The creation, movement, and consumption of distinct biomolecules by marine organisms has far reaching implications regarding ecosystem material and energy flow and how we manage the marine environment. Lipids are ubiquitous, energy rich biomolecules that are essential for all life and are used for cell membrane structure, energy storage and serve as useful indicators for ecosystem and food web dynamics. In this dissertation, the flow of specific lipid biomolecules through multiple marine environments is measured, explored, and clarified to better understand biogeochemical cycles, marine food webs and ecosystem connectivity. In the first chapter of my dissertation, I measure, quantify, and close the loop of the open ocean microbial hydrocarbon cycle, with implications for priming effects of the ocean microbiome to oil spills. It is estimated that seeps, spills, and other oil pollution introduce ~ 1.3 million tons (1.3 Tg) of hydrocarbons into the ocean each year. Additionally, it is known that globally abundant marine cyanobacteria Prochlorococcus and Synechococcus which account for ~25% of ocean net primary production also produce hydrocarbons from fatty acids. But little is known about the size, turnover and fate of these cyanobacterial hydrocarbons and the implications for the ocean’s microbiome response to future oil spills. From a research expedition in the North Atlantic, I report that cyanobacteria in an oligotrophic gyre mainly produce n-pentadecane which correlates tightly with fluorescence and Prochlorococcus abundance in oligotrophic waters. Using chemical and isotopic tracing I find that pentadecane production and diel dynamics mainly occurs in the lower euphotic zone at the deep chlorophyll maximum. I estimate the global flux of cyanobacteria-produced pentadecane exceeds total oil input in the ocean by 100 to 500-fold, with cyanobacteria producing ~ 130-650 million tons of pentadecane per year. Analysis of sinking particles at the base of the euphotic zone show that nearly all pentadecane (< 0.001 % remaining) is consumed within the euphotic zone, suggesting near complete consumption of these hydrocarbons by hydrocarbon degrading microbes. These findings characterize a wide-spread microbial hydrocarbon cycle that selectively primes the ocean’s microbiome with long-chain alkanes. In the second chapter of my dissertation, I conduct a large-scale feeding experiment on a symbiotic reef-building coral (Stylophora pistillata) in the Red Sea to clarify fatty acid and isotopic biomarker patterns of coral heterotrophy for use in the field. Coral heterotrophy is an often-overlooked facet of coral nutrition that provides essential nutrients that help corals resist and recover from thermally induced bleaching that is degrading reef ecosystems around the world due to rising global ocean temperatures. Yet, methods for measuring coral mixotrophy, the balance between organic matter contributions to the coral host from autotrophic photo endosymbionts and heterotrophy on particles and plankton have typically been too coarse to elucidate source contributions. Through my experiment I show that fatty acids and isotopic biomarkers reliably separate experimental and reef nutritional source groups (heterotrophic or autotrophic). I show that heterotrophic fatty acid biomarkers are reliably recorded into coral host and symbiont tissues, with a divergent metabolic pattern of autotrophic biomarkers as feeding increases due to positive feedback of heterotrophy on the in hospite photo symbiont population. Additionally, I show that nitrogen and essential fatty acids are preferentially recorded into coral tissue while most heterotrophic carbon is respired or exuded as mucous; this shows that the use of bulk carbon isotopes as a feeding proxy for the last ~ 40 years is largely underestimating the contribution of heterotrophy to the trophic ecology of reef building corals. Overall, this finding underscores a connectivity between oceanic phyto- and zooplankton and reef-building coral. In the third chapter of my dissertation, I explore the mixotrophic differences of divergent bleaching responses of Acropora hyacinthus colonies on the forereef of Mo’orea during the 2019 mass bleaching event. During this bleaching event, all colonies of A. hyacinthus on the deep forereef (14 m) bleached and recovered, while colonies on the shallow forereef (5 m) near the reef crest resisted bleaching entirely, despite the same temperature stress. Using fatty acid and isotopic biomarkers I show through several lines of evidence that bleaching resistant colonies near the reef crest were likely consuming more particulate organic matter than deep forereef colonies. This conclusion is supported by isotopic feeding proxies, less isotopic niche overlap of the host and symbiont of resistant colonies, and larger proportions of putative POM fatty acid biomarkers in the host of resistant colonies relative to recovered colonies. This interpretation is in line with observations that benthic communities on the reef crest are a net sink of oceanic POM and that increased reliance on heterotrophy is associated with bleaching resistance. These data show the vital importance of reef environment, coral heterotrophy, and planktonic subsidies in structuring bleaching response of corals in a warming ocean and ultimately show that the reef crest may serve as a potent zone for reseeding coral populations after marine heat waves.