Climate warming enhances aerobic methane emissions from invasive Raphidiopsis raciborskii blooms

Freshwater ecosystems contribute approximately half of global methane emissions; phytoplankton-mediated aerobic methane production is a key process resolving the "methane paradox" in oxic surface waters. However, the role of invasive cyanobacteria in aerobic methane production and its regulation by temperature remain poorly understood. Here, we combined 7‑month in situ field monitoring in a subtropical drinking water reservoir, controlled laboratory incubations, and transcriptomic sequencing to elucidate the mechanisms linking blooms of the invasive cyanobacterium Raphidiopsis raciborskii to freshwater methane release under climate warming. Field monitoring revealed unimodal temporal patterns for both surface R. raciborskii abundance and methane flux, with peaks co-occurring in August; surface methane flux was significantly positively correlated with R. raciborskii cell density (p < 0.001). Linear mixed-effects models identified water temperature, dissolved oxygen and electrical conductivity as key environmental drivers of methane emissions, while water temperature and total phosphorus predominantly regulate R. raciborskii growth. Incubation experiments confirmed 25 °C as the optimal temperature for R. raciborskii growth with methylphosphonate as the sole phosphorus source, whereas 30 °C maximized methane release. Transcriptomic analysis showed that warming upregulated methylphosphonate-degrading gene clusters and synergistically enhanced the expression of genes related to carbon fixation, methyl donor generation, nitrogen fixation and iron uptake, thereby boosting the aerobic methane production capacity of R. raciborskii. Our findings demonstrate that R. raciborskii is a key biogenic source of aerobic methane in freshwaters, with temperature as a key regulator, providing a scientific basis for assessing the ecological risks of R. raciborskii invasion and for managing cyanobacterial blooms and aquatic methane emissions.