Metabolomes are an emergent property of marine microbial systems

Abstract

Microbial communities underpin ocean biogeochemical cycles and form the basis of marine ecosystems. Microbes use and maintain pools of small, organic molecules called metabolites as the core intermediates and building blocks of their metabolisms and as currencies in the exchanges of nutrients, energy, and information. Microbes also use metabolites to adapt to environmental conditions such as osmotic pressure and oxidative stress. Metabolomics, or the measurement of all metabolites in a system (the metabolome), is a powerful tool for characterizing microbial systems in the marine environment. Metabolomics studies have revealed the role of taxonomy and physiochemical factors in controlling marine microbial metabolite pools. However, microbial ecosystems are also shaped by the myriad of biological and chemical interactions that occur among their component parts, leading to the emergence of new dynamics at the community level not predictable from studying a single organism. In this dissertation, I employ metabolomics to characterize the metabolite pools of marine microbial communities at an unprecedented scale and investigate the roles of a diverse suite of interactions in shaping metabolic processes. In Chapter 2, I developed a novel extraction approach for separating dissolved metabolites from seawater, enabling the first measurement of many dissolved compounds in marine samples. In Chapter 3, I used metabolomics and transcriptomics to characterize viral infection of the globally important cyanobacterium Prochlorococcus, revealing extensive metabolic remodeling and demonstrating the importance of viral infection in shaping marine metabolite dynamics. In Chapter 4, I used uptake experiments to quantify the cycling of two metabolites, glycine betaine and homarine, and show that the uptake rates and standing stocks of these compounds is dependent on the concentrations of other metabolites present in the system. Finally, in Chapter 5, I measured pools of osmolytes inside and outside of cells at the basin scale in the North and Equatorial Pacific Ocean and the Salish Sea. I found that the composition of osmolyte pools was largely conserved at the community level despite vast changes in microbial biomass, community composition, nutrient status, and productivity. Taken together, these projects demonstrate that the composition and fluxes of marine metabolite pools are an emergent property that stem from a wide range of interactions across scales in microbial ecosystems.