Oligotrophic regions of the world ocean sustain vast phytoplankton populations despite extremely low nutrient levels. However, the mechanisms governing their coexistence, interdependence, and mortality are poorly understood. This dissertation investigates how evolutionary dependency, community feedback, and regulated cell death (RCD) jointly shape the stability of marine microbial communities using the Prochlorococcus/Parasynechococcus/Alteromonas model system.
In Chapter 1, I argue that the Black Queen (BQ) hypothesis—which posits that microbes lose costly metabolic functions supplied by community partners—provides a unifying framework for understanding phytoplankton ecology. This framework helps resolve longstanding puzzles, including the paradox of the plankton and the evolutionary maintenance of RCD in unicellular organisms. Building on this framework, Chapter 2 uses transcriptomic analysis of Alteromonas in co-culture with picocyanobacteria to demonstrate that community composition induces greater changes in gene expression than pCO₂ alone. Reduced 2-phosphoglycolate/glycolate exudation by Prochlorococcus under elevated pCO₂ may disrupt the helper heterotroph effect underlying this cyanobacterium’s BQ dependency.
Chapter 3 integrates co-culture experiments, RNA-seq, metabolomics, and mathematical modeling to demonstrate that the stable coexistence of Prochlorococcus and Parasynechococcus is maintained by an “Ouroboros network” of feedback loops. In this network, resource competition, carbon exudation, BQ dependency, and possibly RCD collectively stabilize the community across environmental gradients and during adaptation to changing conditions.
Chapter 4 resolves the cellular mechanisms underlying RCD in these cyanobacteria, showing that differences in cell death modes and the number of checkpoint-linked mortality events between taxa are associated with divergent life-history strategies. These findings suggest that carbon released at these checkpoints may shape interactions with helper Alteromonas, linking individual cell death to community-level interdependencies.
In conclusion, these findings converge on a new resolution to the paradox of the plankton: coexistence in resource-limited environments emerges from interdependent metabolic exchanges, feedback, and regulated cell death shaped by multilevel selection. I propose that together, these processes form an “altruistic bargain” in which stability arises from self-constraint rather than competition alone. Because these interactions are environmentally sensitive, climate change, including warming and acidification, may disrupt the dependencies that sustain microbial diversity and ecosystem function in the world ocean.
Malisano Barreto Filho M., 2026. Surviving together: Evolutionary dependency, community dynamics, and mortality in marine microbial communities. PhD thesis, University of Alabama, 408 p. Thesis.
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