Extracellular polymeric substances drive Curvibacter host adaptation and cospeciation with Hydra

The interactions between hosts and their microbial symbionts play a crucial role to host physiology. Bacteria can adapt to specific host environments over evolutionary timescales, leading to cospeciation and the formation of specialized host-microbe relationships. Understanding the molecular mechanisms underlying these adaptations provides key insights into the evolution of symbiosis and the stability of microbial communities. This study investigates the cospeciation and molecular adaptations of Curvibacter to its host Hydra, a well-established model for the study of host-microbe interactions. We provide strong evidence of cospeciation, as demonstrated by phylogenetic congruence between different Hydra species and their corresponding Curvibacter symbionts, along with preferential recolonization of germ-free Hydra by their native Curvibacter strains. Comparative genomic analyses reveal that host-associated Curvibacter strains exhibit distinct metabolic and biosynthetic adaptations compared to their free-living relatives. Specifically, the enrichment of proteins linked to host glycan interactions, extracellular polymeric substances (EPS), DNA metabolic processes, ABC transport, sugar metabolism, and bacterial chemotaxis highlights specialized adaptations of Curvibacter symbionts within the Hydra glycocalyx. Importantly, some of these signatures are only detectable within the Hydra vulgaris-associated Curvibacter subgroup, emphasizing the need to examine host-specific adaptations at a finer taxonomic resolution. Functional experiments identify a symbiont-specific EPS operon as a factor for host colonization, thereby establishing its role in facilitating symbiont specificity and stability. These findings provide insights into the molecular mechanisms driving host-microbe coevolution and highlight the evolutionary forces shaping microbial specialization within host-symbiont relationships.