1887

Abstract

For many smallholder farmers of Sub-Saharan Africa, pigeonpea () is an important crop to make ends meet. To ascertain the taxonomic status of pigeonpea isolates of Côte d’Ivoire previously identified as bradyrhizobia, a polyphasic approach was applied to strains CI-1B, CI-14A, CI-19D and CI-41S. Phylogeny of 16S ribosomal RNA (rRNA) genes placed these nodule isolates in a separate lineage from current species of the super clade. In phylogenetic analyses of single and concatenated partial , , , and sequences, the isolates again formed a separate lineage, with strain CI-1B sharing the highest sequence similarity (95.2 %) with SEMIA 6148. Comparative genomic analyses corroborated the novel species status, with 86 % ANIb and 89 % ANIm as the highest average nucleotide identity (ANI) values with USDA 76. Although CI-1B, CI-14A, CI-19D and CI-41S shared similar phenotypic and metabolic properties, growth of CI-41S was slower in/on various media. Symbiotic efficacy varied significantly between isolates, with CI-1B and CI-41S scoring on the ‘Light-Brown’ landrace as the most and least proficient bacteria, respectively. Also proficient on (mung bean), (cowpea, niébé) and additional cultivars, CI-1B represents a potential bioinoculant adapted to local soil conditions and capable of fostering the growth of diverse legume crops in Côte d'Ivoire. Given the data presented here, we propose the 19 . isolates to belong to a novel species called sp. nov., with CI-1B (=CCOS 1862=CCMM B1296) as a type strain.

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2020-01-02
2020-01-27
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References

  1. Varshney RK, Penmetsa RV, Dutta S, Kulwal PL, Saxena RK et al. Pigeonpea genomics initiative (PGI): an international effort to improve crop productivity of pigeonpea (Cajanus cajan L.). Mol Breed 2010;26: 393– 408 [CrossRef]
    [Google Scholar]
  2. Fossou RK, Kouassi NKI, kouadjo GCZ, Zako S, Zézé A. Diversité de rhizobia dans un Champ cultivé de pois d'Angole (Cajanus cajan L.) Yamoussoukro (centre de la Côte d'Ivoire). Agronomie Africaine 2012;24: 29– 38
    [Google Scholar]
  3. Koné AW, Edoukou EF, Tondoh JE, Gonnety JT, Angui PKT et al. Comparative study of earthworm communities, microbial biomass, and plant nutrient availability under 1-year Cajanus cajan (L.) Millsp and Lablab purpureus (L.) Sweet cultivations versus natural regrowths in a guinea savanna zone. Biol Fertil Soils 2012;48: 337– 347 [CrossRef]
    [Google Scholar]
  4. Charpentier H, Doumbia S, Coulibaly Z, Zana O. Fixation de l'agriculture au Nord et au centre de la Côte d'Ivoire: quels nouveaux systèmes de culture?. Agri Dév 1999;21: 41– 70
    [Google Scholar]
  5. Akanvou R, Kropff MJ, Bastiaans L, Becker M. Evaluating the use of two contrasting legume species as relay intercrop in upland rice cropping systems. Field Crops Res 2002;74: 23– 36 [CrossRef]
    [Google Scholar]
  6. Degefu T, Wolde-meskel E, Frostegård Åsa. Phylogenetic diversity of Rhizobium strains nodulating diverse legume species growing in Ethiopia. Syst Appl Microbiol 2013;36: 272– 280 [CrossRef]
    [Google Scholar]
  7. Wolde-Meskel E, Terefework Z, Frostegård A, Lindström K. Genetic diversity and phylogeny of rhizobia isolated from agroforestry legume species in southern Ethiopia. Int J Syst Evol Microbiol 2005;55: 1439– 1452 [CrossRef]
    [Google Scholar]
  8. Stępkowski 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]
    [Google Scholar]
  9. Araújo J, Díaz-Alcántara C-A, Velázquez E, Urbano B, González-Andrés F. Bradyrhizobium yuanmingense related strains form nitrogen-fixing symbiosis with Cajanus cajan L. in Dominican Republic and are efficient biofertilizers to replace N fertilization. Sci Hortic 2015;192: 421– 428 [CrossRef]
    [Google Scholar]
  10. Ramsubhag A, Umaharan P, Donawa A. Partial 16S rRNA gene sequence diversity and numerical taxonomy of slow growing pigeonpea (Cajanus cajan L. Millsp) nodulating rhizobia. FEMS Microbiol Lett 2002;216: 139– 144 [CrossRef]
    [Google Scholar]
  11. Araújo J, Flores-Félix JD, Igual JM, Peix A, González-Andrés F et al. Bradyrhizobium cajani sp. nov. isolated from nodules of Cajanus cajan. Int J Syst Evol Microbiol 2017;67: 2236– 2241 [CrossRef]
    [Google Scholar]
  12. 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]
  13. Stępkowski T, Banasiewicz J, Granada C, Andrews M, Passaglia L. Phylogeny and phylogeography of rhizobial symbionts nodulating legumes of the tribe Genisteae. Genes 2018;9: 163 [CrossRef]
    [Google Scholar]
  14. Aserse AA, Räsänen LA, Aseffa F, Hailemariam A, Lindström K. Phylogenetically diverse groups of Bradyrhizobium isolated from nodules of Crotalaria spp., Indigofera spp., Erythrina brucei and Glycine max growing in Ethiopia. Mol Phylogenet Evol 2012;65: 595– 609 [CrossRef]
    [Google Scholar]
  15. Avontuur JR, Palmer M, Beukes CW, Chan WY, Coetzee MPA et al. Genome-informed Bradyrhizobium taxonomy: where to from here?. Syst Appl Microbiol 2019
    [Google Scholar]
  16. Wang R, Chang YL, Zheng WT, Zhang D, Zhang XX et al. Bradyrhizobium arachidis sp. nov., isolated from effective nodules Arachis hypogaea grown in China. Syst Appl Microbiol 2013;36: 101– 105 [CrossRef]
    [Google Scholar]
  17. Rivas R, Willems A, Palomo JL, Garciá-Benavides P, Mateos PF et al. Bradyrhizobium betae sp. nov., isolated from roots of Beta vulgaris affected by tumour-like deformations. Int J Syst Evol Microbiol 2004;54: 1271– 1275 [CrossRef]
    [Google Scholar]
  18. 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]
    [Google Scholar]
  19. Islam MS, Kawasaki H, Muramatsu Y, Nakagawa Y, Seki T. Bradyrhizobium iriomotense sp. nov., isolated from a tumor-like root of the legume Entada koshunensis from Iriomote Island in Japan. Biosci Biotech Biochem 2008;72(6: 1416– 1429
    [Google Scholar]
  20. Kaneko T, Maita H, Hirakawa H, Uchiike N, Minamisawa K et al. Complete genome sequence of the soybean symbiont Bradyrhizobium japonicum strain USDA6T. Genes 2011;2: 763– 787 [CrossRef]
    [Google Scholar]
  21. LM X, Ge C, Cui Z, Li J, Fan H. Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. Int J Syst Bacteriol 1995;45: 706– 711
    [Google Scholar]
  22. XM Y, Cloutier S, Tambong JT, Bromfield ESP. Bradyrhizobium ottawaense sp. nov., a symbiotic nitrogen fixing bacterium from root nodules of soybeans in Canada. Int J Syst Evol Microbiol 2014;64: 3202– 3207
    [Google Scholar]
  23. Grönemeyer JL, Reinhold-Hurek B. Diversity of bradyrhizobia in subsahara Africa: a rich resource. Front Microbiol 2018;9: [CrossRef]
    [Google Scholar]
  24. 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]
    [Google Scholar]
  25. Michel DC, Passos SR, Simões-Araujo JL, Baraúna AC, da Silva K et al. Bradyrhizobium centrolobii and Bradyrhizobium macuxiense sp. nov. isolated from Centrolobium paraense grown in soil of Amazonia, Brazil. Arch Microbiol 2017;199: 657– 664 [CrossRef]
    [Google Scholar]
  26. 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]
    [Google Scholar]
  27. Grönemeyer JL, Kulkarni A, Berkelmann D, Hurek T, Reinhold-Hurek B. Rhizobia Indigenous to the Okavango region in sub-Saharan Africa: diversity, adaptations, and host specificity. Appl Environ Microbiol 2014;80: 7244– 7257 [CrossRef]
    [Google Scholar]
  28. Ndungu SM, Messmer MM, Ziegler D, Gamper HA, Mészáros Éva et al. Cowpea (Vigna unguiculata L. Walp) hosts several widespread bradyrhizobial root nodule symbionts across contrasting agro-ecological production areas in Kenya. Agric Ecosyst Environ 2018;261: 161– 171 [CrossRef]
    [Google Scholar]
  29. Wade TK, Le Quéré A, Laguerre G, N’Zoué A, Ndione JA et al. Eco-geographical diversity of cowpea bradyrhizobia in Senegal is marked by dominance of two genetic types. Syst Appl Microbiol 2014;37: 129– 139 [CrossRef]
    [Google Scholar]
  30. Fossou RK, Ziegler D, Zézé A, Barja F, Perret X. Two major clades of bradyrhizobia dominate symbiotic interactions with pigeonpea in fields of Côte d'Ivoire. Front Microbiol 1793;2016: 7
    [Google Scholar]
  31. Willems A, Coopman R, Gillis M. Phylogenetic and DNA-DNA hybridization analyses of Bradyrhizobium species. Int J Syst Evol Microbiol 2001;51: 111– 117 [CrossRef]
    [Google Scholar]
  32. Rivas R, Martens M, de Lajudie P, Willems A. Multilocus sequence analysis of the genus Bradyrhizobium. Syst Appl Microbiol 2009;32: 101– 110 [CrossRef]
    [Google Scholar]
  33. Grönemeyer JL, Bünger W, Reinhold-Hurek B. Bradyrhizobium namibiense sp. nov., a symbiotic nitrogen-fixing bacterium from root nodules of Lablab purpureus, hyacinth bean, in Namibia. Int J Syst Evol Microbiol 2017;67: 4884– 4891 [CrossRef]
    [Google Scholar]
  34. Helene LCF, Delamuta JRM, Ribeiro RA, Ormeño-Orrillo E, Rogel MA et al. Bradyrhizobium viridifuturi sp. nov., encompassing nitrogen-fixing symbionts of legumes used for green manure and environmental services. Int J Syst Evol Microbiol 2015;65: 4441– 4448 [CrossRef]
    [Google Scholar]
  35. Auch AF, von Jan M, Klenk HP, Göker M. Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2010;2: 117– 134 [CrossRef]
    [Google Scholar]
  36. 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 [CrossRef]
    [Google Scholar]
  37. Broughton WJ, Wong C-H, Lewin A, Samrey U, Myint H. Identification of Rhizobium plasmid sequences involved in recognition of Psophocarpus, Vigna, and other legumes. J Cell Biol 1986;102: 1173– 1182 [CrossRef]
    [Google Scholar]
  38. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016;33: 1870– 1874 [CrossRef]
    [Google Scholar]
  39. Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010;27: 221– 224 [CrossRef]
    [Google Scholar]
  40. Rogers JS, Swofford DL. A fast method for approximating maximum likelihoods of phylogenetic trees from nucleotide sequences. Syst Biol 1998;47: 77– 89 [CrossRef]
    [Google Scholar]
  41. Jourand P, Giraud E, Bena G, Sy A, Willems A et al. Methylobacterium nodulans sp. nov., for a group of aerobic, facultatively methylotrophic, legume root-nodule-forming and nitrogen-fixing bacteria. Int J Syst Evol Microbiol 2004;54: 2269– 2273 [CrossRef]
    [Google Scholar]
  42. Schwarz G. Estimating the dimension of a model. Ann Statist. 1978;6: 461– 464 [CrossRef]
    [Google Scholar]
  43. Rashid MH-or, Clercx P, Everall I, Wink M, Willems A et al. Average nucleotide identity of genome sequences supports the description of Rhizobium lentis sp. nov., Rhizobium bangladeshense sp. nov. and Rhizobium binae sp. nov. from lentil (Lens culinaris) nodules. Int J Syst Evol Microbiol 2015;65: 3037– 3045 [CrossRef]
    [Google Scholar]
  44. Chevreux B, Wetter T, Suhai S. Genome sequence assembly using trace signals and additional sequence information Computer Science and Biology. German Conference on Bioinformatics (CGB)99 1999
    [Google Scholar]
  45. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010;5: e11147 [CrossRef]
    [Google Scholar]
  46. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014;30: 2068– 2069 [CrossRef]
    [Google Scholar]
  47. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016;32: 929– 931 [CrossRef]
    [Google Scholar]
  48. 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 [CrossRef]
    [Google Scholar]
  49. Martínez-Hidalgo P, Ramírez-Bahena MH, Flores-Félix JD, Igual JM, Sanjuán J et al. Reclassification of strains MAFF 303099T and R7A into Mesorhizobium japonicum sp. nov. Int J Syst Evol Microbiol 2016;66: 4936– 4941
    [Google Scholar]
  50. Tighe SW, de Lajudie P, Dipietro K, Lindström K, Nick G et al. Analysis of cellular fatty acids and phenotypic relationships of Agrobacterium, Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium species using the sherlock microbial identification system. Int J Syst Evol Microbiol 2000;50: 787– 801 [CrossRef]
    [Google Scholar]
  51. Fumeaux C, Bakkou N, Kopćinska J, Golinowski W, Westenberg DJ et al. Functional analysis of the nifQdctA1y4vGHIJ operon of Sinorhizobium fredii strain NGR234 using a transposon with a NifA-dependent read-out promoter. Microbiology 2011;157: 2745– 2758 [CrossRef]
    [Google Scholar]
  52. Ramírez-Bahena MH, Peix A, Rivas R, Camacho M, Rodríguez-Navarro DN et al. Bradyrhizobium pachyrhizi sp. nov. and Bradyrhizobium jicamae sp. nov., isolated from effective nodules of Pachyrhizus erosus. Int J Syst Evol Microbiol 2009;59: 1929– 1934 [CrossRef]
    [Google Scholar]
  53. Delamuta JRM, Ribeiro RA, Ormeño-Orrillo E, Parma MM, Melo IS et al. Bradyrhizobium tropiciagri sp. nov. and Bradyrhizobium embrapense sp. nov., nitrogen-fixing symbionts of tropical forage legumes. Int J Syst Evol Microbiol 2015;65: 4424– 4433 [CrossRef]
    [Google Scholar]
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