Metabolic drivers of community dynamics in marine microorganisms

Abstract

Marine microorganisms adopt metabolic strategies, the biochemical means by which they acquire energy and nutrients, in part, because of the interactions between biological entities in their community. The eco-evolutionary strategies adopted by marine microbes both shape and are shaped by the environments in which they can live and remain competitive, the flow of carbon and nutrients through the environment, and the structure of the marine ecosystem. While many theories exist to explain the metabolic underpinnings of plankton ecology, there remains significant gaps in our understanding of how organisms fill metabolic niches and the mechanisms underlying these dynamics. This work focuses on three biotic relationships (parasitism, predation, and competition) and how these community dynamics both shape and are shaped by organismal metabolism using planktonic laboratory systems. To test the effects of parasitism and predation, we compared the cosmopolitan marine cyanobacteria Prochlorococcus MED4 lipidome under ideal conditions to its lipidome modulated due to top-down pressures from P-SSP7, a T7-like phage, and Paraphysomonas bandaiensis, a phagotrophic nanoflagellete predator. From cultures containing only Prochlorococcus MED4, we assemble the first complete lipidome of the abundant marine cyanobacteria Prochlorococcus MED4. Using this core lipidome as a baseline, we identify several characteristic ways phage infection alters the fatty acid, phospholipid, and other lipid metabolic pathways in Prochlorococcus. We also describe an unknown mechanism by which the energy storage metabolism of Paraphysomonas bandaiensis is affected by grazing on P-SSP7 infected prey. Next, to test how competitive dynamics shape metabolic niche partitioning, we assemble a novel model system using multiple strains of the marine mixotroph Ochromonas, with differing metabolic requirements. These mixotrophs were grown in competition with Paraphysomonas bandaiensis in batch and chemostatic culture. Generally, mixotrophic metabolism is assumed to confer a competitive advantage through the acquisition of energy and nutrients from multiple pools and the ability to relieve competitive pressures by switching trophic investments away from limiting pathways. Despite this, both obligately phagotrophic strains of Ochromonas tested instead ‘doubled-down’ on phagotrophy in response to competition with Paraphysomonas bandaiensis. Whereas the facultatively phagotrophic strain used in this study, Ochromonas 1391, followed typical mixotrophic competitive behavior of increased investment in phototrophy. These strains also experienced significant growth and energy efficiency tradeoffs because of this investment. We find evidence that this tradeoff may be due to prey nutrition needs or prey quotas in these organisms.

Additionally, we show how metabolic landscapes, i.e. multidimensional conceptualizations of metabolism, can inform metabolic tradeoffs and realized metabolic niches in response to community dynamics. Our results underscore the powerful effects of community interactions and metabolism, and vice versa. The dynamics captured within this dissertation research, inform microbial metabolic niches and how energy and nutrients flow through mixed planktonic communities with complex biotic interactions.