Abstract
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.
Highlights
The aims of this study were to investigate how an acute increase in temperature (+12 ◦C), comparable to those associated with marine heatwaves (MHWs) events and leading to thermal stress in A. minutum could alter the physiological state and biogenic sulfur cycling dynamics of A. minutum and determine how these changes might influence the composition of the Alexandrium microbiome
A. minutum cell abundance exponentially increased over time in both the control (20 ◦C) and 24 ◦C temperature treatment, but a significantly faster growth rate (p = 0.001, t test) occurred at 24 ◦C (2.66 ± 0.01 d−1; average ± SE) compared to the 20 ◦C control (2.57 ± 0.01 d−1), resulting in significantly greater cell abundance at 96 h (p = 0.007) and 120h (p < 0.001)
We found no evidence for reactive oxygen species (ROS) build-up in A. minutum cultures, possibly because ROS concentrations were kept in check by sufficient dimethyl sulfide (DMS) synthesis and active DMS-mediated ROS scavenging (Lesser, 2006; Sunda et al, 2002)
Summary
Many marine phytoplankton produce the organic sulfur compound dimethyl sulfoniopropionate (DMSP) (Zhou et al, 2009; Berdalet et al, 2011; Caruana and Malin, 2014), as it can function as an antioxidant, osmolyte, chemoattractant and currency in reciprocal chemical exchanges with heterotrophic bacteria (Stefels, 2000; Sunda et al, 2002; Kiene et al, 2000; Seymour et al, 2010). Phytoplankton-derived DMSP is a major source of sulfur and carbon for marine heterotrophic bacteria (Kiene et al, 2000), which in turn. Some strains of Alexandrium, including A. minutum, produce saxitoxins, which lead to paralytic shellfish poisoning (PSP) and are responsible for the most harmful algal blooms in terms of magnitude, distribution and consequences on human health (Anderson et al, 2012)
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