Phylogenomic Analyses of Bradyrhizobium Reveal Uneven Distribution of the Lateral and Subpolar Flagellar Systems, Which Extends to Rhizobiales

Garrido‐Sanz, Daniel; Redondo‐Nieto, Miguel; Mongiardini, Elías J.; Blanco-Romero, Esther; Durán, David; Quelas, Juan Ignacio; Martín, Marta; Rivilla, Rafael; Lodeiro, Aníbal Roberto; Althabegoiti, María Julia

doi:10.3390/microorganisms7020050

Cited by 14 publications

(19 citation statements)

References 63 publications

(100 reference statements)

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“…Notably, during the compilation of this paper, two phylogenomic analyses focusing on the genus Bradyrhizobium were published, but they did not include exactly the same taxa as our study. One study was also based on the core genome [50], whereas the other was based on the genome-to-genome blast distance phylogeny (GBDP) [51]. The phylogenetic trees of these two studies show a very similar topology to that presented here (), which confirms the robustness of these different phylogenomic analyses.…”

Section: Resultssupporting

confidence: 65%

Phylogenetic distribution and evolutionary dynamics of nod and T3SS genes in the genus Bradyrhizobium

et al. 2020

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Bradyrhizobium are abundant soil bacteria and the major symbiont of legumes. The recent availability of Bradyrhizobium genome sequences provides a large source of information for analysis of symbiotic traits. In this study, we investigated the evolutionary dynamics of the nodulation genes (nod) and their relationship with the genes encoding type III secretion systems (T3SS) and their effectors among bradyrhizobia. Based on the comparative analysis of 146 Bradyrhizobium genome sequences, we identified six different types of T3SS gene clusters. The two predominant cluster types are designated RhcIa and RhcIb and both belong to the RhcI-T3SS family previously described in other rhizobia. They are found in 92/146 strains, most of them also containing nod genes. RhcIa and RhcIb gene clusters differ in the genes they carry: while the translocon-encoding gene nopX is systematically found in strains containing RhcIb, the nopE and nopH genes are specifically conserved in strains containing RhcIa, suggesting that these last two genes might functionally substitute nopX and play a role related to effector translocation. Phylogenetic analysis suggests that bradyrhizobia simultaneously gained nod and RhcI-T3SS gene clusters via horizontal transfer or subsequent vertical inheritance of a symbiotic island containing both. Sequence similarity searches for known Nop effector proteins in bradyrhizobial proteomes revealed the absence of a so-called core effectome, i.e. that no effector is conserved among all Bradyrhizobium strains. However, NopM and SUMO proteases were found to be the main effector families, being represented in the majority of the genus. This study indicates that bradyrhizobial T3SSs might play a more significant symbiotic role than previously thought and provides new candidates among T3SS structural proteins and effectors for future functional investigations.

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Section: Resultssupporting

confidence: 65%

Phylogenetic distribution and evolutionary dynamics of nod and T3SS genes in the genus Bradyrhizobium

et al. 2020

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“…The alignment of FliL S and FliL L amino acid sequences indicated a low relationship, with 19.8% identity and 40% similarity between them ( Fig. S1B), in agreement with their pertaining to evolutionary different flagellar systems (3). To further characterize their relationship with other FliL proteins, we constructed the cladogram shown in Fig.…”

Section: Resultsmentioning

confidence: 52%

Characterization of FliL Proteins in Bradyrhizobium diazoefficiens: Lateral FliL Supports Swimming Motility, and Subpolar FliL Modulates the Lateral Flagellar System

et al. 2020

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Bradyrhizobium diazoefficiens is a soil alphaproteobacterium that possesses two evolutionarily distinct flagellar systems, a constitutive subpolar flagellum and inducible lateral flagella that, depending on the carbon source, may be expressed simultaneously in liquid medium and used interactively for swimming. In each system, more than 30 genes encode the flagellar proteins, most of which are well characterized. Among the exceptions is FliL, which has been scarcely studied in alphaproteobacteria and whose function in other bacterial classes is somewhat controversial. Because each B. diazoefficiens flagellar system contains its own fliL paralog, we obtained the respective deletions ΔfliLS (subpolar) and ΔfliLL (lateral) to study their functions in swimming. We determined that FliLL was essential for lateral flagellum-driven motility. FliLS was dispensable for swimming in either liquid or semisolid medium; however, it was found to play a crucial role in upregulation of the lateral flagellum regulon under conditions of increased viscosity/flagellar load. Therefore, although FliLS seems to be not essential for swimming, it may participate in a mechanosensor complex that controls lateral flagellum induction. IMPORTANCE Bacterial motility propelled by flagella is an important trait in most environments, where microorganisms must explore the habitat toward beneficial resources and evade toxins. Most bacterial species have a unique flagellar system, but a few species possess two different flagellar systems in the same cell. An example is Bradyrhizobium diazoefficiens, the N2-fixing symbiont of soybean, which uses both systems for swimming. Among the less-characterized flagellar proteins is FliL, a protein typically associated with a flagellum-driven surface-based collective motion called swarming. By using deletion mutants in each flagellar system’s fliL, we observed that one of them (lateral) was required for swimming, while the other (subpolar) took part in the control of lateral flagellum synthesis. Hence, this protein seems to participate in the coordination of activity and production of both flagellar systems.

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“…A recent study has identified orthologous flag-2 loci among members of the alpha-proteobacterial order Rhizobiales and furthermore, they are similar to the lateral flagellar system of Vibrio and Aeromonas spp. [15,37]. A more (See figure on previous page.)…”

Section: Discussionmentioning

confidence: 96%

Comparative genomic analysis of the secondary flagellar (flag-2) system in the order Enterobacterales

2020

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Background: The order Enterobacterales encompasses a broad range of metabolically and ecologically versatile bacterial taxa, most of which are motile by means of peritrichous flagella. Flagellar biosynthesis has been linked to a primary flagella locus, flag-1, encompassing~50 genes. A discrete locus, flag-2, encoding a distinct flagellar system, has been observed in a limited number of enterobacterial taxa, but its function remains largely uncharacterized.Results: Comparative genomic analyses showed that orthologous flag-2 loci are present in 592/4028 taxa belonging to 5/8 and 31/76 families and genera, respectively, in the order Enterobacterales. Furthermore, the presence of only the outermost flag-2 genes in many taxa suggests that this locus was far more prevalent and has subsequently been lost through gene deletion events. The flag-2 loci range in size from~3.4 to 81.1 kilobases and code for between five and 102 distinct proteins. The discrepancy in size and protein number can be attributed to the presence of cargo gene islands within the loci. Evolutionary analyses revealed a complex evolutionary history for the flag-2 loci, representing ancestral elements in some taxa, while showing evidence of recent horizontal acquisition in other enterobacteria. Conclusions:The flag-2 flagellar system is a fairly common, but highly variable feature among members of the Enterobacterales. Given the energetic burden of flagellar biosynthesis and functioning, the prevalence of a second flagellar system suggests it plays important biological roles in the enterobacteria and we postulate on its potential role as locomotory organ or as secretion system.

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Phylogenomic Analyses of Bradyrhizobium Reveal Uneven Distribution of the Lateral and Subpolar Flagellar Systems, Which Extends to Rhizobiales

Cited by 14 publications

References 63 publications

Phylogenetic distribution and evolutionary dynamics of nod and T3SS genes in the genus Bradyrhizobium

Phylogenetic distribution and evolutionary dynamics of nod and T3SS genes in the genus Bradyrhizobium

Characterization of FliL Proteins in Bradyrhizobium diazoefficiens: Lateral FliL Supports Swimming Motility, and Subpolar FliL Modulates the Lateral Flagellar System

Comparative genomic analysis of the secondary flagellar (flag-2) system in the order Enterobacterales

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