Cross-scale eco-evolutionary dynamics of bacterial symbionts associated with lucinid bivalves in response to environmental change

Bacterial symbionts can extend the phenotype of their animal hosts, providing access to new resources and enabling colonization of habitats that would otherwise be out of reach. These partnerships may become especially important as environments change due to shifts in climate conditions or nutrient regimes. Since bacterial symbionts can respond more quickly than their animal hosts due to their capacity for rapid genomic change and highly responsive metabolic regulation, they will likely play a central role in mediating animal responses to such changes. Therefore, understanding how symbionts respond to environmental changes is essential for predicting the resilience of animal-microbe associations.
This thesis focuses on the obligate nutritional symbiosis between bivalves of the family Lucinidae J. Fleming, 1828 (lucinids), and sulfide-oxidizing Gammaproteobacteria. The ancient origin of this family, its survival through multiple mass extinctions, and its present-day success in diverse marine habitats highlight the central role of its chemosynthetic symbionts in its ecological and evolutionary resilience. Lucinids most commonly associate with symbionts of the genus Candidatus Thiodiazotropha, which are acquired from environmental populations. Recent studies have revealed considerable metabolic and taxonomic diversity within this genus. However, the role of lucinid symbionts in responding to environmental change, as well as the ecological and evolutionary mechanisms that generate, maintain, and shape this diversity, remain poorly understood. To address these gaps, I investigated lucinid symbionts under environmental variability operating across geological and seasonal timescales, and examined within-species diversity to gain a better understanding of their genomic plasticity.
The closure of the Isthmus of Panama was leveraged as a natural experiment that allowed the comparison of symbionts from lucinid sister species in the nutrient-poor Caribbean Sea and the nutrient-rich Tropical Eastern Pacific (TEP) (Chapter 2). I found that nitrogen fixation genes were consistently present in Caribbean symbionts, but absent in their TEP relatives, and phylogenetic analyses suggest that these genes were acquired multiple times via horizontal gene transfer. In this chapter, I proposed that nitrogen limitation has repeatedly driven the acquisition of new metabolic traits, enabling symbionts to persist in oligotrophic conditions and shaping the diversification of certain clades.
I zoomed in on the response to short-term environmental variability caused by seasonal upwelling in the TEP by analyzing symbiont community composition and transcriptional responses before and during an upwelling event (Chapter 3). While community composition remained stable, both dominant symbiont clades responded by upregulating methanol oxidation genes during non-upwelling periods and sulfide oxidation genes during upwelling. Based on these findings, I hypothesized that the ability of the symbionts to adjust their energy metabolism facilitates the acclimatization of the symbiosis to changes in sediment biogeochemistry and resource availability driven by the upwelling.
Finally, I examined the mechanisms that generate genome plasticity in lucinid symbionts (Chapter 4) by comparing within-species diversity and its potential genomic drivers in two co-occurring Caribbean species: the globally distributed Ca. T. endolucinida and the geographically restricted Ca. T. fergusoni. The former exhibited greater pangenome variability, more mobile genetic elements, and weaker purifying selection than the latter. These are signatures of higher genomic plasticity, but also of ongoing genome erosion, which could be indicative of increasing host dependence.
Together, these findings exemplify different mechanisms by which lucinid symbionts respond to environmental change. I argue that their implications extend beyond lucinids to offer insights into general principles of microbiome-mediated acclimatization and adaptation, in which microbial genomic and physiological plasticity play central roles. In Chapter 5, I discuss how these strategies may benefit the host directly or indirectly and how they may interact with host flexibility in physiology, ecology, and partner choice to buffer the impacts of change on the symbiosis. Finally, I emphasize key knowledge gaps, such as the ecology of free-living symbionts, and place the findings of this thesis within the broader context of human-driven ocean change.