Modeling bacteria-enhanced thermal tolerance in marine phytoplankton

Background/Question/Methods

: Marine phytoplankton account for 50% of global primary productivity, regulate nutrient cycles, and form the base of the oceanic food web. Warming ocean temperatures due to climate change will affect their growth and range but typical predictive models do not consider interspecies interactions. Recent studies on freshwater species have shown that cross-feeding between phytoplankton and bacteria in their microbiome influences phytoplankton thermal tolerance. Phytoplankton supplies photosynthate to bacteria, receiving cobalamin (vitamin B12) in return. Cobalamin allows phytoplankton to synthesize an essential amino acid, methionine, with a specific pathway (METH) that functions better at high temperatures than an alternate, cobalamin-independent pathway (METE). Few studies have investigated this mutualism in marine species. We investigate how cross-feeding affects the ecology and evolution of marine phytoplankton, especially their thermal tolerance and response to global warming. We developed an ODE model where the mutualists exchange the nutrients they synthesize (cobalamin and carbon) while also competing for nitrogen. We analyzed it using a quasi-equilibrium framework and conducted an evolutionary analysis, employing tools from adaptive dynamics and quantitative genetics. The model explores tradeoffs between allocating resources to growth VS. substrate synthesis, temperature effects on algal growth, conditions required for coexistence, and sensitivity of the mutualism to warming.

Results/Conclusions

: Focusing on the ecological interaction, we found that the mutualists could stably coexist in the presence of both pathways, with temperature affecting the equilibrium population value and nutrient limitation scenario. Bifurcation analysis for the fractional allocations revealed that the mutualist that invests more in growth has a higher equilibrium population. However, when we imposed a tradeoff between growth and substrate synthesis such that species were allowed to evolve their position along this tradeoff, we found that the stability of this ecological interaction collapsed. Our analyses suggest that this occurs because fractional allocation affects the minimum resource requirement (R*) of the mutualists. Invaders could achieve a positive invasion fitness by increasing their fractional allocation and lowering their R*, consequently breaking the cross-feeding relationship. This recapitulates classic puzzles in the theory of mutualisms over their evolutionary stability. We propose additional mechanisms that might stabilize this interaction from an eco-evolutionary perspective, including imposing spatial constraints, nutrient recycling, and accounting for nutrient concentrations within cells. This study provides a quantitative tool for understanding future algal blooms and carbon sequestration under climate change. Additionally, it expands fundamental understanding of how species interactions affect adaptation to thermal gradients.