Metabolite diversity amongProchlorococcusstrains belonging to divergent ecotypes

Primary AbstractThe euphotic zone of the surface ocean contains distinct physical-chemical regimes that vary inversely in light and nutrient concentrations as a function of depth. The most numerous phytoplankter of the mid- and low-latitude ocean is the picocyanobacteriumProchlorococcus,which consists of ecologically distinct subpopulations (i.e., “ecotypes”). Ecotypes have different temperature, light and nutrient optima and display distinct relative abundances along gradients of these niche dimensions. As a primary producer,Prochlorococcusfixes and releases organic carbon to neighboring microbes as part of the microbial loop. However, little is known about the specific moleculesProchlorococcusaccumulates and releases or how these processes vary among its ecotypes. Here we characterize metabolite diversity ofProchlorococcusby profiling three ecologically-distinct cultured strains: MIT9301, representing a high-light adapted ecotype dominating shallow tropical and sub-tropical waters, MIT0801, representing a low-light adapted ecotype found throughout the euphotic zone and MIT9313, representing a low-light adapted ecotype relatively most abundant at the base of the euphotic zone. In both intracellular and extracellular metabolite profiles, we observe striking differences across strains in the accumulation and release of molecules. Some differences reflect variable genome content across the strains, while others likely reflect variable regulation of genetically-conserved pathways. In the extracellular profiles, we identify molecules that may serve as currencies inProchlorococcus’interactions with neighboring microbes and therefore merit further investigation.ImportanceApproximately half of the annual carbon fixation on Earth occurs in the surface ocean through the photosynthetic activities of phytoplankton such as the ubiquitous picocyanobacteriumProchlorococcus.Ecologically-distinct subpopulations ofProchlorococcus(or ecotypes) are central conduits of organic substrates into the ocean microbiome, thus playing important roles in surface ocean production. By measuring the chemical profile of three cultured ecotype strains, we observed striking differences in the likely chemical impact ofProchlorococcussubpopulations on their surroundings. Subpopulations differ along gradients of temperature, light and nutrient concentrations, suggesting that these chemical differences could affect carbon cycling in different ocean strata and should be considered in models ofProchlorococcusphysiology and marine carbon dynamics.