Trait changes induced by species interactions in two phenotypically distinct strains of a marine dinoflagellate

Wohlrab, Sylke; Tillmann, Urban; Cembella, Allan; John, Uwe

doi:10.1038/ismej.2016.57

Cited by 16 publications

(10 citation statements)

References 51 publications

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“…The concept that species interactions via chemical signals are a major driving force in shaping the structure of plankton communities has recently found experimental support [ 14 , 40 ]. However, data explaining the molecular mechanisms underlying these processes are still scarce.…”

Section: Discussionmentioning

confidence: 99%

“…Most of the regulated genes have unknown function, making it difficult to reconstruct a mechanism for the response. Transcriptomics allowed the exploration of the differences in gene expression between two Alexandrium fundyense strains exposed to a protist grazer [ 14 ]. Signal transduction via G protein-coupled receptors (GPCRs) was hypothesised in A. fundyense when exposed to the heterotrophic dinoflagellate, but DNA methylation and thus epigenetic regulation was also indicated.…”

Section: Introductionmentioning

confidence: 99%

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Grazer-induced transcriptomic and metabolomic response of the chain-forming diatom Skeletonema marinoi

et al. 2018

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Diatoms and copepods are main actors in marine food webs. The prey–predator interactions between them affect bloom dynamics, shape marine ecosystems and impact the energy transfer to higher trophic levels. Recently it has been demonstrated that the presence of grazers may affect the diatom prey beyond the direct effect of grazing. Here, we investigated the response of the chain-forming centric diatom Skeletonema marinoi to grazer cues, including changes in morphology, gene expression and metabolic profile. S. marinoi cells were incubated with Calanus finmarchicus or with Centropages typicus and in both cases responded by reducing the chain length, whereas changes in gene expression indicated an activation of stress response, changes in the lipid and nitrogen metabolism, in cell cycle regulation and in frustule formation. Transcripts linked to G protein-coupled receptors and to nitric oxide synthesis were differentially expressed suggesting involvement of these signalling transduction pathways in the response. Downregulation of a lipoxygenase in the transcriptomic data and of its products in the metabolomic data also indicate an involvement of oxylipins. Our data contribute to a better understanding of the gene function in diatoms, providing information on the nature of genes implicated in the interaction with grazers, a crucial process in marine ecosystems.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Grazer-induced transcriptomic and metabolomic response of the chain-forming diatom Skeletonema marinoi

et al. 2018

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“…Cellular signal transduction depends on the perception of external cues, but how the diatoms or other phytoplankton species perceive the predator cues is still poorly understood. Perception by signal transduction via G protein-coupled receptors is proposed for the dinoflagellate Alexandrium catenella exposed to a heterotrophic dinoflagellate grazer [12]. When exposed to different grazers (copepods), the induced defense response and the discrimination between copepod species were suggested to be regulated by protein kinases and calcium signaling [13].…”

Section: Introductionmentioning

confidence: 99%

Transcriptomic responses to grazing reveal the metabolic pathway leading to the biosynthesis of domoic acid and highlight different defense strategies in diatoms

et al. 2019

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Background A major cause of phytoplankton mortality is predation by zooplankton. Strategies to avoid grazers have probably played a major role in the evolution of phytoplankton and impacted bloom dynamics and trophic energy transport. Certain species of the genus Pseudo-nitzschia produce the neurotoxin, domoic acid (DA), as a response to the presence of copepod grazers, suggesting that DA is a defense compound. The biosynthesis of DA comprises fusion of two precursors, a C10 isoprenoid geranyl pyrophosphate and l -glutamate. Geranyl pyrophosphate (GPP) may derive from the mevalonate isoprenoid (MEV) pathway in the cytosol or from the methyl-erythritol phosphate (MEP) pathway in the plastid. l -glutamate is suggested to derive from the citric acid cycle. Fragilariopsis , a phylogenetically related but nontoxic genus of diatoms, does not appear to possess a similar defense mechanism. We acquired information on genes involved in biosynthesis, precursor pathways and regulatory functions for DA production in the toxigenic Pseudo-nitzschia seriata , as well as genes involved in responses to grazers to resolve common responses for defense strategies in diatoms. Results Several genes are expressed in cells of Pseudo-nitzschia when these are exposed to predator cues. No genes are expressed in Fragilariopsis when treated similarly, indicating that the two taxa have evolved different strategies to avoid predation. Genes involved in signal transduction indicate that Pseudo-nitzschia cells receive signals from copepods that transduce cascading molecular precursors leading to the formation of DA. Five out of seven genes in the MEP pathway for synthesis of GPP are upregulated, but none in the conventional MEV pathway. Five genes with known or suggested functions in later steps of DA formation are upregulated. We conclude that no gene regulation supports that l -glutamate derives from the citric acid cycle, and we suggest the proline metabolism to be a downstream precursor. Conclusions Pseudo-nitzschia cells, but not Fragilariopsis , receive and respond to copepod cues. The cellular route for the C10 isoprenoid product for biosynthesis of DA arises from the MEP metabolic pathway and we suggest proline metabolism to be a downstream precursor for l -glutamate. We suggest 13 genes with unknown function to be involved in diatom responses to grazers. Electronic supplementary material The online version of this article (10.1186/s12867-019-0124-0) contains supplementary material, which is available to authorized users.

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“…; Wohlrab et al . ), and the detoxification of secondary metabolites (Arfi, Levasseur & Record ). Such changes, though only observable at the molecular level, may be of major importance in determining the strength, type and outcome of species interactions (Schulze et al .…”

Section: Introductionmentioning

confidence: 99%

Ecological interactions and coexistence are predicted by gene expression similarity in freshwater green algae

et al. 2017

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1. Phenotypic variation controls the species interactions which determine whether or not species coexist. Long-standing hypotheses in ecology and evolution posit that phenotypic differentiation enables coexistence by increasing the size of niche differentiation. This hypothesis has only been tested using macroscopic traits to date, but niche differentiation, particularly of microscopic organisms, also occurs at the molecular and metabolic level. 2. We examined how phenotypic variation that arises at the level of gene expression over evolutionary time affects phytoplankton species interactions and coexistence. 3. We predicted that similarity in gene expression among species would decline with phylogenetic distance, and that reduced similarity in gene expression would weaken competition, increase facilitation and promote coexistence. 4. To test this, we grew eight species of freshwater green algae in monocultures and bicultures for 46 days in a laboratory microcosm experiment. We quantified the strength of species interactions by: (i) fitting Lotka-Volterra models to time-series densities and estimating interaction coefficients, and (ii) calculating relative densities that compare species' steady-state densities in biculture to those in monoculture. We used Illumina high throughput sequencing to quantify the expression of 1253 families of homologous genes, including a set of 17 candidate genes that we hypothesized a priori to be involved in competition or facilitation. 5. Synthesis. We found that closely related species had greater similarity in gene expression than did distantly related species, but as gene expression became more similar, species experienced weaker competition or greater facilitation, and were more likely to coexist. We identified gene functional categories that were uniquely differentially regulated in association with particular species interaction types. Contrary to common thinking in ecology and evolution, similarity in gene expression, and not differentiation, was associated with weaker competition, facilitation and coexistence.

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Trait changes induced by species interactions in two phenotypically distinct strains of a marine dinoflagellate

Cited by 16 publications

References 51 publications

Grazer-induced transcriptomic and metabolomic response of the chain-forming diatom Skeletonema marinoi

Grazer-induced transcriptomic and metabolomic response of the chain-forming diatom Skeletonema marinoi

Transcriptomic responses to grazing reveal the metabolic pathway leading to the biosynthesis of domoic acid and highlight different defense strategies in diatoms

Ecological interactions and coexistence are predicted by gene expression similarity in freshwater green algae

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