UC Davis

Lipids are a fascinating but under-utilized molecular tool - they are taxonomically specific, can be used to reconstruct environmental conditions, and once their functional groups are removed, they are stable over geologic timescales. Lipids are a diverse class of hydrophobic biomolecules, commonly called fats, that have many cell functions including: the bulk of cell membranes, signaling molecules, and energy storage. Different organisms biosynthesize different lipids, these informative biomarkers allow lipids to serve as proxies for which organisms were present in addition to broader environmental conditions. Chemotaxonomy is the study of unique lipids that have very constrained taxonomic sources, for example 2Me-hopanoids are only produced by methanogenic bacteria. Of the many different types of lipids, this thesis focuses primarily on two classes: sterols and fatty acids (FAs). Sterols, such as cholesterol, are a major group of lipids that modulate cell membrane permeability, in addition to providing the building blocks for more complex molecules like hormones and bile acids. FAs are a common lipid class that make up the majority of the phospholipid bilayer in cell membranes, in addition to larger molecules for energy storage. By coordinating lipid biomarker research with bioinformatics and field experiments, we can make robust proxies that can be used for pressing ecological questions, with geologic data providing crucial context. Studying the ecology of animals often requires direct observations of their diet or signs of their presence, but lipids provide an indirect method to study these interactions. This thesis is founded on two major concepts to disentangle many details of animal ecology using lipids: the ‘holobiont,’ and trophic transfer of lipids. The holobiont concept unifies a host animal and all of the microbiomes nested on and within it to a single meta-organism. This framework recognizes the independent metabolic importance of microbial symbionts - for example, a cow as a single organism cannot digest fiber from grass but the cow holobiont can, owing to their fermentation-adapted foregut microbiome. The metabolic capacity of holobionts impacts how they digest their lipids, and therefore the recovery of different lipids in stool or environmental samples can have implications for the animal’s functional ecology and conservation. The other significant pattern of lipid ecology is that animals partially take on a lipid signature reflecting their diet, or their prey’s diet, allowing researchers to estimate their trophic linkages using lipid tracers. For example, essential omega FAs are not synthesized by most animals but instead are primarily produced by plants and algaes and are highly retained trophically, with nearly a 1:1 transfer rate between prey and predators. The unique lipid metabolites found in animals can provide novel proxy insights to presence (e.g. lipids extracted from sediments), taxonomic affinity, diets, and microbial symbionts. The three chapters in this thesis each explore a different aspect of lipid biomarker work. The first chapter focuses on a unique sterol metabolite found in a half-billion-year-old animal fossil and searches for the genes responsible for the conversion in living animal gut microbiomes. The second chapter continues working on the same compound but develops new applications for conservation biology and tests if diverse sterols can be used to predict gut fermentation strategies. The last chapter flips the approach to use animals to ask questions about the larger environment, by developing a novel technique to use bird fecal FAs to noninvasively monitor a vulnerable keystone species called seagrass.