Sublethal interactions between the harmful alga karenia brevis and its competitors

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Poulson, Kelsey L.
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I investigated how competitor species respond to chemical cues released from the red tide dinoflagellate Karenia brevis. K. brevis produces a mix of unstable, relatively polar, allelopathic organic molecules that are produced and released at low concentrations. The production of these compounds also varies greatly within and among strains of K. brevis. The majority of these compounds caused sublethal reductions in competitor growth. In laboratory experiments, these compounds inhibited the growth of competitors Asterionellopsis glacialis, Skeletonema grethae, Prorocentrum minimum, and Akashiwo sanguinea, although each species was susceptible to a different sub-set of K. brevis compounds. Cell physiological state and population densities were important in dictating the susceptibility of competitors to allelopathy: phytoplankton were most susceptible to K. brevis allelopathy when in earlier growth stages (rather than later stages) and in lower cell concentrations. However, these compounds have limited negative effects on natural, mixed populations of competitors from both near and offshore environments, and competitors from inshore and offshore environments appear to respond similarly to K. brevis allelopathy. In the sensitive competitor, Thalassiosira pseudonana, allelopathic compounds ultimately caused a reshuffling of cellular nitrogen pools, altered carbon storage and impaired osmotic regulation as determined using a nuclear magnetic resonance (NMR) based metabolomics approach. By characterizing the pool of primary metabolites present in the cell after exposure to K. brevis cues, we inferred which metabolic pathways may be affected by allelopathy. For instance, concentrations of betaine and the aromatic metabolite homarine were suppressed, indicating that K. brevis allelopathy may disrupt this competitor’s ability to osmoregulate. Exposure to K. brevis cues enhanced the concentrations of glutamate and the fatty acid caprylate/caprate in T. pseudonana, suggesting that protein degradation was enhanced and that energy metabolism was altered. This contrasts with the response to K. brevis allelopathy of the diatom Asterionellopsis glacialis, which was much more resistant to chemical cues produced by K. brevis, likely through as yet unidentified detoxification pathways. Overall, my dissertation research provides insight into how species-specific, antagonistic interactions among phytoplankton competitors can affect community structure through direct or indirect mechanisms, highlights the potential role of allelopathy in the maintenance of K. brevis blooms, and uses a novel tool set (i.e., metabolomics) to determine the molecular targets of K. brevis allelopathy. It further demonstrates that planktonic communities are complex and dynamic ecological systems and that interspecific interactions between phytoplankton can have unexpected, cascading impacts in marine systems.
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