Characterization of grazer-induced responses in the marine dinoflagellate Alexandrium tamarense

Sylke.Wohlrab [ at ]


Harmful algal blooms (HABs) have increased worldwide over the last several decades. The characterization of processes that promote the ecological success of toxic algae species that form such blooms has therefore gained immense importance. The HAB-dinoflagellate Alexandrium tamarense causes outbreaks of Paralytic Shellfish Poisoning (PSP) due to the synthesis of the highly neurotoxic alkaloid saxitoxin and several of its analogues (Paralytic Shellfish Toxins, PSTs). While the ecological function of PST production is still unknown and their allelochemical nature is mainly supposed due to the negative effects they have on some copepod species, there are other unknown secondary metabolites produced by A. tamarense which are definitely known to possess allelochemical properties. These compounds are distinct from PSTs and have a lytic effect on co-occurring competitors and protistan grazers. The investigations in this thesis focus on the analysis of mechanisms that promote the success in grazer interactions related to secondary metabolite synthesis in A. tamarense. The implementation of functional genomic tools enabled a detailed characterization of processes that are induced due to the presence of grazers in A. tamarense. Such induced processes that either decrease grazing pressure and/or provide an advantage over co-occurring species in the presence of grazers can strongly promote a species’ success. Within this thesis work an increase in PST content due to the presence of copepods and their cues was demonstrated to occur in A. tamarense. Behavioral investigations on the fitness of the copepods and the analysis of gene expression patterns in A. tamarense showed that toxin production only increases when the copepod represents a threat in terms of grazing pressure. Co-evolution therefore seems to have driven the ability of A. tamarense to recognize threatening grazers based on their cues and in turn drove selection for less susceptible grazers. The results further show that the increased toxin synthesis in the presence of cues from copepods is accompanied by a reduction in cell-chain length in A. tamarense and that both responses are reversible. Hence the inducing cue is well suited to track ambient grazer concentrations. In addition, the response of A. tamarense towards this cue appeared to be more complex than previously thought, i.e. they comprise trait changes at the morphological and physiological level. It was further demonstrated that this induced defense response against copepods is realized in different ways in two A. tamarense strains. Hundreds of genes were differentially expressed in response to trace amount of copepod cues, with a large discrepancy between the two A. tamarense strains tested. Furthermore, the two genotypes seem to express different target-defended phenotypes that are, however, both able to enhance defense against copepods, but with varying costs and efforts as inferred from the transcriptomic analysis. As a consequence, the induced defense response implies different trade-offs for each A. tamarense strain investigated. A further discrepancy was observed for the physiological realization of the increased PST synthesis, which points towards a convoluted regulation of toxin synthesis in A. tamarense. Transcriptomic analysis of the response of A. tamarense towards a protistan grazer (Polykrikos kofoidii, Dinophyceae) showed that a large number of genes are associated with this species interaction. Lytic compound production seems therefore to be only one of several traits that promote the success of A. tamarense in the presence of such grazers. Endocytic processes, outer-membrane properties and cell cycle progression might be influenced additionally due to the presence of a protistan grazer. The investigated differences in the gene expression of the lytic and non-lytic strain without grazers points towards a maintenance of high allelic variation in natural A. tamarense populations perhaps as a consequence of large scale gene duplications. The transcriptional analysis of the grazer-induced responses provided the basis for the successive establishment of a gene library derived from a high-throughput sequencing platform. The annotation of the final data indicated a comparable high abundance of genes involved in signal transduction processes and secondary metabolite biosynthesis, affirming that species interactions might have a major influence on the selection of genomic features. In conclusion, the fact that co-occurring grazers have the potential to influence several traits in A. tamarense indicates that a sophisticated range of responses that enable A. tamarense strains to succeed under diverse grazing pressure has been selected for through evolution. These multifaceted grazer-induced responses may have further consequences on the community structure that go beyond simple ingestion and thus loss of cell cohorts from the population. Investigation of co-evolutionary driven adaptations in addition to grazer behavior as well as mesocosm studies might contribute substantially to the ongoing search for conceptual models to describe the formation and development of harmful algal blooms.

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Wohlrab, S. (2013): Characterization of grazer-induced responses in the marine dinoflagellate Alexandrium tamarense PhD thesis, Universität Bremen.

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