skip to main content


Title: Phenotypic and genomic signatures of interspecies cooperation and conflict in naturally occurring isolates of a model plant symbiont
Given the need to predict the outcomes of (co)evolution in host-associated microbiomes, whether microbial and host fitnesses tend to trade-off, generating conflict, remains a pressing question. Examining the relationships between host and microbe fitness proxies at both the phenotypic and genomic levels can illuminate the mechanisms underlying interspecies cooperation and conflict. We examined naturally occurring genetic variation in 191 strains of the model microbial symbiont Sinorhizobium meliloti , paired with each of two host Medicago truncatula genotypes in single- or multi-strain experiments to determine how multiple proxies of microbial and host fitness were related to one another and test key predictions about mutualism evolution at the genomic scale, while also addressing the challenge of measuring microbial fitness. We found little evidence for interspecies fitness conflict; loci tended to have concordant effects on both microbe and host fitnesses, even in environments with multiple co-occurring strains. Our results emphasize the importance of quantifying microbial relative fitness for understanding microbiome evolution and thus harnessing microbiomes to improve host fitness. Additionally, we find that mutualistic coevolution between hosts and microbes acts to maintain, rather than erode, genetic diversity, potentially explaining why variation in mutualism traits persists in nature.  more » « less
Award ID(s):
1856744 1645875 2022049
NSF-PAR ID:
10349813
Author(s) / Creator(s):
; ;
Date Published:
Journal Name:
Proceedings of the Royal Society B: Biological Sciences
Volume:
289
Issue:
1978
ISSN:
0962-8452
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    Evolutionary biologists typically envision a trait’s genetic basis and fitness effects occurring within a single species. However, traits can be determined by and have fitness consequences for interacting species, thus evolving in multiple genomes. This is especially likely in mutualisms, where species exchange fitness benefits and can associate over long periods of time. Partners may experience evolutionary conflict over the value of a multi-genomic trait, but such conflicts may be ameliorated by mutualism’s positive fitness feedbacks. Here, we develop a simulation model of a host–microbe mutualism to explore the evolution of a multi-genomic trait. Coevolutionary outcomes depend on whether hosts and microbes have similar or different optimal trait values, strengths of selection and fitness feedbacks. We show that genome-wide association studies can map joint traits to loci in multiple genomes and describe how fitness conflict and fitness feedback generate different multi-genomic architectures with distinct signals around segregating loci. Partner fitnesses can be positively correlated even when partners are in conflict over the value of a multi-genomic trait, and conflict can generate strong mutualistic dependency. While fitness alignment facilitates rapid adaptation to a new optimum, conflict maintains genetic variation and evolvability, with implications for applied microbiome science. 
    more » « less
  2. Wilson, Daniel ; Parkhill, Julian (Ed.)
    ABSTRACT A goal of modern biology is to develop the genotype-phenotype (G→P) map, a predictive understanding of how genomic information generates trait variation that forms the basis of both natural and managed communities. As microbiome research advances, however, it has become clear that many of these traits are symbiotic extended phenotypes , being governed by genetic variation encoded not only by the host’s own genome, but also by the genomes of myriad cryptic symbionts. Building a reliable G→P map therefore requires accounting for the multitude of interacting genes and even genomes involved in symbiosis. Here, we use naturally occurring genetic variation in 191 strains of the model microbial symbiont Sinorhizobium meliloti paired with two genotypes of the host Medicago truncatula in four genome-wide association studies (GWAS) to determine the genomic architecture of a key symbiotic extended phenotype— partner quality , or the fitness benefit conferred to a host by a particular symbiont genotype, within and across environmental contexts and host genotypes. We define three novel categories of loci in rhizobium genomes that must be accounted for if we want to build a reliable G→P map of partner quality; namely, (i) loci whose identities depend on the environment, (ii) those that depend on the host genotype with which rhizobia interact, and (iii) universal loci that are likely important in all or most environments. IMPORTANCE Given the rapid rise of research on how microbiomes can be harnessed to improve host health, understanding the contribution of microbial genetic variation to host phenotypic variation is pressing, and will better enable us to predict the evolution of (and select more precisely for) symbiotic extended phenotypes that impact host health. We uncover extensive context-dependency in both the identity and functions of symbiont loci that control host growth, which makes predicting the genes and pathways important for determining symbiotic outcomes under different conditions more challenging. Despite this context-dependency, we also resolve a core set of universal loci that are likely important in all or most environments, and thus, serve as excellent targets both for genetic engineering and future coevolutionary studies of symbiosis. 
    more » « less
  3. Glass, Jennifer B. (Ed.)
    ABSTRACT The environmental context of the nitrogen-fixing mutualism between leguminous plants and rhizobial bacteria varies over space and time. Variation in resource availability, population density, and composition likely affect the ecology and evolution of rhizobia and their symbiotic interactions with hosts. We examined how host genotype, nitrogen addition, rhizobial density, and community complexity affected selection on 68 rhizobial strains in the Sinorhizobium meliloti – Medicago truncatula mutualism. As expected, host genotype had a substantial effect on the size, number, and strain composition of root nodules (the symbiotic organ). The understudied environmental variable of rhizobial density had a stronger effect on nodule strain frequency than the addition of low nitrogen levels. Higher inoculum density resulted in a nodule community that was less diverse and more beneficial but only in the context of the more selective host genotype. Higher density resulted in more diverse and less beneficial nodule communities with the less selective host. Density effects on strain composition deserve additional scrutiny as they can create feedback between ecological and evolutionary processes. Finally, we found that relative strain rankings were stable across increasing community complexity (2, 3, 8, or 68 strains). This unexpected result suggests that higher-order interactions between strains are rare in the context of nodule formation and development. Our work highlights the importance of examining mechanisms of density-dependent strain fitness and developing theoretical predictions that incorporate density dependence. Furthermore, our results have translational relevance for overcoming establishment barriers in bioinoculants and motivating breeding programs that maintain beneficial plant-microbe interactions across diverse agroecological contexts. IMPORTANCE Legume crops establish beneficial associations with rhizobial bacteria that perform biological nitrogen fixation, providing nitrogen to plants without the economic and greenhouse gas emission costs of chemical nitrogen inputs. Here, we examine the influence of three environmental factors that vary in agricultural fields on strain relative fitness in nodules. In addition to manipulating nitrogen, we also use two biotic variables that have rarely been examined: the rhizobial community's density and complexity. Taken together, our results suggest that (i) breeding legume varieties that select beneficial strains despite environmental variation is possible, (ii) changes in rhizobial population densities that occur routinely in agricultural fields could drive evolutionary changes in rhizobial populations, and (iii) the lack of higher-order interactions between strains will allow the high-throughput assessments of rhizobia winners and losers during plant interactions. 
    more » « less
  4. Abstract

    Most insects harbour influential, yet non‐essential heritable microbes in their hemocoel. Communities of these symbionts exhibit low diversity. But their frequent multi‐species nature raises intriguing questions on roles for symbiont–symbiont synergies in host adaptation, and on the stability of the symbiont communities, themselves. In this study, we build on knowledge of species‐defined symbiont community structure across US populations of the pea aphid,Acyrthosiphon pisum. Through extensive symbiont genotyping, we show that pea aphids' microbiomes can be more precisely defined at the symbiont strain level, with strain variability shaping five out of nine previously reported co‐infection trends. Field data provide a mixture of evidence for synergistic fitness effects and symbiont hitchhiking, revealing causes and consequences of these co‐infection trends. To test whether within‐host metabolic interactions predict common versus rare strain‐defined communities, we leveraged the high relatedness of our dominant, community‐defined symbiont strains vs. 12 pea aphid‐derived Gammaproteobacteria with sequenced genomes. Genomic inference, using metabolic complementarity indices, revealed high potential for cooperation among one pair of symbionts—Serratia symbioticaandRickettsiella viridis. Applying the expansion network algorithm, through additional use of pea aphid and obligateBuchnerasymbiont genomes,SerratiaandRickettsiellaemerged as the only symbiont community requiring both parties to expand holobiont metabolism. Through their joint expansion of the biotin biosynthesis pathway, these symbionts may span missing gaps, creating a multi‐party mutualism within their nutrient‐limited, phloem‐feeding hosts. Recent, complementary gene inactivation, within the biotin pathways ofSerratiaandRickettsiella, raises further questions on the origins of mutualisms and host–symbiont interdependencies.

     
    more » « less
  5. ABSTRACT Microbial communities are shaped by interactions among their constituent members. Some Gram-negative bacteria employ type VI secretion systems (T6SSs) to inject protein toxins into neighboring cells. These interactions have been theorized to affect the composition of host-associated microbiomes, but the role of T6SSs in the evolution of gut communities is not well understood. We report the discovery of two T6SSs and numerous T6SS-associated Rhs toxins within the gut bacteria of honey bees and bumble bees. We sequenced the genomes of 28 strains of Snodgrassella alvi , a characteristic bee gut microbe, and found tremendous variability in their Rhs toxin complements: altogether, these strains appear to encode hundreds of unique toxins. Some toxins are shared with Gilliamella apicola , a coresident gut symbiont, implicating horizontal gene transfer as a source of toxin diversity in the bee gut. We use data from a transposon mutagenesis screen to identify toxins with antibacterial function in the bee gut and validate the function and specificity of a subset of these toxin and immunity genes in Escherichia coli . Using transcriptome sequencing, we demonstrate that S. alvi T6SSs and associated toxins are upregulated in the gut environment. We find that S. alvi Rhs loci have a conserved architecture, consistent with the C-terminal displacement model of toxin diversification, with Rhs toxins, toxin fragments, and cognate immunity genes that are expressed and confer strong fitness effects in vivo . Our findings of T6SS activity and Rhs toxin diversity suggest that T6SS-mediated competition may be an important driver of coevolution within the bee gut microbiota. IMPORTANCE The structure and composition of host-associated bacterial communities are of broad interest, because these communities affect host health. Bees have a simple, conserved gut microbiota, which provides an opportunity to explore interactions between species that have coevolved within their host over millions of years. This study examined the role of type VI secretion systems (T6SSs)—protein complexes used to deliver toxic proteins into bacterial competitors—within the bee gut microbiota. We identified two T6SSs and diverse T6SS-associated toxins in bacterial strains from bees. Expression of these genes is increased in bacteria in the bee gut, and toxin and immunity genes demonstrate antibacterial and protective functions, respectively, when expressed in Escherichia coli . Our results suggest that coevolution among bacterial species in the bee gut has favored toxin diversification and maintenance of T6SS machinery, and demonstrate the importance of antagonistic interactions within host-associated microbial communities. 
    more » « less