Insights into the Shark 'Holobiont' through the Skin Microbiome and Host Genetics

摘要

Eukaryotic organisms are covered by a collection of microbial organisms, termed the microbiome. Emergent properties of the microbiome are associated with the health of their host and fluctuates with changes to microbiome community diversity. Understanding processes of microbiome diversity is a critical question for insight into the health of host organisms. Historically, microbiome insight was gained through limited procedure which provide an incomplete assessment. For example, culture-based microbial assays provide insight into the < 1 % of microbial organism which can be cultured, and gene marker surveys reveal only the taxonomic composition of the microbiome. The microbiome is however dynamic, being influenced by ecology and evolutionary processes at the genetic level, therefore characterizing all the genes across all the microbes in an environment is required to describe the microbiome. Advances in high through-put DNA sequencing technology have enabled this insight in the form of random shotgun metagenomics.;My thesis provides insight into the microbiome composition through space and time and determine the ecological factors which are acting to structure the microbial community. With the novelty of microbiome research to date, macroecological community concepts have only been tested within the context of host associated microbiomes for disparate host organisms, such as mammals. For my dissertation work, I have investigated baseline microbiome diversity associated with the skin surface of three shark species. The primary aim was to test whether processes described through macroecological theory are apparent in the microbiome composition. For chapter 1, I asked a basic, yet fundament question of whether the microbiome composition exhibited neutral based community dynamics. With chapter 2, I examine the skin microbiome composition across a major evolutionary divergence, comparing microbiome composition among elasmobranchs (cartilaginous fishes), and teleost fishes (ray-finned fishes) to determine if processes of selectivity in the skin microbiome are concordant with host evolutionary trajectory. For chapter 3, I introduce a framework for examining host mitochondrial DNA which can be used to identify host evolutionary principles regulating the microbiome (Chapter 2), by characterizing the mitogenome of the common thresher shark (Alopias vulpinus). Overall, this work advances the understanding for microbiome community dynamics in context of existing ecological community framework for community assemblages. In addition, this work introduces skin microbiome dynamics in a unique corner of vertebrate evolutionary history and discusses host factors which may lead to varying microbiome patterns on an ancient vertebrate group.;Chapter 1: I first tested whether the skin microbiome of the common thresher shark (Alopias vulpinus) exhibited host specificity. The microbiome composition of the thresher shark was compared to an algal host species and the water column microbiome. I chose the algal host microbiome as a comparison to determine whether thresher shark microbiome adhered to the Lottery mechanism of community assemblage, which was first described in context of the microbiome from the algal host. The Lottery mechanisms of community assemblage posits that several species have similar functional roles (i.e. functional redundancy) and can occupy the same niche. Therefore, taxonomic composition can be random within a community while the functional composition is specific. I found that the shark microbiome was fundamentally different than the algal host and water column microbiome. Genera distinguishing the A. vulpinus microbiome from the water column included, Pseudoalteromonas (12.8 % +/- 4.7 of sequences), Erythrobacter (5. 3 % +/- 0.5) and Idiomarina (4.2 % +/- 1.2) and distinguishing gene pathways included, cobalt, zinc and cadmium resistance (2.2 % +/- 0.1); iron acquisition (1.2 % +/- 0.1) and ton/tol transport (1.3 % +/- 0.08). Taxonomic community overlap (100--dissimilarity index) was greater in the skin microbiome (77.6), relative to the water column microbiome (70.6) and the algal host-associated microbiome (algae: 71.5). I demonstrate that the unannotated sequences of the shark skin microbiome are more similar at a base-pair level (i.e. greater sequence turn-over) relative to both the algal and water column microbiomes. Overall, these results suggest the shark skin microbiome exhibits greater selectivity than the algal or water column microbiome.;Chapter 2: In Chapter 1, I demonstrated for the first time that shark skin is a selective surface, relative to an algal and water column microbiome and is influenced by different community structure principles. For chapter 2, I test the microbiome structure across a major evolutionary divergence within vertebrates, elasmobranchs and teleost fishes. The observation that host microbiomes are generally species specific has led naturally to the null hypothesis that the host microbiome evolves with the host and this called phylosymbiosis. The theory posits that host evolutionary trajectory influences microbiome composition, thus the microbiome of two closely related species is more similar than the microbiome of two distantly related species. (Abstract shortened by ProQuest.).