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.