Partners in space: Discordant population structure between legume hosts and rhizobium symbionts in their native range

Abstract

Coevolution is predicted to depend on how the genetic diversity of interacting species is geographically structured. Plant-microbe symbioses such as the legume-rhizobium mutualism are ecologically and economically important, but distinct life history and dispersal mechanisms for these macrobial and microbial partners, plus dynamic genome composition in bacteria, present challenges for understanding spatial genetic processes in these systems. Here we study the model rhizobium Ensifer meliloti using a hierarchically-structured sample of 191 strains from 21 sites in the native range and compare its population structure to that of its host plant Medicago truncatula. We find high local genomic variation and minimal isolation by distance across the rhizobium genome, particularly at the two symbiosis elements pSymA and pSymB, which have evolutionary histories and population structures similar to each other and distinct from both the chromosome and the host. While the chromosome displays weak isolation by distance, it is uncorrelated with hosts. Patterns of discordant population structure among elements with the bacterial genome has implications for bacterial adaptation to life in the soil versus symbiosis, while discordant population genetic structure of hosts and microbes might restrict local adaptation of species to each other and give rise to phenotypic mismatches in coevolutionary traits.

Phenotypic and genomic signatures of interspecies cooperation and conflict in naturally-occurring isolates of a model plant symbiont

“…Study system. Full details are provided in Riley et al (52) and SI Methods. Ensifer (formerly Sinorhizobium) meliloti is an Alphaproteobacteria that forms symbiosis with various Medicago spp., fixing atmospheric N in return for plant photosynthate.…”

“…DNA isolation, whole-genome sequencing, and variant calling. Detailed methods are provided in Riley et al(50), and SI Methods. We obtained DNA from each of the 191 rhizobium isolates, sequenced their full genomes including the chromosome and two symbiosis plasmids, used a common reference-based assembly pipeline to align sequences and call single nucleotide polymorphisms (SNPs), and filtered the resulting SNPs based on sequence quality, depth, minor allele frequency, and missingness, resulting in a total of 36,526 filtered SNPs.…”

Genome-wide association studies across environmental and genetic contexts reveal complex genetic architecture of symbiotic extended phenotypes

“…For example, by experimentally-evolving strains of S. meliloti on five M. truncatula lines, Batstone et al (66) found that local adaptation was largely governed by conditional neutrality (beneficial on local host, neutral on non-local hosts) or mildly deleterious effects on non-local hosts, likely due to drift in the local context. Yet, in nature where rhizobium population sizes are much larger and more diverse, and gene flow is present, the extent to which local adaptation occurs has rarely been tested but might be unlikely (28, 111, 112), except for populations differentiated by strong ecological gradients (e.g., 102). Moreover, the host genotypes used in our study, DZA and A17, are unlikely to share an evolutionary history with our strains, and so it remains unclear whether stronger trade-offs (and less conditional neutrality) would be present if our strains shared an evolutionary history with the host lines being tested.…”

“…Previous mapping efforts in the legume-rhizobium system have focused on the HapMap collections, which maximize diversity using a range-wide sample. Our study focuses on the segregating natural variation at a smaller geographic scale, a scale at which pSymA and pSymB segregate (107); thus the G × G-driven variation we find here would be available to local evolutionary and/or coevolutionary processes. G × G interactions for fitness outcomes have long been of interest in the legume-rhizobium symbiosis (25,116,28,97,117) and other interactions (118,119,120) (132,133,134,135).…”