
    [Google Scholar]
  77. Higashide E, Hatano K, Shibata M, Enduracidin NK. A new antibiotic I. Streptomyces fungicidicus No. B5477, an enduracidin producing organism. J Antibiot 1968; 21:126–137
    [Google Scholar]
  78. Mandala SM, Thornton RA, Milligan J, Rosenbach M, Garcia-Calvo M et al. Rustmicin, a potent antifungal agent, inhibits sphingolipid synthesis at inositol phosphoceramide synthase. J Biol Chem 1998; 273:14942–14949 [View Article][PubMed]
    [Google Scholar]
  79. MacKintosh C, Klumpp S. Tautomycin from the bacterium Streptomyces verticillatus. another potent and specific inhibitor of protein phosphatases 1 and 2A. FEBS Lett 1990; 277:137–140 [View Article][PubMed]
    [Google Scholar]
  80. Castro JF, Razmilic V, Gomez-Escribano JP, Andrews B, Asenjo J et al. The ‘gifted’ actinomycete Streptomyces leeuwenhoekii . Antonie van Leeuwenhoek 2018; 111:1433–1448 [View Article]
    [Google Scholar]
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