The frequency and intensity of harmful algal blooms (HABs) and phytoplankton community shifts toward toxic species have increased worldwide. Although most research has focused on eutrophication as the cause of this trend, many other global-and regional-scale anthropogenic influences may also play a role. Ocean acidification (high pCO 2 /low pH), greenhouse warming, shifts in nutrient availability, ratios, and speciation, changing exposure to solar irradiance, and altered salinity all have the potential to profoundly affect the growth and toxicity of these phytoplankton. Except for ocean acidification, the effects of these individual factors on harmful algae have been studied extensively. In this review, we summarize our understanding of the influence of each of these single factors on the physiological properties of important marine HAB groups. We then examine the much more limited literature on how rising CO 2 together with these other concurrent environmental changes may affect these organisms, including what is possibly the most critical property of many species: toxin production. New work with several diatom and dinoflagellate species suggests that ocean acidification combined with nutrient limitation or temperature changes may dramatically increase the toxicity of some harmful groups. This observation underscores the need for more in-depth consideration of poorly understood interactions between multiple global change variables on HAB physiology and ecology. A key limitation of global change experiments is that they typically span only a few algal generations, making it difficult to predict whether they reflect likely future decadal-or century-scale trends. We conclude by calling for thoughtfully designed experiments and observations that include adequate consideration of complex multivariate interactive effects on the long-term responses of HABs to a rapidly changing future marine environment.
Anthropogenic CO2 is progressively acidifying the ocean, but the responses of harmful algal bloom species that produce toxins that can bioaccumulate remain virtually unknown. The neurotoxin domoic acid is produced by the globally-distributed diatom genus Pseudo-nitzschia. This toxin is responsible for amnesic shellfish poisoning, which can result in illness or death in humans and regularly causes mass mortalities of marine mammals and birds. Domoic acid production by Pseudo-nitzschia cells is known to be regulated by nutrient availability, but potential interactions with increasing seawater CO2 concentrations are poorly understood. Here we present experiments measuring domoic acid production by acclimatized cultures of Pseudo-nitzschia fraudulenta that demonstrate a strong synergism between projected future CO2 levels (765 ppm) and silicate-limited growth, which greatly increases cellular toxicity relative to growth under modern atmospheric (360 ppm) or pre-industrial (200 ppm) CO2 conditions. Cellular Si∶C ratios decrease with increasing CO2, in a trend opposite to that seen for domoic acid production. The coastal California upwelling system where this species was isolated currently exhibits rapidly increasing levels of anthropogenic acidification, as well as widespread episodic silicate limitation of diatom growth. Our results suggest that the current ecosystem and human health impacts of toxic Pseudo-nitzschia blooms could be greatly exacerbated by future ocean acidification and ‘carbon fertilization’ of the coastal ocean.
Increasing pCO 2 (partial pressure of CO 2 ) in an "acidified" ocean will affect phytoplankton community structure, but manipulation experiments with assemblages briefly acclimated to simulated future conditions may not accurately predict the long-term evolutionary shifts that could affect inter-specific competitive success. We assessed community structure changes in a natural mixed dinoflagellate bloom incubated at three pCO 2 levels (230, 433, and 765 ppm) in a short-term experiment (2 weeks). The four dominant species were then isolated from each treatment into clonal cultures, and maintained at all three pCO 2 levels for approximately 1 year. Periodically (4, 8, and 12 months), these pCO 2 -conditioned clones were recombined into artificial communities, and allowed to compete at their conditioning pCO 2 level or at higher and lower levels. The dominant species in these artificial communities of CO 2 -conditioned clones differed from those in the original short-term experiment, but individual species relative abundance trends across pCO 2 treatments were often similar. Specific growth rates showed no strong evidence for fitness increases attributable to conditioning pCO 2 level. Although pCO 2 significantly structured our experimental communities, conditioning time and biotic interactions like mixotrophy also had major roles in determining competitive outcomes. New methods of carrying out extended mixed species experiments are needed to accurately predict future long-term phytoplankton community responses to changing pCO 2 .
Ocean acidification and greenhouse warming will interactively influence competitive success of key phytoplankton groups such as diatoms, but how long-term responses to global change will affect community structure is unknown. We incubated a mixed natural diatom community from coastal New Zealand waters in a short-term (two-week) incubation experiment using a factorial matrix of warming and/or elevated p CO 2 and measured effects on community structure. We then isolated the dominant diatoms in clonal cultures and conditioned them for 1 year under the same temperature and p CO 2 conditions from which they were isolated, in order to allow for extended selection or acclimation by these abiotic environmental change factors in the absence of interspecific interactions. These conditioned isolates were then recombined into ‘artificial’ communities modelled after the original natural assemblage and allowed to compete under conditions identical to those in the short-term natural community experiment. In general, the resulting structure of both the unconditioned natural community and conditioned ‘artificial’ community experiments was similar, despite differences such as the loss of two species in the latter. p CO 2 and temperature had both individual and interactive effects on community structure, but temperature was more influential, as warming significantly reduced species richness. In this case, our short-term manipulative experiment with a mixed natural assemblage spanning weeks served as a reasonable proxy to predict the effects of global change forcing on diatom community structure after the component species were conditioned in isolation over an extended timescale. Future studies will be required to assess whether or not this is also the case for other types of algal communities from other marine regimes.
Ochromonas spp. strains CCMP1393 and BG-1 are phagotrophic phytoflagellates with different nutritional strategies. Strain CCMP1393 is an obligate phototroph while strain BG-1 readily grows in continuous darkness in the presence of bacterial prey. Growth and gene expression of strain CCMP1393 were investigated under conditions allowing phagotrophic, mixotrophic, or phototrophic nutrition. The availability of light and bacterial prey led to the differential expression of 42% or 45–59% of all genes, respectively. Data from strain CCMP1393 were compared to those from a study conducted previously on strain BG-1, and revealed notable differences in carbon and nitrogen metabolism between the 2 congeners under similar environmental conditions. Strain BG-1 utilized bacterial carbon and amino acids through glycolysis and the tricarboxylic acid cycle, while downregulating light harvesting and carbon fixation in the Calvin cycle when both light and bacteria were available. In contrast, the upregulation of genes related to photosynthesis, light harvesting, chlorophyll synthesis, and carbon fixation in the presence of light and prey for strain CCMP1393 implied that this species is more phototrophic than strain BG-1, and that phagotrophy may have enhanced phototrophy. Cellular chlorophyll a content was also significantly higher in strain CCMP1393 supplied with bacteria compared to those without prey. Our results thus point to very different physiological strategies for mixotrophic nutrition in these closely related chrysophyte species.
The karlotoxins are a family of amphidinol-like compounds that play roles in avoiding predation and in prey capture for the toxic dinoflagellate Karlodinium veneficum. The first member of the toxin group to be reported was KmTx 1 (1), and here we report an additional five new members of this family (3-7) from the same strain. Of these additional compounds, KmTx 3 (3) differs from KmTx 1 (1) in having one less methylene group in the saturated portion of its lipophilic arm. In addition, 64-E-chloro-KmTx 3 (4) and 10-O-sulfo-KmTx 3 (5) were identified. Likewise, 65-Echloro-KmTx 1 (6) and 10-O-sulfo-KmTx 1 (7) were also isolated. Comparison of the hemolytic activities of the newly isolated compounds to that of KmTx 1 shows that potency correlates positively with the length of the lipophilic arm and is disrupted by sulfonation of the polyol arm.The karlotoxins are a class of amphidinol-like compounds produced by mixotrophic strains of the dinoflagellate Karlodinium veneficum.1 , 2 The karlotoxins have been reported to display a variety of interesting effects on biological systems including cellular lysis,1 , 3 -6 damage of fish gills,1 , 3 , 7 -9 and immobilization of prey organisms.10 There is growing evidence that the karlotoxins support a number of ecological roles for K. veneficum including deterring predation,11 and assisting prey capture.2 , 12 The cytolytic activity of the karlotoxins is modulated by membrane sterol composition which has been proposed as a mechanism for K. veneficum avoiding autotoxicity.13 -15 K. veneficum has been implicated in several fish kill events apparently caused by the damaging effects of the karlotoxins. 1 , 3 , 12 , 16 , 17 Two families of karlotoxins have been described as belonging to the KmTx 1 and KmTx 2 groups that differ from one another in UV absorbance maxima, potency, and geographic distribution.18 Although the reports of toxic compounds from K. veneficum (originally Gymnodinium veneficum) date back to the 1950s,7 it has only been in recent years that structures were reported for KmTx 1 (1),4 and KmTx 2 (2),17 , 19 including the absolute configuration for the latter compound.19 With the structures of KmTx 1 (1) and KmTx 2 (2) now reported, the difference between the two compounds in carbon chain structure is * Author to whom correspondence should be addressed. Phone: 910 962 2397 Fax: 910 962 2410 wrightj@uncw.edu. † Center for Marine Science, UNC Wilmington ‡ Center for Food Safety and Applied Nutrition, USFDA § Institute for Marine and Environmental Technology, University of Maryland Center of Environmental Sciences Supporting Information Available: 1D and 2D NMR spectra for compounds 3-7; EPI spectra for compounds 3, 4, and 6; highresolution mass spectra for compounds 3-7; hemolytic assay EC 50 curves for compounds 3-7. This material is available free of charge via the Internet at http://pubs.acs.org. localized to the length of the lipophilic side chain. In KmTx 1 (1) the side chain is 18 carbons in length (C-48-C-65) whereas in KmTx 2 (2) it is two carbons s...
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