THE EVOLUTIONARY GENOMICS OF MOBILE GENETIC ELEMENTS INVOLVED IN HOST-MICROBE COOPERATION
Creators: name: Montoya, Angeliqua P
Publisher: name: Washington State University
Year: 2024
Subjects: subject: Host-microbe
subject: Mobile genetic elements
subject: mutualism
subject: symbiosis island
subject: Genomics
subject: Symbiosis
subject: Genetics
subject: FOS: Biological sciences

description: Mobile genetic elements (MGEs) are fundamentally important to microbial innovation and evolution. MGEs may provide a fitness advantage to microbial host genomes if they harbor adaptive genes that confer environmental adaptation or symbiotic association with hosts. Beneficial symbiotic microbes have a critical role in plant and animal health. However, much of our understanding of the genetics of host-microbe interactions concerns pathogenicity, such as antibiotic resistance genes carried on MGEs. While understanding pathogen genetics allows scientists to mitigate harm from disease, much less is known about the evolutionary genetics of host-microbe cooperation despite the great potential to improve host health by enhancing microbial cooperation. My dissertation uses the model symbiosis between leguminous plants and beneficial nitrogen-fixing rhizobium bacteria to investigate the evolutionary genomics of MGEs that underly cooperation and environmental adaptation in the bacterial symbiont. The legume-rhizobium holobiont—comprising the host, its symbionts, and mobile genetic elements—can evolve as selection and fitness alignments shift. This dissertation contributes to filling knowledge gaps at multiple levels of the holobiont. The first level I examine is interactions between the host and multiple symbionts. Hosts can discriminate among symbionts that differ in the benefits they confer, to preferentially interact with the most beneficial symbionts. The first chapter investigates how the presence of multiple symbionts in the social environment impacts host plant discrimination mechanisms and consequently, rhizobium fitness. We reveal that host discrimination mechanisms are absolute and conditional, such that their impact on rhizobium fitness depends on a focal strain’s own genotype as well as the genotype of other conspecifics in the social environment, respectively. The next level I explore is among genomic compartments in the symbiont. The second chapter investigates how environmental variation and horizontal gene transfer have shaped the evolutionary history of genomic compartments within Mesorhizobium rhizobia bacteria. I examined the core chromosome and two ecologically important MGEs in a wild population of Mesorhizobium, 1) a nickel resistance island (NRI), which enables adaptation to nickel-enriched serpentine soils, and 2) a symbiosis island (SI), which enables symbiosis with host plants. The imperfect pattern of phylogenetic congruence found among MGEs and the host cell’s chromosome is connected to the adaptive significance of the MGEs across variable environments. Cophylogenetic patterns are consistent with selection for co-adapted genomic compartments via vertical co-inheritance for both MGEs, and/or MGE transmission primarily among close relatives, particularly for the SI, as well as NRI loss as strains migrate across soil environments. The third level I examine is the interactions among symbiotic rhizobia, co-occurring commensal strains, and the SI. In this final chapter, I investigate how heritable variation in rates of transfer, acquisition, and function of the SI is distributed among donor and recipient lineages. SI+ donors that contain the SI were mated with SI- recipients that lack the SI, transmission frequency was quantified, and the functional consequences of SI acquisition were measured in symbiosis with host plants. This investigation revealed heritable variation in SI transmission and function, such that the ability to act as an MGE donor or recipient, and the ability to benefit from an MGE can differ among strains and contribute to the evolvability of a lineage. Taken together, the dissertation contributes novel insights on how interactions among host and symbionts, symbionts in the social environment, and genomic compartments in the symbiont host cell, as well as heritable variation in MGE transmission and function, will contribute to the evolutionary dynamics of the legume-rhizobium holobiont.