Plastic responses lead to increased neurotoxin production in the diatom Pseudo-nitzschia under ocean warming and acidification

Abstract

Ocean warming (OW) and acidification (OA) are recognized as two major climatic conditions influencing phytoplankton growth and nutritional or toxin content. However, there is limited knowledge on the responses of harmful algal bloom species that produce toxins. Here, the study provides quantitative and mechanistic understanding of the acclimation and adaptation responses of the domoic acid (DA) producing diatom Pseudo-nitzschia multiseries to rising temperature and pCO2 using both a one-year in situ bulk culture experiment, and an 800-day laboratory acclimation experiment. Ocean warming showed larger selective effects on growth and DA metabolism than ocean acidification. In a bulk culture experiment, increasing temperature +4 °C above ambient seawater temperature significantly increased DA concentration by up to 11-fold. In laboratory when the long-term warming acclimated samples were assayed under low temperatures, changes in growth rates and DA concentrations indicated that P. multiseries did not adapt to elevated temperature, but could instead rapidly and reversibly acclimate to temperature shifts. However, the warming-acclimated lines showed evidence of adaptation to elevated temperatures in the transcriptome data. Here the core gene expression was not reversed when warming-acclimated lines were moved back to the low temperature environment, which suggested that P. multiseries cells might adapt to rising temperature over longer timescales. The distinct strategies of phenotypic plasticity to rising temperature and pCO2 demonstrate a strong acclimation capacity for this bloom-forming toxic diatom in the future ocean.

Short-term and long-term exposure to combined elevated temperature and CO2 leads to differential growth, toxicity, and fatty acid profiles in the harmful dinoflagellate Karlodinium veneficum

“…In contrast, when exposed to long term high CO 2 (~900 generations), the diatom Phaeodactylum tricornutum reduced photosynthesis and respiration, thereby allocating a similar amount of carbon for growth as the low CO 2 selected population with no change in growth rates (Jin et al, 2022). Similar to our LT treatments, phytoplankton elemental composition, including in other dinoflagellates, does not necessarily change in response to elevated CO 2 (Burkhardt et al, 1999;Clark et al, 2014;Wynn-Edwards et al, 2014;Sugie and Yoshimura, 2016;Bercel and Kranz, 2019;Xu et al, 2023), but intracellular distributions can still change, as Chl a content approximately doubled in our LT treatments. In contrast, nitrogen, protein, and carbohydrate quotas increased in the ST cultures and this excess stored carbon may reflect a more immediate physiological response to elevated temperature and CO 2 .…”

“…In contrast, others have reported that ocean acidification alone or, in combination with elevated temperature, did not affect prey or zooplankton FA composition (Meyers et al, 2022). While these responses are results of a complex interplay of trophic interactions, short-term acclimation vs longterm adaptation as well as differences in sensitivities to elevated temperature and/or CO 2 among different taxa may explain some of this variability (Lohbeck et al, 2012;Tatters et al, 2013b;Bermudez et al, 2015;Jin et al, 2020;Xu et al, 2023). Among the order Gymnodiniales, Karlodinium species are globally prevalent (Le Bescot et al, 2016), and K. veneficum is a common constituent in coastal mid-Atlantic waters such as the Chesapeake Bay (Zhang et al, 2008).…”

No adaptation to warming after selection for 800 generations in the coccolithophore Emiliania huxleyi BOF 92

“…By contrast, the warming treatment (21 °C) for E. huxleyi BOF 92 from high latitude in our study was below its optimal growth temperature (~23°C), resulting in no adaptation over 800 generations. This implies that mild warming treatment that exerts no selective pressure can hardly give rise to evolutionary change (Xu et al, 2023).…”

Recombinase Polymerase Amplification Combined with Lateral Flow Dipstick Assay for the Rapid and Sensitive Detection of Pseudo-nitzschia multiseries

“…The number and scale of HABs are on the rise globally due to the intensification of water eutrophication and global climate change [3]. In addition, more than 70 HAB species produce toxins that pose threats to both wild and cultured marine animals and human consumers through the food chain [4,5]. Alarmingly, algal toxins account for 15% of annual poisoning-related deaths.…”

“…The neurotoxin DA has the potential to induce amnesic shellfish poisoning (ASP), with the first recorded ASP incident occurring in 1987 [10][11][12]. Subsequent investigations confirmed the origin of this toxic substance in the genus Pseudonitzschia, and since then, DA-producing Pseudo-nitzschia species have been discovered worldwide, including the HAB species of Pseudo-nitzschia multiseries [5,[13][14][15]. The diatom genus Pseudo-nitzschia has been associated with ASP events globally and is one of the key harmful microalga groups in the Guangdong coastal waters, situated in the northern South China Sea (SCS) [9].…”