Transcriptomic Profiling of Burkholderia Phymatum STM815, Cupriavidus Taiwanensis LMG19424 and Rhizobium Mesoamericanum STM3625 in Response to Mimosa Pudica Root Exudates Illuminates the Molecular Basis of Their Nodulation Competitiveness And...

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2018 Jan 31

PMID 29378510

Citations 15

Authors

Agnieszka Klonowska

Remy Melkonian

Lucie Miche

Pierre Tisseyre

Lionel Moulin

Affiliations

Soon will be listed here.

Abstract

Background: Rhizobial symbionts belong to the classes Alphaproteobacteria and Betaproteobacteria (called "alpha" and "beta"-rhizobia). Most knowledge on the genetic basis of symbiosis is based on model strains belonging to alpha-rhizobia. Mimosa pudica is a legume that offers an excellent opportunity to study the adaptation toward symbiotic nitrogen fixation in beta-rhizobia compared to alpha-rhizobia. In a previous study (Melkonian et al., Environ Microbiol 16:2099-111, 2014) we described the symbiotic competitiveness of M. pudica symbionts belonging to Burkholderia, Cupriavidus and Rhizobium species.

Results: In this article we present a comparative analysis of the transcriptomes (by RNAseq) of B. phymatum STM815 (BP), C. taiwanensis LMG19424 (CT) and R. mesoamericanum STM3625 (RM) in conditions mimicking the early steps of symbiosis (i.e. perception of root exudates). BP exhibited the strongest transcriptome shift both quantitatively and qualitatively, which mirrors its high competitiveness in the early steps of symbiosis and its ancient evolutionary history as a symbiont, while CT had a minimal response which correlates with its status as a younger symbiont (probably via acquisition of symbiotic genes from a Burkholderia ancestor) and RM had a typical response of Alphaproteobacterial rhizospheric bacteria. Interestingly, the upregulation of nodulation genes was the only common response among the three strains; the exception was an up-regulated gene encoding a putative fatty acid hydroxylase, which appears to be a novel symbiotic gene specific to Mimosa symbionts.

Conclusion: The transcriptional response to root exudates was correlated to each strain nodulation competitiveness, with Burkholderia phymatum appearing as the best specialised symbiont of Mimosa pudica.

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References

Chen W, de Faria S, Chou J, James E, Elliott G, Sprent J . Burkholderia sabiae sp. nov., isolated from root nodules of Mimosa caesalpiniifolia. Int J Syst Evol Microbiol. 2008; 58(Pt 9):2174-9. DOI: 10.1099/ijs.0.65816-0. View

Liu X, Wei S, Wang F, James E, Guo X, Zagar C . Burkholderia and Cupriavidus spp. are the preferred symbionts of Mimosa spp. in southern China. FEMS Microbiol Ecol. 2012; 80(2):417-26. DOI: 10.1111/j.1574-6941.2012.01310.x. View

Angus A, Agapakis C, Fong S, Yerrapragada S, Estrada-de Los Santos P, Yang P . Plant-associated symbiotic Burkholderia species lack hallmark strategies required in mammalian pathogenesis. PLoS One. 2014; 9(1):e83779. PMC: 3885511. DOI: 10.1371/journal.pone.0083779. View

Fernandez-Lopez R, Garcillan-Barcia M, Revilla C, Lazaro M, Vielva L, de la Cruz F . Dynamics of the IncW genetic backbone imply general trends in conjugative plasmid evolution. FEMS Microbiol Rev. 2006; 30(6):942-66. DOI: 10.1111/j.1574-6976.2006.00042.x. View

Klonowska A, Chaintreuil C, Tisseyre P, Miche L, Melkonian R, Ducousso M . Biodiversity of Mimosa pudica rhizobial symbionts (Cupriavidus taiwanensis, Rhizobium mesoamericanum) in New Caledonia and their adaptation to heavy metal-rich soils. FEMS Microbiol Ecol. 2012; 81(3):618-35. DOI: 10.1111/j.1574-6941.2012.01393.x. View

Mimmack M, Borthakur D, Jones M, Downie J, Johnston A . The psi operon of Rhizobium leguminosarum biovar phaseoli: identification of two genes whose products are located at the bacterial cell surface. Microbiology (Reading). 1994; 140 ( Pt 5):1223-9. DOI: 10.1099/13500872-140-5-1223. View

Gyaneshwar P, Hirsch A, Moulin L, Chen W, Elliott G, Bontemps C . Legume-nodulating betaproteobacteria: diversity, host range, and future prospects. Mol Plant Microbe Interact. 2011; 24(11):1276-88. DOI: 10.1094/MPMI-06-11-0172. View

Ampe F, Kiss E, Sabourdy F, Batut J . Transcriptome analysis of Sinorhizobium meliloti during symbiosis. Genome Biol. 2003; 4(2):R15. PMC: 151305. DOI: 10.1186/gb-2003-4-2-r15. View

Dunn M, Ramirez-Trujillo J, Hernandez-Lucas I . Major roles of isocitrate lyase and malate synthase in bacterial and fungal pathogenesis. Microbiology (Reading). 2009; 155(Pt 10):3166-3175. DOI: 10.1099/mic.0.030858-0. View

10.

Barrett C, Parker M . Coexistence of Burkholderia, Cupriavidus, and Rhizobium sp. nodule bacteria on two Mimosa spp. in Costa Rica. Appl Environ Microbiol. 2006; 72(2):1198-206. PMC: 1392967. DOI: 10.1128/AEM.72.2.1198-1206.2006. View

11.

Giltner C, Habash M, Burrows L . Pseudomonas aeruginosa minor pilins are incorporated into type IV pili. J Mol Biol. 2010; 398(3):444-61. DOI: 10.1016/j.jmb.2010.03.028. View

12.

Chen W, Laevens S, Lee T, Coenye T, de Vos P, Mergeay M . Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa species and sputum of a cystic fibrosis patient. Int J Syst Evol Microbiol. 2001; 51(Pt 5):1729-1735. DOI: 10.1099/00207713-51-5-1729. View

13.

Camerini S, Senatore B, Lonardo E, Imperlini E, Bianco C, Moschetti G . Introduction of a novel pathway for IAA biosynthesis to rhizobia alters vetch root nodule development. Arch Microbiol. 2008; 190(1):67-77. DOI: 10.1007/s00203-008-0365-7. View

14.

Andam C, Mondo S, Parker M . Monophyly of nodA and nifH genes across Texan and Costa Rican populations of Cupriavidus nodule symbionts. Appl Environ Microbiol. 2007; 73(14):4686-90. PMC: 1932833. DOI: 10.1128/AEM.00160-07. View

15.

Coutinho B, Mitter B, Talbi C, Sessitsch A, Bedmar E, Halliday N . Regulon studies and in planta role of the BraI/R quorum-sensing system in the plant-beneficial Burkholderia cluster. Appl Environ Microbiol. 2013; 79(14):4421-32. PMC: 3697526. DOI: 10.1128/AEM.00635-13. View

16.

Roche P, Lerouge P, Ponthus C, Prome J . Structural determination of bacterial nodulation factors involved in the Rhizobium meliloti-alfalfa symbiosis. J Biol Chem. 1991; 266(17):10933-40. View

17.

Lemaire B, Dlodlo O, Chimphango S, Stirton C, Schrire B, Boatwright J . Symbiotic diversity, specificity and distribution of rhizobia in native legumes of the Core Cape Subregion (South Africa). FEMS Microbiol Ecol. 2015; 91(2):1-17. DOI: 10.1093/femsec/fiu024. View

18.

Kohler P, Zheng J, Schoffers E, Rossbach S . Inositol catabolism, a key pathway in sinorhizobium meliloti for competitive host nodulation. Appl Environ Microbiol. 2010; 76(24):7972-80. PMC: 3008233. DOI: 10.1128/AEM.01972-10. View

19.

Amadou C, Pascal G, Mangenot S, Glew M, Bontemps C, Capela D . Genome sequence of the beta-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Res. 2008; 18(9):1472-83. PMC: 2527706. DOI: 10.1101/gr.076448.108. View

20.

Masson-Boivin C, Giraud E, Perret X, Batut J . Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes?. Trends Microbiol. 2009; 17(10):458-66. DOI: 10.1016/j.tim.2009.07.004. View