Host-selected mutations converging on a global regulator drive an adaptive leap towards symbiosis in bacteria

Pankey, M. Sabrina; Foxall, Randi L; Ster, Ian M; Perry, Lauren A; Schuster, Brian G.; Donner, Rachel A; Coyle, Matthew; Cooper, Vaughn S.; Whistler, Cheryl A.

doi:10.7554/elife.24414

Cited by 48 publications

(25 citation statements)

References 155 publications

(294 reference statements)

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“…Strikingly, all identified adaptive mutations for infection affect global regulatory proteins (HrpG, VsrA, EfpR, PhcA) controlling, positively or negatively, the expression of several hundreds of genes (Figure 3) [23,86,[89][90][91][92]. This is in accordance with other evolution experiments in which global regulators were frequently targeted [93][94][95][96][97]. Our results confirmed that mutations in global regulators can be highly beneficial by changing the expression of hundreds of genes in a concerted way, particularly during the first steps of adaptation to a new environment [98].…”

Section: Regulatory Rewiring Of the Recipient Genome As A Main Driversupporting

confidence: 86%

Experimental Evolution of Legume Symbionts: What Have We Learnt?

Moura

Remigi

Masson‐Boivin

et al. 2020

Genes

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Rhizobia, the nitrogen-fixing symbionts of legumes, are polyphyletic bacteria distributed in many alpha- and beta-proteobacterial genera. They likely emerged and diversified through independent horizontal transfers of key symbiotic genes. To replay the evolution of a new rhizobium genus under laboratory conditions, the symbiotic plasmid of Cupriavidus taiwanensis was introduced in the plant pathogen Ralstonia solanacearum, and the generated proto-rhizobium was submitted to repeated inoculations to the C. taiwanensis host, Mimosa pudica L. This experiment validated a two-step evolutionary scenario of key symbiotic gene acquisition followed by genome remodeling under plant selection. Nodulation and nodule cell infection were obtained and optimized mainly via the rewiring of regulatory circuits of the recipient bacterium. Symbiotic adaptation was shown to be accelerated by the activity of a mutagenesis cassette conserved in most rhizobia. Investigating mutated genes led us to identify new components of R. solanacearum virulence and C. taiwanensis symbiosis. Nitrogen fixation was not acquired in our short experiment. However, we showed that post-infection sanctions allowed the increase in frequency of nitrogen-fixing variants among a non-fixing population in the M. pudica–C. taiwanensis system and likely allowed the spread of this trait in natura. Experimental evolution thus provided new insights into rhizobium biology and evolution.

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Section: Regulatory Rewiring Of the Recipient Genome As A Main Driversupporting

confidence: 86%

Experimental Evolution of Legume Symbionts: What Have We Learnt?

Moura

Remigi

Masson‐Boivin

et al. 2020

Genes

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“…Interestingly, in Cupriavidus taiwanensis, a Ralstonianeighboring taxon that evolved into Mimosa symbionts, the phcB and phcS orthologous genes were found under positive selection and associated with the transition to symbiosis during the natural evolution of this rhizobium species (29), likely reflecting the need to adjust QS to the legume endosymbiotic niche. Adaptive mutations altering QS responsiveness were also evidenced during experimental and natural evolution of other pathogenic and symbiotic bacteria such as Vibrio fischeri and Staphylococcus aureus (35)(36)(37)(38), exemplifying the role of these sensory systems in bacterial adaptation and phenotypic diversification. The role of QS in rhizobial symbiosis is, however, variable, either neutral (39), positive (40)(41)(42), or negative (43,44).…”

Section: Discussionmentioning

confidence: 94%

Modulation of Quorum Sensing as an Adaptation to Nodule Cell Infection during Experimental Evolution of Legume Symbionts

Tang

Bouchez

Cruveiller

et al. 2020

mBio

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Over millions of years, changes have occurred in regulatory circuitries in response to genome reorganization and/or persistent changes in environmental conditions. How bacteria optimize regulatory circuitries is crucial to understand bacterial adaptation. Here, we analyzed the experimental evolution of the plant pathogen Ralstonia solanacearum into legume symbionts after the transfer of a natural plasmid encoding the essential mutualistic genes. We showed that the Phc quorum sensing system required for the virulence of the ancestral bacterium was reconfigured to improve intracellular infection of root nodules induced by evolved Ralstonia. A single mutation in either the PhcB autoinducer synthase or the PhcQ regulator of the sensory cascade tuned the kinetics of activation of the central regulator PhcA in response to cell density so that the minimal stimulatory concentration of autoinducers needed for a given response was increased. Yet, a change in the expression of a PhcA target gene was observed in infection threads progressing in root hairs, suggesting early programming for the late accommodation of bacteria in nodule cells. Moreover, this delayed switch to the quorum sensing mode decreased the pathogenicity of the ancestral strain, illustrating the functional plasticity of regulatory systems and showing how a small modulation in signal response can produce drastic changes in bacterial lifestyle. IMPORTANCE Rhizobia are soil bacteria from unrelated genera able to form a mutualistic relationship with legumes. Bacteria induce the formation of root nodules, invade nodule cells, and fix nitrogen to the benefit of the plant. Rhizobial lineages emerged from the horizontal transfer of essential symbiotic genes followed by genome remodeling to activate and/or optimize the acquired symbiotic potential. This evolutionary scenario was replayed in a laboratory evolution experiment in which the plant pathogen Ralstonia solanacearum successively evolved the capacities to nodulate Mimosa pudica and poorly invade, then massively invade, nodule cells. In some lines, the improvement of intracellular infection was achieved by mutations modulating a quorum sensing regulatory system of the ancestral strain. This modulation that affects the activity of a central regulator during the earliest stages of symbiosis has a huge impact on late stages of symbiosis. This work showed that regulatory rewiring is the main driver of this pathogeny-symbiosis transition.

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“…Additionally, we note that the sypE frameshift is not present in SR5, arguing for distinct modes of biofilm regulation in groups A, B, and C. At the same time, this study provides evidence that some aspects of biofilm regulation are conserved in diverse squid symbionts, such as the effects of the strong biofilm negative regulator BinK. Published data indicate that evolved BinK alleles can alter colonization of H905 (group B) and MJ11 (group C), and that a deletion of MJ11 binK leads to enhanced colonization (20). Our experiments in Fig.…”

Section: Discussionmentioning

confidence: 53%

“…The entire colonization lifecycle likely requires a balance between biofilm formation/cohesion and biofilm dispersal, and these data argue that group A strains are more strongly tilted toward the biofilm-producing state. There is evidence that strains lacking BinK exhibit a colonization advantage in the laboratory (18,20), suggesting that this strategy of more readily forming biofilms provides a fitness advantage in nature. At the same time, the biofilm negative regulator BinK is conserved among V. fischeri strains examined (including MB11B1 [Fig.…”

Section: Discussionmentioning

confidence: 99%

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Natural Strain Variation Reveals Diverse Biofilm Regulation in Squid-Colonizing Vibrio fischeri

et al. 2019

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The mutualistic symbiont Vibrio fischeri builds a symbiotic biofilm during colonization of squid hosts. Regulation of the exopolysaccharide component, termed Syp, has been examined in strain ES114, where production is controlled by a phosphorelay that includes the inner membrane hybrid histidine kinase RscS. Most strains that lack RscS or encode divergent RscS proteins cannot colonize a squid host unless RscS from a squid symbiont is heterologously expressed. In this study, we examine V. fischeri isolates worldwide to understand the landscape of biofilm regulation during beneficial colonization. We provide a detailed study of three distinct evolutionary groups of V. fischeri and find that while the RscS-Syp biofilm pathway is required in one of the groups, two other groups of squid symbionts require Syp independent of RscS. Mediterranean squid symbionts, including V. fischeri SR5, colonize without an RscS homolog encoded by their genome. Additionally, group A V. fischeri strains, which form a tightly related clade of Hawaii isolates, have a frameshift in rscS and do not require the gene for squid colonization or competitive fitness. These same strains have a frameshift in sypE, and we provide evidence that this group A sypE allele leads to an upregulation in biofilm activity. Thus, this work describes the central importance of Syp biofilm in colonization of diverse isolates and demonstrates that significant evolutionary transitions correspond to regulatory changes in the syp pathway. IMPORTANCE Biofilms are surface-associated, matrix-encased bacterial aggregates that exhibit enhanced protection to antimicrobial agents. Previous work has established the importance of biofilm formation by a strain of luminous Vibrio fischeri bacteria as the bacteria colonize their host, the Hawaiian bobtail squid. In this study, expansion of this work to many natural isolates revealed that biofilm genes are universally required, yet there has been a shuffling of the regulators of those genes. This work provides evidence that even when bacterial behaviors are conserved, dynamic regulation of those behaviors can underlie evolution of the host colonization phenotype. Furthermore, this work emphasizes the importance of investigating natural diversity as we seek to understand molecular mechanisms in bacteria.A fundamental question in studying host-associated bacterial communities is understanding how specific microbial taxa assemble reproducibly in their host. Key insights into these processes were first obtained by studying plant-associated microbes, and the discovery and characterization of Nod factors in rhizobia were valuable to understanding how partner choice between microbe and host could be mediated at the molecular level (1, 2). There are complex communities in humans and other vertebrate animals, yet metagenomic and imaging analyses of these communities have Citation Rotman ER,

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Host-selected mutations converging on a global regulator drive an adaptive leap towards symbiosis in bacteria

Cited by 48 publications

References 155 publications

Experimental Evolution of Legume Symbionts: What Have We Learnt?

Experimental Evolution of Legume Symbionts: What Have We Learnt?

Modulation of Quorum Sensing as an Adaptation to Nodule Cell Infection during Experimental Evolution of Legume Symbionts

Natural Strain Variation Reveals Diverse Biofilm Regulation in Squid-Colonizing Vibrio fischeri

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