1887

Abstract

Strain aSej3 was isolated from a root nodule of a plant growing in Bizerte, Tunisia. 16S rRNA gene analysis placed this strain within the genus . Multilocus sequence analysis (MLSA) including three housekeeping genes (, and ) grouped aSej3 together with CTAW71, CTAW11, RITF806, USDA 3051 and BTA-1. MLSA with five housekeeping genes (, , , and ) revealed that this strain shares less than 93.5 % nucleotide identity with other type strains. Genome sequencing and inspection revealed a genome size of 8.83 Mbp with a G+C content of 62.8 mol%. Genome-wide average nucleotide identity and digital DNA–DNA hybridization values were below 87.5 and 36.2 %, respectively, when compared to described species. Strain aSej3 nodulated plants under axenic conditions and its gene clustered within the genistearum symbiovar. Altogether, the phylogenetic data and the chemotaxonomic characteristics of this strain support that aSej3 represents a new species for which we propose the name sp. nov. with the type strain aSej3 (=DSM 108913=LMG 31020).

Funding
This study was supported by the:
  • Not Applicable , Bundesministerium für Bildung und Forschung , (Award 01DH16008)
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004445
2020-09-08
2020-09-28
Loading full text...

Full text loading...

References

  1. Lucas MM, Stoddard FL, Annicchiarico P, Frías J, Martínez-Villaluenga C et al. The future of lupin as a protein crop in Europe. Front Plant Sci 2015; 6:705 [CrossRef][PubMed]
    [Google Scholar]
  2. Materechera SA, Alston AM, Kirby JM, Dexter AR. Field evaluation of laboratory techniques for predicting the ability of roots to penetrate strong soil and of the influence of roots on water sorptivity. Plant Soil 1993; 149:149–158 [CrossRef]
    [Google Scholar]
  3. Rhodes P, Askin D, White J. The effect of grain legumes on soil fertility. Proc Agron Soc NZ 1982; 12:5–8
    [Google Scholar]
  4. Reeves TG, Ellington A, Brooke HD. Effects of lupin-wheat rotations on soil fertility, crop disease and crop yields. Aust J Exp Agric 1984; 24:595–600 [CrossRef]
    [Google Scholar]
  5. Bolland MDA, Brennan RF. Comparing the phosphorus requirements of wheat, lupin, and canola. Aust J Agric Res 2008; 59:983–998 [CrossRef]
    [Google Scholar]
  6. Rejili M, Msaddak A, Filali I, Benabderrahim MA, Mars M et al. New chromosomal lineages within Microvirga and Bradyrhizobium genera nodulate Lupinus angustifolius growing on different Tunisian soils. FEMS Microbiol Ecol 2019; 95: [CrossRef][PubMed]
    [Google Scholar]
  7. Msaddak A, Rejili M, Durán D, Rey L, Imperial J et al. Members of Microvirga and Bradyrhizobium genera are native endosymbiotic bacteria nodulating Lupinus luteus in Northern Tunisian soils. FEMS Microbiol Ecol 2017; 93: [CrossRef][PubMed]
    [Google Scholar]
  8. Msaddak A, Durán D, Rejili M, Mars M, Ruiz-Argüeso T et al. Diverse bacteria affiliated with the genera Microvirga, Phyllobacterium, and Bradyrhizobium nodulate Lupinus micranthus growing in soils of northern Tunisia. Appl Environ Microbiol 2017; 83: [CrossRef][PubMed]
    [Google Scholar]
  9. Msaddak A, Rejili M, Durán D, Rey L, Palacios JM et al. Definition of two new symbiovars, sv. lupini and sv. mediterranense, within the genera Bradyrhizobium and Phyllobacterium efficiently nodulating Lupinus micranthus in Tunisia. Syst Appl Microbiol 2018; 41:487–493 [CrossRef][PubMed]
    [Google Scholar]
  10. Jarabo-Lorenzo A, Pérez-Galdona R, Donate-Correa J, Rivas R, Velázquez E et al. Genetic diversity of bradyrhizobial populations from diverse geographic origins that nodulate Lupinus spp. and Ornithopus spp. Syst Appl Microbiol 2003; 26:611–623 [CrossRef][PubMed]
    [Google Scholar]
  11. Stepkowski T, Hughes CE, Law IJ, Markiewicz Łukasz, Gurda D et al. Diversification of lupine Bradyrhizobium strains: evidence from nodulation gene trees. Appl Environ Microbiol 2007; 73:3254–3264 [CrossRef][PubMed]
    [Google Scholar]
  12. Velázquez E, Valverde A, Rivas R, Gomis V, Peix A et al. Strains nodulating Lupinus albus on different continents belong to several new chromosomal and symbiotic lineages within Bradyrhizobium. Antonie van Leeuwenhoek 2010; 97:363–376 [CrossRef][PubMed]
    [Google Scholar]
  13. Bourebaba Y, Durán D, Boulila F, Ahnia H, Boulila A et al. Diversity of Bradyrhizobium strains nodulating Lupinus micranthus on both sides of the Western Mediterranean: Algeria and Spain. Syst Appl Microbiol 2016; 39:266–274 [CrossRef][PubMed]
    [Google Scholar]
  14. Mellal H, Yacine B, Boukaous L, Khouni S, Benguedouar A et al. Phylogenetic diversity of Bradyrhizobium strains isolated from root nodules of Lupinus angustifolius grown wild in the North East of Algeria. Syst Appl Microbiol 2019; 42:397–402 [CrossRef][PubMed]
    [Google Scholar]
  15. Durán D, Rey L, Sánchez-Cañizares C, Navarro A, Imperial J et al. Genetic diversity of indigenous rhizobial symbionts of the Lupinus mariae-josephae endemism from alkaline-limed soils within its area of distribution in Eastern Spain. Syst Appl Microbiol 2013; 36:128–136 [CrossRef][PubMed]
    [Google Scholar]
  16. Granada CE, Beneduzi A, Lisboa BB, Turchetto-Zolet AC, Vargas LK et al. Multilocus sequence analysis reveals taxonomic differences among Bradyrhizobium sp. symbionts of Lupinus albescens plants growing in arenized and non-arenized areas. Syst Appl Microbiol 2015; 38:323–329 [CrossRef][PubMed]
    [Google Scholar]
  17. Parte AC. LPSN - List of Prokaryotic names with Standing in Nomenclature (bacterio.net), 20 years on. Int J Syst Evol Microbiol 2018; 68:1825–1829 [CrossRef][PubMed]
    [Google Scholar]
  18. Jordan DC. Notes: transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. nov., a genus of slow-growing, root nodule bacteria from leguminous plants. Int J Syst Bacteriol 1982; 32:136–139 [CrossRef]
    [Google Scholar]
  19. Wolko B, Clemens J, Naganowska B, Nelson M, Yang H et al. Lupinus. Wild Crop Relatives: Genomic and Breeding Resources,Legume Crops and Forages Springer; 2011
    [Google Scholar]
  20. Vincent JM. The cultivation, isolation and maintenance of rhizobia; 1970
  21. Herrera-Cervera JA, Caballero-Mellado J, Laguerre G, Tichy H-V, Requena N et al. At least five rhizobial species nodulate Phaseolus vulgaris in a Spanish soil. FEMS Microbiol Ecol 1999; 30:87–97 [CrossRef]
    [Google Scholar]
  22. Salmi A, Boulila F, Bourebaba Y, Le Roux C, Belhadi D et al. Phylogenetic diversity of Bradyrhizobium strains nodulating Calicotome spinosa in the Northeast of Algeria. Syst Appl Microbiol 2018; 41:452–459 [CrossRef][PubMed]
    [Google Scholar]
  23. Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 2017
    [Google Scholar]
  24. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [CrossRef][PubMed]
    [Google Scholar]
  25. Menna P, Barcellos FG, Hungria M. Phylogeny and taxonomy of a diverse collection of Bradyrhizobium strains based on multilocus sequence analysis of the 16S rRNA gene, ITS region and glnII, recA, atpD and dnaK genes. Int J Syst Evol Microbiol 2009; 59:2934–2950 [CrossRef][PubMed]
    [Google Scholar]
  26. Urquiaga MCdeO, Klepa MS, Somasegaran P, Ribeiro RA, Delamuta JRM et al. Bradyrhizobium frederickii sp. nov., a nitrogen-fixing lineage isolated from nodules of the caesalpinioid species Chamaecrista fasciculata and characterized by tolerance to high temperature in vitro. Int J Syst Evol Microbiol 2019; 69:3863–3877 [CrossRef][PubMed]
    [Google Scholar]
  27. Durán D, Rey L, Mayo J, Zúñiga-Dávila D, Imperial J et al. Bradyrhizobium paxllaeri sp. nov. and Bradyrhizobium icense sp. nov., nitrogen-fixing rhizobial symbionts of lima bean (Phaseolus lunatus L.) in Peru. Int J Syst Evol Microbiol 2014; 64:2072–2078 [CrossRef][PubMed]
    [Google Scholar]
  28. Rivas R, Martens M, de Lajudie P, Willems A. Multilocus sequence analysis of the genus Bradyrhizobium. Syst Appl Microbiol 2009; 32:101–110 [CrossRef][PubMed]
    [Google Scholar]
  29. Sánchez-Cañizares C, Rey L, Durán D, Temprano F, Sánchez-Jiménez P et al. Endosymbiotic bacteria nodulating a new endemic lupine Lupinus mariae-josephi from alkaline soils in Eastern Spain represent a new lineage within the Bradyrhizobium genus. Syst Appl Microbiol 2011; 34:207–215 [CrossRef][PubMed]
    [Google Scholar]
  30. Turner SL, Young JP. The glutamine synthetases of rhizobia: phylogenetics and evolutionary implications. Mol Biol Evol 2000; 17:309–319 [CrossRef][PubMed]
    [Google Scholar]
  31. Stepkowski T, Czaplińska M, Miedzinska K, Moulin L. The variable part of the dnaK gene as an alternative marker for phylogenetic studies of rhizobia and related alpha Proteobacteria. Syst Appl Microbiol 2003; 26:483–494 [CrossRef][PubMed]
    [Google Scholar]
  32. William S, Feil H, C A. Bacterial genomic DNA isolation using CTAB. joint genome Institute. Walnut Creek, CA 2012
    [Google Scholar]
  33. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [CrossRef][PubMed]
    [Google Scholar]
  34. Haft DH, DiCuccio M, Badretdin A, Brover V, Chetvernin V et al. RefSeq: an update on prokaryotic genome annotation and curation. Nucleic Acids Res 2018; 46:D851–D860 [CrossRef][PubMed]
    [Google Scholar]
  35. Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci U S A 2005; 102:2567–2572 [CrossRef][PubMed]
    [Google Scholar]
  36. 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 [CrossRef][PubMed]
    [Google Scholar]
  37. 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 [CrossRef][PubMed]
    [Google Scholar]
  38. Rogel MA, Ormeño-Orrillo E, Martinez Romero E. Symbiovars in rhizobia reflect bacterial adaptation to legumes. Syst Appl Microbiol 2011; 34:96–104 [CrossRef][PubMed]
    [Google Scholar]
  39. Vinuesa P, León-Barrios M, Silva C, Willems A, Jarabo-Lorenzo A et al. Bradyrhizobium canariense sp. nov., an acid-tolerant endosymbiont that nodulates endemic genistoid legumes (Papilionoideae: Genisteae) from the Canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies alpha and Bradyrhizobium genospecies beta. Int J Syst Evol Microbiol 2005; 55:569–575 [CrossRef][PubMed]
    [Google Scholar]
  40. Guerrouj K, Ruíz-Díez B, Chahboune R, Ramírez-Bahena M-H, Abdelmoumen H et al. Definition of a novel symbiovar (sv. retamae) within Bradyrhizobium retamae sp. nov., nodulating Retama sphaerocarpa and Retama monosperma. Syst Appl Microbiol 2013; 36:218–223 [CrossRef][PubMed]
    [Google Scholar]
  41. Cobo-Díaz JF, Martínez-Hidalgo P, Fernández-González AJ, Martínez-Molina E, Toro N et al. The endemic Genista versicolor from Sierra Nevada National Park in Spain is nodulated by putative new Bradyrhizobium species and a novel symbiovar (sierranevadense). Syst Appl Microbiol 2014; 37:177–185 [CrossRef][PubMed]
    [Google Scholar]
  42. Bejarano A, Ramírez-Bahena M-H, Velázquez E, Peix A. Vigna unguiculata is nodulated in Spain by endosymbionts of Genisteae legumes and by a new symbiovar (vignae) of the genus Bradyrhizobium. Syst Appl Microbiol 2014; 37:533–540 [CrossRef][PubMed]
    [Google Scholar]
  43. Ramírez-Bahena MH, Flores-Félix JD, Chahboune R, Toro M, Velázquez E et al. Bradyrhizobium centrosemae (symbiovar centrosemae) sp. nov., Bradyrhizobium americanum (symbiovar phaseolarum) sp. nov. and a new symbiovar (tropici) of Bradyrhizobium viridifuturi establish symbiosis with Centrosema species native to America. Syst Appl Microbiol 2016; 39:378–383 [CrossRef][PubMed]
    [Google Scholar]
  44. Delamuta JRM, Menna P, Ribeiro RA, Hungria M. Phylogenies of symbiotic genes of Bradyrhizobium symbionts of legumes of economic and environmental importance in Brazil support the definition of the new symbiovars pachyrhizi and sojae. Syst Appl Microbiol 2017; 40:254–265 [CrossRef][PubMed]
    [Google Scholar]
  45. Bromfield ESP, Cloutier S, Tambong JT, Tran Thi TV. Soybeans inoculated with root zone soils of Canadian native legumes harbour diverse and novel Bradyrhizobium spp. that possess agricultural potential. Syst Appl Microbiol 2017; 40:440–447 [CrossRef][PubMed]
    [Google Scholar]
  46. Sarita S, Sharma PK, Priefer UB, Prell J. Direct amplification of rhizobial nodC sequences from soil total DNA and comparison to nodC diversity of root nodule isolates. FEMS Microbiol Ecol 2005; 54:1–11 [CrossRef][PubMed]
    [Google Scholar]
  47. Kabdullayeva T, Crosbie DB, Marín M. Mesorhizobium norvegicum sp. nov., a rhizobium isolated from a Lotus corniculatus root nodule in Norway. Int J Syst Evol Microbiol 2020; 70:388–396 [CrossRef][PubMed]
    [Google Scholar]
  48. Miller LT. Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids. J Clin Microbiol 1982; 16:584–586 [CrossRef][PubMed]
    [Google Scholar]
  49. Kuykendall LD, Roy MA, Neill JJ, Devine TE. Fatty acids, antibiotic resistance, and Deoxyribonucleic acid homology groups of Bradyrhizobium japonicum. Int J Syst Bacteriol 1988; 38:358–361 [CrossRef]
    [Google Scholar]
  50. Kämpfer P, Kroppenstedt RM. Numerical analysis of fatty acid patterns of coryneform bacteria and related taxa. Can J Microbiol 1996; 42:989–1005 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004445
Loading
/content/journal/ijsem/10.1099/ijsem.0.004445
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error