Why are rhizobial symbiosis genes mobile?

Abstract

Rhizobia are one of the most important and best studied groups of bacterial symbionts. They are defined by their ability to establish nitrogen-fixing intracellular infections within plant hosts. One surprising feature of this symbiosis is that the bacterial genes required for this complex trait are not fixed within the chromosome, but are encoded on mobile genetic elements (MGEs), namely plasmids or integrative and conjugative elements. Evidence suggests that many of these elements are actively mobilizing within rhizobial populations, suggesting that regular symbiosis gene transfer is part of the ecology of rhizobial symbionts. At first glance, this is counterintuitive. The symbiosis trait is highly complex, multipartite and tightly coevolved with the legume hosts, while transfer of genes can be costly and disrupt coadaptation between the chromosome and the symbiosis genes. However, horizontal gene transfer is a process driven not only by the interests of the host bacterium, but also, and perhaps predominantly, by the interests of the MGEs that facilitate it. Thus understanding the role of horizontal gene transfer in the rhizobium–legume symbiosis requires a ‘mobile genetic element's-eye view' on the ecology and evolution of this important symbiosis. This article is part of the theme issue ‘The secret lives of microbial mobile genetic elements’.

Fitness costs of CRISPR-Cas systems in bacteria

“…This correlation was primarily suggested to be because symbionts can benefit from an element of protection from viral predation by the host [5]. However, additional possible explanations include the potential environmental resource benefits a symbiotic relationship may confer, the fact that many symbiosis genes are carried on MGEs [65], and the integration with host signalling molecules required for engaging in a successful symbiosis. In support of a role for resource conditions and force of infection in shaping CRISPR-related selection dynamics, in Pseudomonas aeruginosa , CRISPR-based immunity has been shown to be selected for following phage challenge in resource-low conditions in vitro , versus receptor mutation-based defence in resource-rich conditions [44], with the force of infection (e.g.…”

MGEs as the MVPs of Partner Quality Variation in Legume-Rhizobium Symbiosis

“…We are witnessing a sea change in the way evolutionary biologists think and write about the mutualism between rhizobia and their legume hosts. While variation in these large and complex bacterial genomes and its impact on plant growth and fitness has been of interest for a long time, the “mobile genetic element’s (MGE)-eye view” ( 2 ) is making its mark on the questions we ask about mutualist partner quality, genome evolution, and geographic variation. Of course, the mobile nature of symbiosis genes in rhizobia is not particularly new ( 3 , 4 ), and evolutionary biologists like Jennifer Wernegreen recognized that symbiosis genes can have their own evolutionary history decades ago ( 5 , 6 ).…”

“…1 ). Selection might even drive mobilization of key sym genes among strains or even species of rhizobia ( 27 ), especially when host distributions are patchy ( 2 ). Weisberg and colleagues ( 1 ) identify several ineffective strains and test whether they may infect other sympatric species and provide comparable beneficial effects to these alternative hosts ( 1 ).…”

Introduction: the secret lives of microbial mobile genetic elements

“…The nitrogen-fixing symbiosis genes of Rhizobia provide an instructive example. In their review on the subject, Wardell et al [20] explain that the complex, multi-component and exquisitely coevolved symbiosis trait is encoded not as part of the core rhizobial genome but is instead located on mobile plasmids or integrative conjugative elements-imposing a fitness cost and impeding co-adaptation with the rest of the genome. Yet this phenomenon makes sense when considering the interests of the MGE and the symbiosis genes it carries: symbiosis mobility enables MGEs to take advantage of patchy selection in the heterogeneous soil environment, to sample different genomic environments, and facilitate competition between different symbiosis elements within the intracellular community.…”