One year of warming leads to the total loss of productivity in a widespread photosymbiosis

ABSTRACT: Photosymbioses, in which photosynthetic microorganisms reside within heterotrophic hosts, are important components of aquatic ecosystems and are under threat from environmental warming. The immediate ecological consequences of acute warming for archetypal photosymbioses, such as those between corals and zooxanthellae, are well documented. In contrast, understanding of the evolutionary responses of photosymbioses to persistent warming remains limited and direct observations of evolution in response to warming are scarce, as many associations are slow-evolving and do not enable observations on a tractable timescale. To address this knowledge gap, we exposed the widespread microbial Paramecium bursaria-Chlorella spp. photosymbiosis to 295 d of continuous growth under +5°°C of persistent warming. We subsequently quantified the thermal responses of traits associated with symbiosis persistence and ecological function (growth rate, symbiont density [the number of symbionts within hosts], and metabolic rates) compared with cultures maintained at ambient temperature and cultures exposed to -5°°C of cooling for the same time period. Strikingly, while growth rate thermal optimum increased with warming, net photosynthesis and carbon-use efficiency (the proportion of photosynthetic carbon available for growth) both strongly declined to zero. These data suggest a significant change in ecological function with persistent warming. We also detected larger autonomous symbiont populations following 295 d of warming, and symbionts from the warm-adapted symbiosis demonstrated a ‘switch’ from exclusive growth on organic to inorganic nitrogen, suggesting that symbionts could have evolved increased autonomy from hosts. Thus, warming could erode the ecological function and promote symbiont autonomy in photosymbiosis over evolutionary timescales.