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The extent and ecological significance of intraspecific functional diversity within marine microbial populations is still poorly understood, and it remains unclear if such strain-level microdiversity will affect fitness and persistence in a rapidly changing ocean environment. In this study, we cultured 11 sympatric strains of the ubiquitous marine picocyanobacteriumSynechococcusisolated from a Narragansett Bay (RI) phytoplankton community thermal selection experiment. Thermal performance curves revealed selection at cool and warm temperatures had subdivided the initial population into thermotypes with pronounced differences in maximum growth temperatures. Curiously, the genomes of all 11 isolates were almost identical (average nucleotide identities of >99.99%, with >99% of the genome aligning) and no differences in gene content or single nucleotide variants were associated with either cool or warm temperature phenotypes. Despite a very high level of genomic similarity, sequenced epigenomes for two strains showed differences in methylation on genes associated with photosynthesis. These corresponded to measured differences in photophysiology, suggesting a potential pathway for future mechanistic research into thermal microdiversity. Our study demonstrates that present-day marine microbial populations can harbor cryptic but environmentally relevant thermotypes which may increase their resilience to future rising temperatures.

Average sea surface temperatures are expected to rise 4° this century, and marine phytoplankton and bacterial community composition, biogeochemical rates, and trophic interactions are all expected to change in a future warmer ocean. Thermal experiments typically use constant temperatures; however, weather and hydrography cause marine temperatures to fluctuate on diel cycles and over multiple days. We incubated natural communities of phytoplankton collected from California coastal waters during spring, summer, and fall under present-day and future mean temperatures, using thermal treatments that were either constant or fluctuated on a 48 h cycle. As assayed by marker-gene sequencing, the emergent microbial communities were consistent within each season, except when culture temperatures exceeded the highest temperature recorded in a 10-year local thermal dataset. When temperature treatments exceeded the 10-year maximum the phytoplankton community shifted, becoming dominated by diatom amplicon sequence variants (ASVs) not seen at lower temperatures. When mean temperatures were above the 10-year maximum, constant and fluctuating regimes each selected for different ASVs. These findings suggest coastal microbial communities are largely adapted to the current range of temperatures they experience. They also suggest a general hypothesis whereby multiyear upper temperature limits may represent thresholds, beyond which large community restructurings may occur. Now inevitable future temperature increases that exceed these environmental thresholds, even temporarily, may fundamentally reshape marine microbial communities and therefore the biogeochemical cycles that they mediate.