1887

Abstract

An actinobacterial strain, CMB-FB, was isolated from surface-sterilized root nodules of a plant growing along Halsema Highway in the province of Benguet (Luzon, Philippines). The 16S rRNA gene sequence of CMB-FB showed high sequence similarity to those of the type strains of (99.4 %), (99.1 %), subsp. (99.0 %), and (98.6 %). The major menaquinones of CMB-FB were composed of MK-9(H), MK-9(H) and MK-9(H), and there was a minor contribution of MK-9(H). The polar lipid profile consisted of phosphatidylethanolamine, unidentified aminolipids and phospholipids, a glycophospholipid and four unidentified lipids. The diagnostic diamino acid of the peptidoglycan was -diaminopimelic acid. The major fatty acids were iso-C, anteiso-C and anteiso-C. The results of physiological analysis indicated that CMB-FB was mesophilic. The results of phylogenetic, genome-genome distance calculation and average nucleotide identity analysis indicated that the isolated strain represents the type strain of a novel species. On the basis of these results, strain CMB-FB (=DSM 112754=LMG 32457) is proposed as the type strain of the novel species sp. nov.

Funding
This study was supported by the:
  • Bundesministerium für Forschung und Technologie (Award BiGi)
    • Principle Award Recipient: NotApplicable
  • Bundesministerium für Forschung und Technologie (Award FKZ 031A533)
    • Principle Award Recipient: NotApplicable
  • Vetenskapsrådet (Award VR 2012-03061)
    • Principle Award Recipient: KatharinaPawlowski
  • 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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2022-12-13
2024-04-27
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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]
    [Google Scholar]
  2. Salam N, Jiao JY, Zhang XT, Li WJ. Update on the classification of higher ranks in the phylum Actinobacteria. Int J Syst Evol Microbiol 2020; 70:1331–1355 [View Article]
    [Google Scholar]
  3. Kämpfer P et al. The family Streptomycetaceae, Part I: Taxonomy. In Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E. eds The Prokaryotes vol 3 New York: Springer; 2006 pp 538–604 [View Article]
    [Google Scholar]
  4. Ward AC, Allenby NE. Genome mining for the search and discovery of bioactive compounds: the Streptomyces paradigm. FEMS Microbiol Lett 2018; 365: [View Article]
    [Google Scholar]
  5. Olanrewaju OS, Babalola OO. Streptomyces: implications and interactions in plant growth promotion. Appl Microbiol Biotechnol 2019; 103:1179–1188 [View Article]
    [Google Scholar]
  6. Goudjal Y, Toumatia O, Sabaou N, Barakate M, Mathieu F et al. Endophytic actinomycetes from spontaneous plants of Algerian Sahara: indole-3-acetic acid production and tomato plants growth promoting activity. World J Microbiol Biotechnol 2013; 29:1821–1829 [View Article]
    [Google Scholar]
  7. Vurukonda SSKP, Giovanardi D, Stefani E. Plant growth promoting and biocontrol activity of Streptomyces spp. as endophytes. Int J Mol Sci 2018; 19:E952 [View Article]
    [Google Scholar]
  8. Loria R, Kers J, Joshi M. Evolution of plant pathogenicity in Streptomyces. Annu Rev Phytopathol 2006; 44:469–487 [View Article]
    [Google Scholar]
  9. Bignell DRD, Huguet-Tapia JC, Joshi MV, Pettis GS, Loria R. What does it take to be a plant pathogen: genomic insights from Streptomyces species. Antonie Van Leeuwenhoek 2010; 98:179–194 [View Article]
    [Google Scholar]
  10. Pawlowski K, Demchenko KN. The diversity of actinorhizal symbiosis. Protoplasma 2012; 249:967–979 [View Article] [PubMed]
    [Google Scholar]
  11. Deng ZS, Zhao LF, Kong ZY, Yang WQ, Lindström K et al. Diversity of endophytic bacteria within nodules of the Sphaerophysa salsula in different regions of Loess Plateau in China. FEMS Microbiol Ecol 2011; 76:463–475 [View Article]
    [Google Scholar]
  12. Pandya M, Rajput M, Rajkumar S. Exploring plant growth promoting potential of non rhizobial root nodules endophytes of Vigna radiata. Microbiology 2015; 84:80–89 [View Article]
    [Google Scholar]
  13. Yokoyama J, Suzuki M, Iwatsuki K, Hasebe M. Molecular phylogeny of Coriaria, with special emphasis on the disjunct distribution. Mol Phylogenet Evol 2000; 14:11–19 [View Article]
    [Google Scholar]
  14. Nguyen TV, Wibberg D, Vigil-Stenman T, Berckx F, Battenberg K et al. Frankia-enriched metagenomes from the earliest diverging symbiotic Frankia cluster: they come in teams. Genome Biol Evol 2019; 11:2273–2291 [View Article]
    [Google Scholar]
  15. Liu J, Wang H, Yang H, Zhang Y, Wang J et al. Composition-based classification of short metagenomic sequences elucidates the landscapes of taxonomic and functional enrichment of microorganisms. Nucleic Acids Res 2013; 41:e3 [View Article]
    [Google Scholar]
  16. Wilson K. Preparation of genomic DNA from bacteria. In Ausubel FM, Brent R, Kingston RE. eds Current Protocols in Molecular Biology Media, PA: Wiley; 1987 p 2
    [Google Scholar]
  17. Ribeiro A, Akkermans AD, van Kammen A, Bisseling T, Pawlowski K. A nodule-specific gene encoding a subtilisin-like protease is expressed in early stages of actinorhizal nodule development. Plant Cell 1995; 7:785–794 [View Article]
    [Google Scholar]
  18. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol 1966; 16:313–340 [View Article]
    [Google Scholar]
  19. Nguyen TV, Wibberg D, Battenberg K, Blom J, Vanden Heuvel B et al. An assemblage of Frankia Cluster II strains from California contains the canonical nod genes and also the sulfotransferase gene nodH. BMC Genomics 2016; 17:796 [View Article]
    [Google Scholar]
  20. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 2015; 31:3210–3212 [View Article]
    [Google Scholar]
  21. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
    [Google Scholar]
  22. Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T et al. GenDB—an open source genome annotation system for prokaryote genomes. Nucleic Acids Res 2003; 31:2187–2195 [View Article]
    [Google Scholar]
  23. 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]
    [Google Scholar]
  24. 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]
    [Google Scholar]
  25. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:421 [View Article]
    [Google Scholar]
  26. 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]
  27. 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]
  28. Farris JS. Estimating phylogenetic trees from distance matrices. Am Nat 1972; 106:645–668 [View Article]
    [Google Scholar]
  29. 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]
  30. Meier-Kolthoff JP, Hahnke RL, Petersen J, Scheuner C, Michael V et al. Complete genome sequence of DSM 30083T, the type strain (U5/41T) of Escherichia coli, and a proposal for delineating subspecies in microbial taxonomy. Stand Genomic Sci 2014; 9:2 [View Article]
    [Google Scholar]
  31. 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]
  32. 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]
    [Google Scholar]
  33. Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, van Wezel GP et al. AntiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res 2021; 49:W29–W35 [View Article]
    [Google Scholar]
  34. Yoolong S, Kruasuwan W, Thanh Phạm HT, Jaemsaeng R, Jantasuriyarat C et al. Modulation of salt tolerance in Thai jasmine rice (Oryza sativa L. cv. KDML105) by Streptomyces venezuelae ATCC 10712 expressing ACC deaminase. Sci Rep 2019; 9:1275 [View Article]
    [Google Scholar]
  35. Chewning SS, Grant DL, O’Banion BS, Gates AD, Kennedz BJ et al. Root-associated Streptomyces isolates harbouring melC genes demonstrate enhanced plant colonisation. Phytobiomes J 2019; 3:165–176 [View Article]
    [Google Scholar]
  36. Alonso-Vega P, Normand P, Bacigalupe R, Pujic P, Lajus A et al. Genome sequence of Micromonospora lupini Lupac 08, isolated from root nodules of Lupinus angustifolius. J Bacteriol 2012; 194:4135 [View Article]
    [Google Scholar]
  37. Ghodhbane-Gtari F, Tisa LS, Katsy EI. Ecology and physiology of non-Frankia actinobacteria from actinorhizal plants. In Katsy EI. eds Plasticity in Plant-Growth-Promoting and Phytopathogenic Bacteria New York: Springer; 2014 pp 27–42 [View Article]
    [Google Scholar]
  38. Carro L, Pujic P, Trujillo ME, Normand P. Micromonospora is a normal occupant of actinorhizal nodules. J Biosci 2013; 38:685–693 [View Article]
    [Google Scholar]
  39. Trujillo ME, Kroppenstedt RM, Schumann P, Carro L, Martínez-Molina E. Micromonospora coriariae sp. nov., isolated from root nodules of Coriaria myrtifolia. Int J Syst Evol Microbiol 2006; 56:2381–2385 [View Article]
    [Google Scholar]
  40. Hirsch AM, Alvarado J, Bruce D, Chertkov O, De Hoff PL et al. Complete genome sequence of Micromonospora strain L5, a potential plant-growth-regulating actinomycete, originally isolated from Casuarina equisetifolia root nodules. Genome Announc 2013; 1:e00759-13 [View Article]
    [Google Scholar]
  41. Ghodhbane-Gtari F, Beauchemin N, Gueddou A, Hezbri K, Ktari A et al. Permanent draft genome sequence of Nocardia sp. BMG111209, an actinobacterium isolated from nodules of Casuarina glauca. Genome Announc 2016; 4:e00770-16 [View Article]
    [Google Scholar]
  42. Ghodhbane-Gtari F, Beauchemin N, Louati M, Nouioui I, Ktari A et al. Permanent improved high-quality draft genome sequence of Nocardia casuarinae strain BMG51109, an endophyte of actinorhizal root nodules of Casuarina glauca. Genome Announc 2016; 4:e00799-16 [View Article]
    [Google Scholar]
  43. Liu N, Wang H, Liu M, Gu Q, Zheng W et al. Streptomyces alni sp. nov., a daidzein-producing endophyte isolated from a root of Alnus nepalensis d. don. Int J Syst Evol Microbiol 2009; 59:254–258 [View Article]
    [Google Scholar]
  44. Vurukonda S, Giovanardi D, Stefani E. Plant growth promoting and biocontrol activity of Streptomyces spp. as endophytes. Int J Mol Sci 2018; 19:952 [View Article]
    [Google Scholar]
  45. Trujillo ME, Riesco R, Benito P, Carro L. Endophytic actinobacteria and the interaction of Micromonospora and nitrogen fixing plants. Front Microbiol 2015; 6:1341 [View Article]
    [Google Scholar]
  46. Lalonde M, Calvert HE. Production of Frankia hyphae and spores as an infective inoculant for Alnus species. In Gordon JC, Wheeler CT, Perry DA. eds Symbiotic Nitrogen Fixation in the Management of Temperate Forest Corvallis: Forest Research Laboratory Oregon State University; 1979 pp 95–110
    [Google Scholar]
  47. Hopwood DA. Genetic analysis and genome structure in Streptomyces coelicolor. Bacteriol Rev 1967; 31:373–403 [View Article] [PubMed]
    [Google Scholar]
  48. Benoist P, Müller A, Diem HG, Schwencke J. High-molecular-mass multicatalytic proteinase complexes produced by the nitrogen-fixing actinomycete Frankia strain BR. J Bacteriol 1992; 174:1495–1504 [View Article]
    [Google Scholar]
  49. 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]
  50. Nguyen TM, Kim J. Antifungal and antibacterial activities of Streptomyces polymachus sp. nov. isolated from soil. Int J Syst Evol Microbiol 2015; 65:2385–2390 [View Article]
    [Google Scholar]
  51. Isono K, Nagatsu J, Kawashima Y, Suzuki S. Studies on polyoxins, antifungal antibiotics. part I. isolation and characterization of polyoxins A and B. Agric Biol Chem 1965; 29:848–854 [View Article]
    [Google Scholar]
  52. Ohmori T, Okanishi M, Kawaguchi H. Glebomycin, a new member of the streptomycin class. III. taxonomic studies on strain no.12096, producer of glebomycin. J Antibiotics 1962; A15:21–27
    [Google Scholar]
  53. 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]
  54. 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]
    [Google Scholar]
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