The evolutionary responses of resurrected Baltic Sea cyanobacteria in a warming world

Abstract

What makes cyanobacteria such formidable winners of climate change? In many aquatic systems, cyanobacteria often outperform their eukaryotic counterparts because they tolerate environmental conditions that constrain growth in other phytoplankton groups. Owing at least in part to their important roles in the nitrogen and carbon cycle, cyanobacteria and their physiological responses to environmental drivers are fairly well studied. However, short-term responses cannot always directly predict long-term responses, but we need to know the latter in order to say with more certainty whether and why cyanobacteria are indeed going to be the winners of a warming planet. This dissertation investigates the eco-evolutionary responses of re-germinated bloom-forming cyanobacteria from different sediment layers (each layer representing different times, from pre-industrial times to the late 1990s) in response to increasing temperature using molecular (whole genome sequencing, methylation assays) and trait-based approaches (thermal performance curves, carbon use efficiency, organic carbon utilisation, biotic interaction assays). The comparative whole genome analysis of historic and recent lineages of Nodularia spumigena tests to what extent cyanobacteria have already evolved in an environment that has seen, among other changes, 2°C of warming over the past 170 years. We find that past evolution in Nodularia spumigena does not follow the "hotter is broader and better" prediction: pre-industrial (1824) lineages had the highest thermal optima but the lowest growth rates at prevailing summer temperatures, while contemporary (1996) lineages had lower thermal optima but higher growth rates at prevailing Baltic Sea summer temperatures, reduced allelopathic capacity, and broader organic carbon substrate use. These patterns are consistent with adaptation to increased thermal variability rather than directional warming alone. Carbon use efficiency was broadly conserved across sediment ages and temperatures, though the contemporary lineage showed the greatest capacity for CUE improvement under experimental warming. Experimental evolution over ~100 generations revealed that all cohorts can reach a similar post-selection Topt, though the magnitude of shift required differs substantially across sediment ages, while the capacity for metabolic efficiency evolution is historically contingent and restricted to lineages with more recent evolutionary histories. Global DNA methylation is historically structured and co-varies with evolutionary shifts in thermal performance, establishing epigenetic state as a dynamically regulated molecular layer accompanying thermal adaptation. Together, these results indicate that N. spumigena has undergone substantial multi-trait evolutionary reorganisation over the past two centuries, and retains rapid adaptive potential under continued warming, but that the specific traits through which evolution is expressed depend on prior evolutionary history.