Site effects on wildlife enteric bacterial diversity: you are where you eat?

The study of microbial biogeography has made vast strides in recent years due, in part, to advances in the technological capacity to document microscopic biodiversity at the community, population and genomic levels. In this dissertation, we apply a combination of molecular and cultivation approaches to the study of enteric microbial diversity in a unique system of sister iguanid species, the Galápagos land and marine iguanas (Conolophus spp. and Amblyrhynchus subcristatus, respectively). We explored the spatial diversity of enteric bacteria in these two species at multiple levels, from communities to genetic traits. The unique host population history and geography of this island chain informed hypotheses about expected biogeographical patterns and the underlying processes that shape microbial diversity in this system. In Chapter 1, we reviewed current understanding of microbial biogeography and explored how incorporation of such ecological theory might benefit understanding of enteric microbial community structure and function across space and time. Chapter 2 explored the spatial community diversity of marine and land iguana enteric communities using a molecular approach based on 454 pyrosequencing. Firstly, we demonstrated that while host species was the strongest force shaping these communities, within a host species, geographical proximity also determined overlap in community composition at the genus level. In addition, we found that the degree of contact among host species can produce distinct local effects in community richness and composition, especially when host species have amplified opportunities for microbial exchange such as higher population densities or limited habitat area. Next in Chapter 3, we explored taxonomically finer-scale diversity patterns among marine iguana populations for the rich enteric genus Clostridium. In contrast to the expectation that each host population should have relatively distinct Clostridium communities, we found a surprising amount of phylogenetic conservation across all sites, despite also demonstrating evidence suggesting on-going taxonomic turnover – forces which might otherwise lead to rapid divergence of enteric communities in allopatric host populations. We then applied a more traditional cultivation and molecular genetic approach in Chapter 4 in order to document Salmonella enterica strain diversity among sites. We serotyped and genotyped Salmonella enterica isolates carried by land and marine iguanas across a geographical gradient and found nearly complete isolation among strain pools. However, we also found suggestions of geographically-dependent genomic similarity among sites, possibly due to long-distance transport of genetic elements by oceanic currents. Finally, in Chapter 5 we explored genetic trait biogeography in this system by documenting phenotypic and genetic patterns of antibiotic resistance. We found that sites farther from high densities of humans (i.e. major port towns) harbored fewer resistant bacteria. We also noted that these antibiotic resistance traits may not be retained within the broader endemic bacterial community of Galápagos wildlife for any appreciable length of time, as Salmonella enteric isolates did not share resistance traits found in Escherichia coli within the same site or even within the same individual fecal sample. Through this work as a whole we demonstrated that, within the context of a single study system, biogeographical patterns and mechanisms can vary widely across bacterial taxonomic levels, with both ecological and evolutionary forces acting in concert on enteric biodiversity. Increased understanding of the interplay among these forces for shaping microbial community form and function across taxonomic scales has potential to improve not only theoretical understanding of microbial ecology but also to advance management of pressing issues such as novel disease emergence or antibiotic resistance dissemination