Ecology and evolution of Prochlorococcus from oxygen-deficient zones

Abstract

Prochlorococcus—the most abundant photosynthetic organism in the global ocean—is central to carbon cycling and a key model for linking microbial diversity to ecological function. Yet the functional traits and ecological roles of its most deeply branching lineages, which inhabit the low-light, blue-shifted, nutrient-rich waters within the upper regions of oxygen-deficient zones (ODZs), remain largely uncharacterized. In this thesis, I integrated metabolomics, metatranscriptomics, comparative genomics, and cultivation-based physiology to characterize both the chemical landscape of ODZs and the traits of the deeply branching Prochlorococcus populations that inhabit them. I first showed that these Prochlorococcus lineages retain ancestral glycine betaine (GBT) synthesis, and that this labile metabolite forms a major organic currency linking primary production to SAR11 demethylation in the ODZ. I then isolated the first representatives of the Prochlorococcus clade AMZ II from ODZs and demonstrated that they retain complete phycobilisomes while synthesizing divinyl chlorophyll b, revealing a transitional light-harvesting state that bridges canonical Prochlorococcus and Synechococcus architectures. Next, I characterized their photophysiology, showing broad irradiance tolerance and strong blue-light specialization consistent with life at ODZ boundaries. Together, these findings clarify the metabolism, light-harvesting strategies, and environmental specialization of ancient Prochlorococcus lineages at the edges of the ocean’s least-oxygenated waters.