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Other research product . 2022

Delineating the evolutionary and ecological controls on coral reef fish gut microbiomes

Degregori, Samuel;
Open Access
Published: 01 Jan 2022
Publisher: eScholarship, University of California
Country: United States

Gut microbes provide vital functions for animal hosts. While it is known that host ecology and evolutionary history play a role in shaping gut microbiomes, a majority of studies have focused on mammal hosts. Other vertebrates, including fish, have received little attention. Coral reef fish, in particular, exhibit a wide range of distinct feeding behaviors, evolutionary histories, and geographic distributions that likely correlate with gut microbiome composition and diversity. They also inhabit a fragile ecosystem that is highly sensitive to anthropogenic disturbance—disturbances that are known to impact coral microbiomes but may or may not affect fish gut microbiomes. My thesis leverages a large unprecedented coral reef fish gut microbiome dataset (N=550), where I sampled the gut microbiomes of 20 host species of fish with robust replication spanning three islands across the South Pacific, to better understand how host phylogeny, host diet, and host environment shape vertebrate gut microbiomes. Comparing the gut microbiomes of distantly related hosts can reveal evolutionary and ecological dynamics that govern gut microbiomes across the animal kingdom. Chapter 1 investigates the possible similarities between coral reef fish and mammal gut microbiomes to elucidate any microbial features that may have converged between the two distantly related hosts. Through multivariate and Bayesian analyses, I show that fish and mammal gut microbiomes exhibit striking similarities in composition, particularly within carnivores and herbivores. Specifically, carnivores and herbivore gut microbiomes show more similarities within their diet groups than within their host phylogenies, and share a significant number of ASVs. Herbivore fish and mammal gut microbiomes, in particular, share a significant number of amplicon sequence variants (ASVs) associated with the functional requirements of herbivory, such as Ruminococcus and Treponema. My results indicate that despite 365 million years of evolution and two drastically distinct habitats (terrestrial vs. marine), fish and mammal gut microbiomes have converged on the basis of diet. Expanding on Chapter 1, Chapter 2 moves beyond host phylogeny and diet and aims to isolate and analyze the effects of host habitat on gut microbiome composition and diversity. Previous work on environmental effects acting on animal gut microbiomes largely focused on captive hosts or wild hosts of a single species, potentially ignoring any interactions between host environment and host phylogeny in the wild. Here, I leverage my dataset of coral reef fish gut microbiomes from a diverse range of hosts from three geographically distinct habitats to better understand how host habitat shapes vertebrate gut microbiomes. I find that host habitat significantly shapes fish gut microbiome composition and diversity and these effects are highly dependent on host phylogeny. For example, within the same analyses, a fish such as R. aculeatus, had significantly different gut microbiomes between the three islands, whereas E. merra gut microbiomes were largely unaffected by island location. For the fish gut microbiomes that were significantly impacted by host habitat, many of the associated ASVs were ASVs found in Chapter 1, suggesting that host habitat may also shape gut microbiome function. While comparative approaches on wild hosts are crucial in elucidating generalizable rules that govern animal gut microbiomes, experimental approaches are also imperative to unpack the finer-scale qualities and mechanisms of these rules. Chapter 3 builds on Chapter 2 by leveraging a simulated nutrient enrichment experimental design to further investigate the effects of host environment on gut microbiome composition and diversity. Nutrient enrichment is one of the most threatening consequences of anthropogenic stress on coral reef ecosystems, and the effects of nutrient enrichment on reef fauna gut microbiomes are largely unknown. Here, I artificially enrich the territories (N=40) of a highly abundant, territorial gardening fish, Stegastes nigricans, and use multivariate and differential abundance analyses to elucidate how nutrient enrichment impacts animal gut microbiome composition and diversity. I find that nutrient enrichment effectively “enriches” the gut microbiome, with S. nigricans gut microbiomes in enriched territories exhibiting significantly higher alpha diversities than those in control territories. I also find that these changes are specific to the hindgut and do not occur in the microbiomes of the food source that S. nigricans gardens.


Molecular biology, 16S, convergence, coral reef, evolution, fish, gut microbiome

Related Organizations
Related to Research communities
European Marine Science