Shifts in dimethylated sulfur concentrations and microbiome composition in the red-tide causing dinoflagellate <i>Alexandrium minutum</i> during a simulated marine heatwave

Abstract

The biogenic sulfur compounds dimethyl sulfide (DMS), dimethyl sulfoniopropionate (DMSP) and dimethyl sulfoxide (DMSO) are produced and transformed by diverse populations of marine microorganisms and have substantial physiological, ecological and biogeochemical importance spanning organism to global scales. Understanding the production and transformation dynamics of these compounds under shifting environmental conditions is important for predicting their roles in a changing ocean. Here, we report the physiological and biochemical response of a robust strain of Alexandrium minutum, a dinoflagellate with the highest reported intracellular DMSP content, exposed to a 6 d increase in temperature mimicking mild and extreme coastal marine heatwave conditions (+4 and +12 ∘C). Under mild temperature increases (+4 ∘C), A. minutum growth was enhanced, with no measurable physiological stress response. However, under a very acute increase in temperature (+12 ∘C) triggering thermal stress, A. minutum growth declined, photosynthetic efficiency (FV∕FM) was impaired, and enhanced oxidative stress was observed. These physiological responses indicative of thermal stress were accompanied by increased DMS and DMSO concentrations followed by decreased DMSP concentration. At this temperature extreme, we observed a cascading stress response in A. minutum, which was initiated 6 h after the start of the experiment by a spike in DMS and DMSO concentrations and a rapid decrease in FV∕FM. This was followed by an increase in reactive oxygen species (ROS) and an abrupt decline in DMS and DMSO on day 2 of the experiment. A subsequent decrease in DMSP coupled with a decline in the growth rate of both A. minutum and its associated total bacterial assemblage coincided with a shift in the composition of the A. minutum microbiome. Specifically, an increase in the relative abundance of the operational taxonomic units (OTUs) matching Oceanicaulis (17.0 %), Phycisphaeraceae SM1A02 (8.8 %) and Balneola (4.9 %) as well as a decreased relative abundance of Maribacter (24.4 %), Marinoscillum (4.7 %) and Seohaeicola (2.7 %) were primarily responsible for differences in microbiome structure observed between temperature treatments. These shifts in microbiome structure are likely to have been driven by either the temperature itself, the changing physiological state of A. minutum cells, shifts in biogenic sulfur concentrations, the presence of other solutes, or a combination of all. Nevertheless, we suggest that these results point to the significant effect of extreme heatwaves on the physiology, growth and microbiome composition of the red-tide causing dinoflagellate A. minutum, as well as potential implications for biogenic sulfur cycling processes and marine DMS emissions.