Abstract
BackgroundRhizobial 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.ResultsIn 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.ConclusionThe transcriptional response to root exudates was correlated to each strain nodulation competitiveness, with Burkholderia phymatum appearing as the best specialised symbiont of Mimosa pudica.
Highlights
Rhizobial symbionts belong to the classes Alphaproteobacteria and Betaproteobacteria
We investigated the molecular bases of competitiveness and symbiosis between three representative and well-studied M. pudica-nodulating symbiotic strains of Burkholderia (B. phymatum STM815), Cupriavidus (C. taiwanensis LMG19424) and Rhizobium (R. mesoamericanum STM3625) by studying their transcriptomic response to root exudates as a mimicking condition of early symbiotic events
We observed that B. phymatum STM815 (BP) has the most substantial response to Root Exudates (RE) both quantitatively and qualitatively compared to C. taiwanensis LMG19424 (CT) and R. mesoamericanum STM3625 (RM), which is in line with its high competitiveness recorded in previous work on Mimosa [29] and more recently on papilionoid legumes [88]
Summary
Rhizobial symbionts belong to the classes Alphaproteobacteria and Betaproteobacteria (called “alpha” and “beta”-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. Rhizobial species are mainly distributed among four genera of Alphaproteobacteria (Rhizobium, Sinorhizobium, Mesorhizobium, Bradyrhizobium; and a few species in seven other genera) and two genera of Betaproteobacteria (Burkholderia, Cupriavidus) leading to the proposal of the terms alpha- and beta-rhizobia to distinguish both classes of symbionts [3]. If beta-rhizobia appeared controversial at the time of their discovery, it is well established that Burkholderia species are the main symbionts of several endemic species of the Mimosoideae and Papilinoideae legume subfamilies in Brazil and South Africa [4,5,6,7], which raises questions about the origin of symbiosis and performance of these new symbionts compared to alpha-rhizobia. Many symbiotic species of Burkholderia (recently rearranged in the Paraburkholderia genus [8]) have been described from mimosoids: B. phymatum [9], B. tuberum [10], B. mimosarum [11], B. nodosa [12, 13], B. sabiae [14], B. symbiotica [15], B. diazotrophica [16], B. piptadeniae and B. ribeironis [17], while Cupriavidus symbionts (C. taiwanensis, C. necator, C. pinatubonensis) were detected mostly in invasive Mimosa species (M. pudica, M. pigra, M. diplotricha) in South, Central and North America [10, 18, 19], in Asia (China, India, Taiwan, Philippines, New Caledonia, Papua New Guinea) [20,21,22,23,24], and in native Mimosa and Parapiptadenia species in Uruguay [25, 26]
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