Phylogenetic Co-Occurrence of ExoR, ExoS, and ChvI, Components of the RSI Bacterial Invasion Switch, Suggests a Key Adaptive Mechanism Regulating the Transition between Free-Living and Host-Invading Phases in Rhizobiales

Abstract

Both bacterial symbionts and pathogens rely on their host-sensing mechanisms to activate the biosynthetic pathways necessary for their invasion into host cells. The Gram-negative bacterium Sinorhizobium meliloti relies on its RSI (ExoR-ExoS-ChvI) Invasion Switch to turn on the production of succinoglycan, an exopolysaccharide required for its host invasion. Recent whole-genome sequencing efforts have uncovered putative components of RSI-like invasion switches in many other symbiotic and pathogenic bacteria. To explore the possibility of the existence of a common invasion switch, we have conducted a phylogenomic survey of orthologous ExoR, ExoS, and ChvI tripartite sets in more than ninety proteobacterial genomes. Our analyses suggest that functional orthologs of the RSI invasion switch co-exist in Rhizobiales, an order characterized by numerous invasive species, but not in the order’s close relatives. Phylogenomic analyses and reconstruction of orthologous sets of the three proteins in Alphaproteobacteria confirm Rhizobiales-specific gene synteny and congruent RSI evolutionary histories. Evolutionary analyses further revealed site-specific substitutions correlated specifically to either animal-bacteria or plant-bacteria associations. Lineage restricted conservation of any one specialized gene is in itself an indication of species adaptation. However, the orthologous phylogenetic co-occurrence of all interacting partners within this single signaling pathway strongly suggests that the development of the RSI switch was a key adaptive mechanism. The RSI invasion switch, originally found in S. meliloti, is a characteristic of the Rhizobiales, and potentially a conserved crucial activation step that may be targeted to control host invasion by pathogenic bacterial species.

Global fingerprint of humans on the distribution ofBartonellabacteria in mammals

“…The proliferation of studies investigating Bartonella in various wildlife populations allows for greater insights into the origins and evolution of Bartonella and its potential for spillover more than ever before. Bartonellaceae is nested within the Rhizobiales, a lineage of soil bacteria that contains nitrogen-fixing root-associated members (13). In our study, B. apis was the most basal strain of Bartonella .…”

“…The 16s rRNA gene is much less powerful for discriminating Bartonella species than gltA (7) and often metagenomic studies amplify only very small fragments of the gene, making it difficult for us to resolve fine scale diversification but we were able to determine that basal strains of Bartonella were largely found in environmental samples and non-hematophagous insects (Figure 1). Additionally, work on Bartonella has shown that the evolution of a type 4 secretion system, along with selection on other invasion mechanisms (13), has been instrumental in allowing Bartonella to diversify and invade host cells (23, 24) while other work has shown Bartonella can incorporate a type 4 secretion system via lateral gene transfer when it coinfects an amoeba with Rhizobium radiobacter (25). Further, examinations of lateral gene transfer of metabolic genes in Bartonella reveals that many of these genes derive from common insect gut commensal bacteria (26).…”

Genome‐wide identification of genes directly regulated by ChvI and a consensus sequence for ChvI binding in Sinorhizobium meliloti

“…ExoS is a membrane-bound histidine kinase with a periplasmic sensing domain and ChvI is a response regulator of the OmpR/PhoB family of response regulators (Cheng and Walker, 1998). ExoS/ChvI has orthologs in related α-proteobacteria (Vanderlinde and Yost, 2012;Heavner et al, 2015), and orthologs such as BvrS/BvrR in the mammalian pathogen Brucella abortus and ChvG/ChvI in the plant pathogen Agrobacterium tumefaciens are required for virulence (Charles and Nester, 1993;Sola-Landa et al, 1998;Heavner et al, 2015). ChvG/ChvI-dependent transcription is activated by acidic pH and BvrS/BvrR-dependent transcription is activated by acidic pH and nutrient limitation (Yuan et al, 2008;Altamirano-Silva et al, 2018).…”

Global fingerprint of humans on the distribution of Bartonella bacteria in mammals

“…The proliferation of studies investigating Bartonella in various wildlife populations allows for greater insights into the origins and evolution of Bartonella and its potential for spillover more than ever before. Bartonellaceae is nested within the Rhizobiales, a lineage of soil bacteria that contains nitrogen-fixing root-associated members [ 43 ]. In our study, the most basal strains of Bartonella were found in environmental samples and arthropods (Figs 1 and 2 ).…”

“…The 16s rRNA gene is much less powerful for discriminating Bartonella species than gltA [ 7 ] and often metagenomic studies amplify only very small fragments of the gene, making it difficult for us to resolve fine scale diversification but we were able to determine that basal strains of Bartonella were largely found in environmental samples and non-hematophagous insects ( Fig 1 ). Additionally, work on Bartonella has shown that the evolution of a type 4 secretion system, along with selection on other invasion mechanisms [ 43 ], has been instrumental in allowing Bartonella to diversify and invade host cells [ 46 , 47 ] while other work has shown Bartonella can incorporate a type 4 secretion system via lateral gene transfer when it coinfects an amoeba with Rhizobium radiobacter [ 48 ]. Further, examinations of lateral gene transfer of metabolic genes in Bartonella reveals that many of these genes derive from common insect gut commensal bacteria [ 49 ].…”