EXAMINING THE ROLE OF HOST DEPENDENCE ON THE ECOLOGY AND EVOLUTION OF EPULOSCIUM SPP. AND THEIR RELATIVES

Abstract

Studies of the gut microbiome have enlightened our perspective on the contributions of microbes to animal health. Commensal bacteria have evolved strategies to maintain associations with their host and gain a foothold in this competitive environment through colonization, maintenance and transmission. Here I studied how dominant commensals of herbivorous surgeonfish have evolved strategies to overcome the obstacles to host association and as a result of this interaction, further explain the unusual biology of these commensals. Epulopiscium spp. and relatives (known as epulos) are morphologically diverse and form a monophyletic clade within the Lachnospiraceae XIVb cluster (Order: Clostridiales). They are renowned for their large size, some reaching lengths up to 0.6 mm, and their extreme polyploidy, containing 100,000s of copies of a ~3.2 Mb genome. The reproductive cycle of epulos follows a predictable diurnal pattern. Establishing a single-cell sequencing technique, I explored questions that were once unattainable for this uncultured bacterium. First, I conducted a population analysis of the mutually exclusive interaction between Epulopiscium sp. type B and Naso tonganus in the Great Barrier Reef. I found evidence of allopatric speciation, governed by host migratory preferences between reef and island habitats. Maintaining genomic diversity for the symbiont depends on horizontal transmission by the host and rampant recombination to overcome genome purification in this polyploid bacteria. Next, I explored the distribution and diversity of co-resident symbiont populations across three Acanthurus species. Genomic insights into their metabolic potential confirmed that the two cohabitating epulos convert ammonia/urea to amino acids. However, differences among these epulo lineages for the ability to degrade dietary complex polysaccharides and diverse strategies for conserving energy suggest niche differentiation in this competitive environment. Lastly, by examining the transcriptomic profiles of an endospore-forming epulo in Naso unicornis, I have shown that the metabolic and reproductive life cycle of this epulo population is synchronized with the feeding/fasting cycles of the host. In conclusion, I suggest that the evolution of epulos is largely influenced by their dependency on surgeonfish hosts. A possible reason for successful transmission and maintenance of epulos in herbivorous surgeonfish worldwide is their ability to anticipate the circadian cycles of their host.