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Abstract

Strain KLBMP 9567, an isolate from weathered soil, was identified as a new actinobacterial species through a comprehensive polyphasic approach. Phylogenetic evaluations relying on 16S rRNA gene sequence placed KLBMP 9567 within the genus , alongside its close relatives NEAU-FHS4 and NEAU-QY2, both sharing 98.6% sequence similarity. However, KLBMP 9567 demonstrated low digital DNA–DNA hybridization values with NEAU-FHS4 and NEAU-QY2, recorded at 48.5 and 29.1%, respectively. Meanwhile, the average nucleotide identity values were correspondingly recorded at 91.1 and 83.1%. The cell wall of KLBMP 9567 contained -diaminopimelic acid, with xylose, mannose, glucose and galactose as diagnostic sugars. The diagnostic dominant phospholipids included diphosphatidylglycerol, phosphatidylethanolamine and phosphatidylinositol. Given phenotypic and genotypic data, KLBMP 9567 is recognized as a new species within the genus, named sp. nov., with the type strain KLBMP 9567 (= CGMCC 4.7773 = NBRC 115787). Genome mining revealed genes associated with plant growth promotion, specifically those encoding enzymes for synthesizing plant hormones like indole acetic acid and gibberellic acid. Experimental validation demonstrated that KLBMP 9567 can produce significant quantities of indole acetic acid (20.6 mg l) and gibberellic acid (42.6 mg l). Moreover, co-culture with showed marked growth enhancements: a 56.3% increase in lateral root proliferation, a 16.7% elongation in primary root length and a 44.8% boost in biomass accumulation. These findings underscore the strain’s potent plant growth-promoting attributes, providing profound insights into the mechanisms by which KLBMP 9567 enhances plant growth.

Funding
This study was supported by the:
  • Postgraduate Research & Practice Innovation Program of Jiangsu Province (Award KYCX24_3023)
    • Principle Award Recipient: LiliWang
  • National College Students Innovation and Entrepreneurship Training Program (Award 202310320003Z)
    • Principle Award Recipient: ZhouaiMa
  • National Natural Science Foundation of China (Award 32030072)
    • Principle Award Recipient: JihongJiang
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2024-11-26
2024-12-08
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References

  1. Qin S, Li J, Zhang Y-Q, Zhu W-Y, Zhao G-Z et al. Plantactinospora mayteni gen. nov., sp. nov., a member of the family Micromonosporaceae. Int J Syst Evol Microbiol 2009; 59:2527–2533 [View Article] [PubMed]
    [Google Scholar]
  2. Zhu W-Y, Zhao L-X, Zhao G-Z, Duan X-W, Qin S et al. Plantactinospora endophytica sp. nov., an actinomycete isolated from Camptotheca acuminata Decne., reclassification of Actinaurispora siamensis as Plantactinospora siamensis comb. nov. and emended descriptions of the genus Plantactinospora and Plantactinospora mayteni. Int J Syst Evol Microbiol 2012; 62:2435–2442 [View Article] [PubMed]
    [Google Scholar]
  3. Carro L, Veyisoglu A, Guven K, Schumann P, Klenk H-P et al. Genomic analysis of a novel heavy metal resistant isolate from a Black Sea contaminated sediment with the potential to degrade alkanes: Plantactinospora alkalitolerans sp. nov. Diversity 2022; 14:947 [View Article]
    [Google Scholar]
  4. Li W, Guo X, Shi L, Zhao J, Yan L et al. Plantactinospora solaniradicis sp. nov., a novel actinomycete isolated from the root of a tomato plant (Solanum lycopersicum L.). Antonie van Leeuwenhoek 2018; 111:227–235 [View Article]
    [Google Scholar]
  5. Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M. List of Prokaryotic names with Standing in Nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 2020; 70:5607–5612 [View Article] [PubMed]
    [Google Scholar]
  6. Li W, Salam N. Plantactinospora. In Whitman WB, Rainey F, Kämpfer P, Trujillo M, Chun J. eds Bergey’s Manual of Systematics of Archaea and Bacteria New York: John Wiley & Sons Inc; 2015 pp 1–7 [View Article]
    [Google Scholar]
  7. Etesami H, Glick BR. Bacterial indole-3-acetic acid: a key regulator for plant growth, plant-microbe interactions, and agricultural adaptive resilience. Microbiol Res 2024; 281:127602 [View Article] [PubMed]
    [Google Scholar]
  8. Tanimoto E. Regulation of root growth by plant hormones—roles for auxin and gibberellin. Crit Rev Plant Sci 2005; 24:249–265 [View Article]
    [Google Scholar]
  9. Khan AL, Waqas M, Kang S-M, Al-Harrasi A, Hussain J et al. Bacterial endophyte Sphingomonas sp. LK11 produces gibberellins and IAA and promotes tomato plant growth. J Microbiol 2014; 52:689–695 [View Article] [PubMed]
    [Google Scholar]
  10. Meenakshi S, Hiremath J, Meenakshi MH, Shivaveerakumar S. Actinomycetes: isolation, cultivation and its active biomolecules. J Pure Appl Microbiol 2024; 18:118–143 [View Article]
    [Google Scholar]
  11. Zhang Y, Gao Y, Yao J, Liu L, Ma Z et al. Antribacter soli sp. nov., a novel actinobacterium isolated from soils of weathering dolomite. Int J Syst Evol Microbiol 2023; 73:005771 [View Article] [PubMed]
    [Google Scholar]
  12. Qiu D, Ruan J, Huang Y. Selective isolation and rapid identification of members of the genus Micromonospora. Appl Environ Microbiol 2008; 74:5593–5597 [View Article] [PubMed]
    [Google Scholar]
  13. Lin Y, Chu X, Xie Y, Xie X, Huang X et al. Streptomyces chengmaiensis sp. nov., isolated from the stem of a mangrove plant in Hainan. Int J Syst Evol Microbiol 2023; 73: [View Article] [PubMed]
    [Google Scholar]
  14. Li W-J, Xu P, Schumann P, Zhang Y-Q, Pukall R et al. Georgenia ruanii sp. nov., a novel actinobacterium isolated from forest soil in Yunnan (China), and emended description of the genus Georgenia. Int J Syst Evol Microbiol 2007; 57:1424–1428 [View Article]
    [Google Scholar]
  15. 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]
  16. Choi I, Srinivasan S, Kim MK. Sphingomonas immobilis sp. nov., and Sphingomonas natans sp. nov bacteria isolated from soil. Arch Microbiol 2024; 206:1–10 [View Article]
    [Google Scholar]
  17. 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]
  18. Lee HJ, Whang KS. Falsiroseomonas oryziterrae sp. nov., and Falsiroseomonas oryzae sp. nov., isolated from rice paddy soil. Int J Syst Evol Microbiol 2024; 74:006349 [View Article]
    [Google Scholar]
  19. 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]
  20. Guo X, Guan X, Liu C, Jia F, Li jiansong et al. Plantactinospora soyae sp. nov., an endophytic actinomycete isolated from soybean root [Glycine max (L.) Merr]. Int J Syst Evol Microbiol 2016; 66:2578–2584 [View Article]
    [Google Scholar]
  21. Ma Z, Liu C, Fan J, He H, Li C et al. Plantactinospora sonchi sp. nov., an actinobacterium isolated from the leaves of common sowthistle (Sonchus oleraceus L.). Int J Syst Evol Microbiol 2015; 65:4895–4901 [View Article] [PubMed]
    [Google Scholar]
  22. Xing H, Liu C, Zhang Y, Zhao J, Li C et al. Plantactinospora veratri sp. nov., an actinomycete isolated from black false hellebore root (Veratrum nigrum L.). Int J Syst Evol Microbiol 2015; 65:1799–1804 [View Article] [PubMed]
    [Google Scholar]
  23. Jiang H, Han L, Li J, Yu M, Zhao J et al. Streptomyces montanus sp. nov., a novel actinomycete isolated from soil. Int J Syst Evol Microbiol 2020; 70:3226–3233 [View Article]
    [Google Scholar]
  24. Luo R, Liu B, Xie Y, Li Z, Huang W et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 2012; 1:18 [View Article] [PubMed]
    [Google Scholar]
  25. 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]
  26. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJM et al. ABySS: a parallel assembler for short read sequence data. Genome Res 2009; 19:1117–1123
    [Google Scholar]
  27. Lin S-H, Liao Y-C. CISA: contig integrator for sequence assembly of bacterial genomes. PLoS One 2013; 8:e60843 [View Article]
    [Google Scholar]
  28. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods 2015; 12:59–60 [View Article] [PubMed]
    [Google Scholar]
  29. 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 Suppl 2023; 51:W46–W50 [View Article]
    [Google Scholar]
  30. Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M. TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res 2022; 50:D801–D807 [View Article]
    [Google Scholar]
  31. Yoon S-H, Ha S-M, Lim J, Kwon S, 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]
  32. Knight CA, Molinari NA, Petrov DA. The large genome constraint hypothesis: evolution, ecology and phenotype. Ann Bot 2005; 95:177–190 [View Article] [PubMed]
    [Google Scholar]
  33. 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]
  34. 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]
  35. Cheng L, Mu H, Zhang X, Jiang P, Liu L et al. Deinococcus arenicola sp. nov., a novel radiation-resistant bacterium isolated from sandy soil in Antarctica. Int J Syst Evol Microbiol 2024; 74:006397 [View Article]
    [Google Scholar]
  36. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H et al. Gene ontology: tool for the unification of biology. Nat Genet 2000; 25:25–29 [View Article]
    [Google Scholar]
  37. Jin T, Ren J, Li Y, Bai B, Liu R et al. Plant growth-promoting effect and genomic analysis of the P. putida LWPZF isolated from C. japonicum rhizosphere. AMB Express 2022; 12:101 [View Article] [PubMed]
    [Google Scholar]
  38. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M. The KEGG resource for deciphering the genome. Nucleic Acids Res 2004; 32:D277–D280 [View Article] [PubMed]
    [Google Scholar]
  39. Galperin MY, Makarova KS, Wolf YI, Koonin EV. Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic Acids Res 2015; 43:D261–9 [View Article] [PubMed]
    [Google Scholar]
  40. Nouioui I, Ha SM, Baek I, Chun J, Goodfellow M. Genome insights into the pharmaceutical and plant growth promoting features of the novel species Nocardia alni sp. nov. BMC Genom 2022; 23:70 [View Article] [PubMed]
    [Google Scholar]
  41. Xu J, Shen S, Hu Z, Xu G, Li H et al. n.d. Enhanced production of sisomicin in Micromonospora inyoensis by protoplast mutagenesis and fermentation optimization. Appl Biochem Biotechnol 2024:1–14 [View Article]
    [Google Scholar]
  42. Banfalvi G. Antifungal activity of gentamicin B1 against systemic plant mycoses. Molecules 2020; 25:2401 [View Article] [PubMed]
    [Google Scholar]
  43. Peng F, Zhang M-Y, Hou S-Y, Chen J, Wu Y-Y et al. Insights into Streptomyces spp. isolated from the rhizospheric soil of Panax notoginseng: isolation, antimicrobial activity and biosynthetic potential for polyketides and non-ribosomal peptides. BMC Microbiol 2020; 20:143 [View Article] [PubMed]
    [Google Scholar]
  44. Kodani S, Komaki H, Suzuki M, Kobayakawa F, Hemmi H. Structure determination of a siderophore peucechelin from Streptomyces peucetius. Biometals 2015; 28:791–801 [View Article] [PubMed]
    [Google Scholar]
  45. Sun Y, Wu J, Shang X, Xue L, Ji G et al. Screening of siderophore-producing bacteria and their effects on promoting the growth of plants. Curr Microbiol 2022; 79:150 [View Article] [PubMed]
    [Google Scholar]
  46. Murata K, Esaki M, Ogura T, Arai S, Yamamoto Y et al. Whole-cell imaging of the budding yeast Saccharomyces cerevisiae by high-voltage scanning transmission electron tomography. Ultramicroscopy 2014; 146:39–45 [View Article] [PubMed]
    [Google Scholar]
  47. Claus D. A standardized Gram staining procedure. World J Microbiol Biotechnol 1992; 8:451–452 [View Article] [PubMed]
    [Google Scholar]
  48. Saygin H, Guven K, Cetin D, Sahin N. Polyphasic characterization and genomic insights into Nocardioides turkmenicus sp. nov. isolated from a desert soil. Antonie van Leeuwenhoek 2024; 117:25 [View Article] [PubMed]
    [Google Scholar]
  49. Liu L, Zhang Y, Chen Q, Shen Q, Li L et al. Nocardioides potassii sp. nov., isolated from weathered potash tailings soil. Int J Syst Evol Microbiol 2023; 73:005967 [View Article]
    [Google Scholar]
  50. Xu P, Li W-J, Tang S-K, Zhang Y-Q, Chen G-Z et al. Naxibacter alkalitolerans gen. nov., sp. nov., a novel member of the family “Oxalobacteraceae” isolated from China. Int J Syst Evol Microbiol 2005; 55:1149–1153 [View Article] [PubMed]
    [Google Scholar]
  51. Srinivasan S, Austin MN, Fiedler TL, Strenk SM, Agnew KJ et al. Amygdalobacter indicium gen. nov., sp. nov., and Amygdalobacter nucleatus sp. nov., gen. nov.: novel bacteria from the family Oscillospiraceae isolated from the female genital tract. Int J Syst Evol Microbiol 2023; 73:006017 [View Article] [PubMed]
    [Google Scholar]
  52. Menon RR, Kumari S, Viver T, Rameshkumar N. Flavobacterium pokkalii sp. nov., a novel plant growth promoting native rhizobacteria isolated from pokkali rice grown in coastal saline affected agricultural regions of southern India, Kerala. Microbiol Res 2020; 240:126533 [View Article] [PubMed]
    [Google Scholar]
  53. Lechevalier MP, Lechevalier H. Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J Syst Evol Microbiol 1970; 20:435–443 [View Article]
    [Google Scholar]
  54. Kuncharoen N, Yuki M, Kudo T, Okuma M, Booncharoen A et al. Comparative genomics and proposal of Streptomyces radicis sp. nov., an endophytic actinomycete from roots of plants in Thailand. Microbiol Res 2022; 254:126889 [View Article] [PubMed]
    [Google Scholar]
  55. Somphong A, Weeraphan T, Poengsungnoen V, Suriyachadkun C, Sripreechasak P et al. Actinoplanes pyxinae sp. nov., a new lichen-derived rare actinobacterium exhibiting antimicrobial and anticancer activity. Int J Syst Evol Microbiol 2024; 74:006215 [View Article] [PubMed]
    [Google Scholar]
  56. 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]
  57. 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]
  58. Glickmann E, Dessaux Y. A critical examination of the specificity of the salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 1995; 61:793–796 [View Article] [PubMed]
    [Google Scholar]
  59. Paiter A, Freitas G, Pinto L, Hass L, Barreiros M et al. IAA production and phosphate solubilization performed by native rhizobacteria in western Paraná. ASB J 2019; 5:70 [View Article]
    [Google Scholar]
  60. Liu Z, Zhang X, Li L, Xu N, Hu Y et al. Isolation and characterization of three plant growth-promoting rhizobacteria for growth enhancement of rice seedling. J Plant Growth Regul 2022; 41:1382–1393 [View Article]
    [Google Scholar]
  61. Ei SL, Myint M, Oo ZK, Lwin KM, Mya KM et al. Study on gibberellin and gibberellin-like substances from endophytes and their effect on maize plants. Biocatalysis and Agricultural Biotechnology 2024; 55:102979 [View Article]
    [Google Scholar]
  62. Mussa A, Million T, Assefa F. Rhizospheric bacterial isolates of grass pea (Lathyrus sativus L.) endowed with multiple plant growth promoting traits. J Appl Microbiol 2018; 125:1786–1801 [View Article]
    [Google Scholar]
  63. Asari S, Tarkowská D, Rolčík J, Novák O, Palmero DV et al. Analysis of plant growth-promoting properties of Bacillus amyloliquefaciens UCMB5113 using Arabidopsis thaliana as host plant. Planta 2017; 245:15–30 [View Article] [PubMed]
    [Google Scholar]
  64. Hussain HI, Kasinadhuni N, Arioli T. The effect of seaweed extract on tomato plant growth, productivity and soil. J Appl Phycol 2021; 33:1305–1314 [View Article]
    [Google Scholar]
  65. Zhang P, Jin T, Kumar Sahu S, Xu J, Shi Q et al. The distribution of tryptophan-dependent indole-3-acetic acid synthesis pathways in bacteria unraveled by large-scale genomic analysis. Molecules 2019; 24:1411 [View Article] [PubMed]
    [Google Scholar]
  66. Ouyang J, Shao X, Li J. Indole-3-glycerol phosphate, a branchpoint of indole-3-acetic acid biosynthesis from the tryptophan biosynthetic pathway in Arabidopsis thaliana. Plant J 2000; 24:327–333 [View Article] [PubMed]
    [Google Scholar]
  67. Huang YP, Chen IH, Kao YS, Hsu YH, Tsai CH. The gibberellic acid derived from the plastidial MEP pathway is involved in the accumulation of Bamboo mosaic virus. New Phytol 2022; 235:1543–1557 [View Article] [PubMed]
    [Google Scholar]
  68. Ghavami M, Merino EF, Yao Z-K, Elahi R, Simpson ME et al. Biological studies and target engagement of the 2- C-methyl-d-erythritol 4-phosphate cytidylyltransferase (IspD)-targeting antimalarial agent (1 R,3 S)-MMV008138 and analogs. ACS Infect Dis 2018; 4:549–559 [View Article] [PubMed]
    [Google Scholar]
  69. Kumar H, Singh K, Kumar S. 2C-methyl- D- erythritol 2,4-cyclodiphosphate synthase from Stevia rebaudiana Bertoni is a functional gene. Mol Biol Rep 2012; 39:10971–10978 [View Article]
    [Google Scholar]
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