Dynamic nutrient competition (de-)stabilizes photosymbiosis

Abstract

ABSTRACT Photosymbioses between heterotrophic hosts and phototrophic symbionts are critical to productivity in oligotrophic aquatic ecosystems. The ecological success of this relationship is rooted in the efficient metabolic exchange between symbiotic partners, yet this nutritional dependency may render these systems highly sensitive to anthropogenic changes. Recent studies suggest that competitive partitioning of nutrients between partners is critical for the maintenance and regulation of symbiotic interactions. However, a solid theoretical foundation for the nutritional regulation of photosymbioses is still lacking. Thus, we designed a mechanistic population model to investigate whether observed ecological dynamics of photosymbioses can be explained by competition for the same limiting nutrient within the holobiont. Our model gives rise to a bistable system where a disturbance in nutrient competition can shift the symbiosis from a “symbiotic” state of efficient carbon recycling between the two partners into a “dysbiotic” state where no photosynthates are allocated to the host. We show that environmental factors such as temperature and nutrient availability, as well as symbiont traits such as nutrient-assimilation rates, may affect the sensitivity of the system to such disturbances. Critically, this nutritional regulation results in a trade-off in which the traits that enhance the fitness of symbiotic partners under stable conditions also enhance their susceptibility to environmental change. The model results reveal that nutrient competition is sufficient to explain ecological dynamics of establishment and initial breakdown of the symbiosis, and provide key insights into an evolutionary trajectory that favors productivity over heat resistance. IMPORTANCE Photosymbiosis, the partnership between heterotrophic hosts and phototrophic symbionts, is a cornerstone of evolutionary innovation that sustains biodiversity from tropical coral reefs to temperate lakes. Despite their evolutionary success, these associations are surprisingly susceptible to anthropogenic change. By developing a universal population growth model, we demonstrate that the very metabolic interactions that sustain their immense productivity also create an inherent sensitivity to anthropogenic stress. We show that the competition for essential nutrients within the partnership makes the most productive symbioses the most vulnerable to breakdown. This work provides a mechanistic framework to predict how global change threatens the stability of these vital ecological cornerstones, offering a new lens through which to understand and mitigate symbiotic collapse.