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INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 72, Issue 11

Six novel species associated with the phyllosphere and roots of leguminous plants: sp. nov., sp. nov., sp. nov., sp. nov., sp. nov., and sp. nov. Open Access

Abstract

Six actinobacterial strains isolated from diverse legume tissues collected in various locations in Spain were characterized to determine their taxonomic status. Using 16S rRNA gene sequencing, the strains were primarily identified as members of the genus with more than 99 % similarity. Digital DNA–DNA hybridization values and average nucleotide identities between the six strains and the nearest type strains confirmed that each strain represented a novel species. Genome sequences were analysed to infer their metabolic profiles, their potential to produce secondary metabolites and plant growth promoting features. Chemotaxonomic and physiological studies were carried out to complete the phenotypic characterization and to distinguish the new species. The genomic and phenotypic characterization of the strains strongly support their classification as representatives of new species with the following names: sp. nov., sp. nov., sp. nov., sp. nov., sp. nov. and sp. nov., with the type strains MED01, LAH09, PSH25, NIE111, PSH03 and NIE79, respectively.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): endophytic , genome , legume , Micromonospora , PGPB and species
Funding
This study was supported by the:
  • Ministerio de Ciencia, Innovación y Universidades (Award PGC2018-096185-B-I00)
    • Principle Award Recipient: MarthaE. Trujillo
© 2022 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2022-11-17
2024-04-20
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References

  1. Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 2012; 488:91–95 [View Article] [PubMed]
     [Google Scholar]
  2. Bulgarelli D, Schlaeppi K, Spaepen S, Ver Loren van Themaat E, Schulze-Lefert P. Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 2013; 64:807–838 [View Article] [PubMed]
     [Google Scholar]
  3. Kent AD, Triplett EW. Microbial communities and their interactions in soil and rhizosphere ecosystems. Annu Rev Microbiol 2002; 56:211–236 [View Article] [PubMed]
     [Google Scholar]
  4. Orozco-Mosqueda MDC, Rocha-Granados MDC, Glick BR, Santoyo G. Microbiome engineering to improve biocontrol and plant growth-promoting mechanisms. Microbiol Res 2018; 208:25–31 [View Article] [PubMed]
     [Google Scholar]
  5. Kandel S, Joubert P, Doty S. Bacterial endophyte colonization and distribution within Plants. Microorganisms 2017; 5:77 [View Article]
     [Google Scholar]
  6. de Oliveira Costa LE, de Queiroz MV, Borges AC, de Moraes CA, de Araújo EF. Isolation and characterization of endophytic bacteria isolated from the leaves of the common bean (Phaseolus vulgaris). Braz J Microbiol 2012; 43:1562–1575 [View Article]
     [Google Scholar]
  7. Haruna E, Zin NM, Kerfahi D, Adams JM. Extensive overlap of tropical rainforest bacterial endophytes between soil, plant parts, and plant species. Microb Ecol 2018; 75:88–103 [View Article]
     [Google Scholar]
  8. Carro L, Riesco R, Spröer C, Trujillo ME. Micromonospora ureilytica sp. nov., Micromonospora noduli sp. nov. and Micromonospora vinacea sp. nov., isolated from Pisum sativum nodules. Int J Syst Evol Microbiol 2016; 66:3509–3514 [View Article]
     [Google Scholar]
  9. Carro L, Riesco R, Spröer C, Trujillo ME. Micromonospora luteifusca sp. nov. isolated from cultivated Pisum sativum. Syst Appl Microbiol 2016; 39:237–242 [View Article] [PubMed]
     [Google Scholar]
  10. Carro L, Veyisoglu A, Riesco R, Spröer C, Klenk H-P et al. Micromonospora phytophila sp. nov. and Micromonospora luteiviridis sp. nov., isolated as natural inhabitants of plant nodules. Int J Syst Evol Microbiol 2018; 68:248–253 [View Article]
     [Google Scholar]
  11. Trujillo ME, Kroppenstedt RM, Fernández-Molinero C, Schumann P, Martínez-Molina E. Micromonospora lupini sp. nov. and Micromonospora saelicesensis sp. nov.,isolated from root nodules of Lupinus angustifolius. Int J Syst Evol Microbiol 2007; 57:2799–2804 [View Article]
     [Google Scholar]
  12. Riesco R, Carro L, Román-Ponce B, Prieto C, Blom J et al. Defining the species Micromonospora saelicesensis and Micromonospora noduli under the framework of genomics. Front Microbiol 2018; 9:1360 [View Article]
     [Google Scholar]
  13. Benito P, Alonso-Vega P, Aguado C, Luján R, Anzai Y et al. Monitoring the colonization and infection of legume nodules by Micromonospora in co-inoculation experiments with rhizobia. Sci Rep 2017; 7:1–12 [View Article] [PubMed]
     [Google Scholar]
  14. Benito P, Carro L, Bacigalupe R, Ortúzar M, Trujillo ME. From roots to leaves: the capacity of Micromonospora to colonize different legume tissues. Phytobiomes Journal 2022; 6:35–44 [View Article]
     [Google Scholar]
  15. Genilloud O et al. Micromonospora. In Trujillo ME, Dedysh S, DeVos P, Hedlund B, Kämpfer P et al. eds Bergey’s Manual of Systematics of Archaea and Bacteria New Jersey: John Wiley & Sons, Inc; pp 2015–2016 [View Article]
     [Google Scholar]
  16. 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]
     [Google Scholar]
  17. 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]
     [Google Scholar]
  18. Trujillo ME, Alonso-Vega P, Rodríguez R, Carro L, Cerda E et al. The genus Micromonospora is widespread in legume root nodules: the example of Lupinus angustifolius. ISME J 2010; 4:1265–1281 [View Article] [PubMed]
     [Google Scholar]
  19. Vincent JM. The cultivation, isolation and maintenance of rhizobia. In A Manual for the Practical Study of Root-Nodule Bacteria Oxford: Blackwell Scientific Publications; 1970 pp 1–13
     [Google Scholar]
  20. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Bacteriol 1966; 16:313–340 [View Article]
     [Google Scholar]
  21. Trujillo ME, Fernández-Molinero C, Velázquez E, Kroppenstedt RM, Schumann P et al. Micromonospora mirobrigensis sp. nov. Int J Syst Evol Microbiol 2005; 55:877–880 [View Article] [PubMed]
     [Google Scholar]
  22. Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. GenBank. Nucleic Acids Res 2016; 44:D67–72 [View Article]
     [Google Scholar]
  23. 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]
  24. 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]
  25. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article] [PubMed]
     [Google Scholar]
  26. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article]
     [Google Scholar]
  27. Riesco R, Ortúzar M, Fernández-Ábalos JM, Trujillo ME. Deciphering genomes: genetic signatures of plant-associated Micromonospora. Front Plant Sci 2022; 13:1–14 [View Article]
     [Google Scholar]
  28. Na S-I, Kim YO, Yoon S-H, Ha S-M, Baek I et al. UBCG: Up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 2018; 56:280–285 [View Article]
     [Google Scholar]
  29. Letunic I, Bork P. Interactive Tree of Life (IToL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article]
     [Google Scholar]
  30. 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]
     [Google Scholar]
  31. 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]
     [Google Scholar]
  32. 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]
     [Google Scholar]
  33. 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]
  34. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M, Access O. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article]
     [Google Scholar]
  35. Gu Z, Eils R, Schlesner M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 2016; 32:2847–2849 [View Article]
     [Google Scholar]
  36. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 2009; 106:19126–19131 [View Article] [PubMed]
     [Google Scholar]
  37. Meier-Kolthoff JP, Klenk H-P, Göker M. Taxonomic use of DNA G+C content and DNA-DNA hybridization in the genomic age. Int J Syst Evol Microbiol 2014; 64:352–356 [View Article] [PubMed]
     [Google Scholar]
  38. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S et al. RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 2015; 5:8365 [View Article]
     [Google Scholar]
  39. 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:D206–14 [View Article] [PubMed]
     [Google Scholar]
  40. Arkin AP, Cottingham RW, Henry CS, Harris NL, Stevens RL et al. KBase: the United States Department of Energy Systems biology knowledgebase. Nat Biotechnol 2018; 36:566–569 [View Article]
     [Google Scholar]
  41. 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]
  42. Trujillo ME, Bacigalupe R, Pujic P, Igarashi Y, Benito P et al. Genome features of the endophytic actinobacterium Micromonospora lupini strain Lupac 08: on the process of adaptation to an endophytic life style?. PLoS One 2014; 9:e108522 [View Article]
     [Google Scholar]
  43. Huang L, Zhang H, Wu P, Entwistle S, Li X et al. dbCAN-seq: a database of carbohydrate-active enzyme (CAZyme) sequence and annotation. Nucleic Acids Res 2018; 46:D516–D521 [View Article]
     [Google Scholar]
  44. R Core Team. R A language and environment for statistical computing. R foundation for statistical computing. Vienna, Austria: 2021 https://www.R-project.org
  45. Ortúzar M, Trujillo ME, Román-Ponce B, Carro L. Micromonospora metallophores: a plant growth promotion trait useful for bacterial-assisted phytoremediation?. Sci Total Environ 2020; 739:139850 [View Article]
     [Google Scholar]
  46. El-Tarabily KA, Ramadan GA, Elbadawi AA, Hassan AH, Tariq S et al. The marine endophytic polyamine-producing Streptomyces mutabilis UAE1 isolated from extreme niches in the Arabian Gulf promotes the performance of mangrove (Avicennia marina) seedlings under greenhouse conditions. Front Mar Sci 2021; 8:1–18 [View Article]
     [Google Scholar]
  47. Alcázar R, Fortes AM, Tiburcio AF. Editorial: Polyamines in plant biotechnology, food nutrition, and human health. Front Plant Sci 2020; 11:10–11 [View Article] [PubMed]
     [Google Scholar]
  48. Carro L, Nouioui I, Sangal V, Meier-Kolthoff JP, Trujillo ME et al. Genome-based classification of micromonosporae with a focus on their biotechnological and ecological potential. Sci Rep 2018; 8:525 [View Article]
     [Google Scholar]
  49. Conn VM, Walker AR, Franco CMM. Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana. Mol Plant Microbe Interact 2008; 21:208–218 [View Article] [PubMed]
     [Google Scholar]
  50. Jones KL. Fresh isolates of actinomycetes in which the presence of sporogenous aerial mycelia is a fluctuating characteristic. J Bacteriol 1949; 57:141–145 [View Article] [PubMed]
     [Google Scholar]
  51. 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]
     [Google Scholar]
  52. Román-Ponce B, Millán-Aguiñaga N, Guillen-Matus D, Chase AB, Ginigini JGM et al. Six novel species of the obligate marine Actinobacterium Salinispora, Salinispora cortesiana sp. nov., Salinispora fenicalii sp. nov., Salinispora goodfellowii sp. nov., Salinispora mooreana sp. nov., Salinispora oceanensis sp. nov. and Salinispora vitiensis sp. nov., and emended description of the genus Salinispora. Int J Syst Evol Microbiol 2020; 70:4668–4682 [View Article]
     [Google Scholar]
  53. Rowbotham TJ, Cross T. Ecology of Rhodococcus coprophilus and associated actinomycetes in fresh water and agricultural habitats. J Gen Microbiol 1977; 100:231–240 [View Article]
     [Google Scholar]
  54. Kanehisa M, Sato Y. KEGG Mapper for inferring cellular functions from protein sequences. Protein Sci 2020; 29:28–35 [View Article]
     [Google Scholar]
  55. Ferreira L, Sánchez-Juanes F, García-Fraile P, Rivas R, Mateos PF et al. MALDI-TOF mass spectrometry is a fast and reliable platform for identification and ecological studies of species from family Rhizobiaceae. PLoS One 2011; 6:e20223 [View Article]
     [Google Scholar]
  56. Minnikin DE, Alshamaony L, Goodfellow M. Differentiation of Mycobacterium, Nocardia, and related taxa by thin-layer chromatographic analysis of whole-organism methanolysates. J Gen Microbiol 1975; 88:200–204 [View Article]
     [Google Scholar]
  57. 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]
  58. Sasser M. Technical Note 101: Identification of bacteria by gas chromatography of cellular fatty acids Newark, DE: Microbial ID, Inc; 1990
     [Google Scholar]
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Six novel Micromonospora species associated with the phyllosphere and roots of leguminous plants: Micromonospora alfalfae sp. nov., Micromonospora cabrerizensis sp. nov., Micromonospora foliorum sp. nov., Micromonospora hortensis sp. nov., Micromonospora salmantinae sp. nov., and Micromonospora trifolii sp. nov.
Int J Syst Evol Microbiol 72, 005680 (2022); https://doi.org/10.1099/ijsem.0.005680
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