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Decision-making of the benthic diatom Seminavis robusta searching for inorganic nutrients and pheromones.

ABSTRACT: Microorganisms encounter a diversity of chemical stimuli that trigger individual responses and influence population dynamics. However, microbial behavior under the influence of different incentives and microbial decision-making is poorly understood. Benthic marine diatoms that react to sexual attractants as well as to nutrient gradients face such multiple constraints. Here, we document and model behavioral complexity and context-sensitive responses of these motile unicellular algae to sex pheromones and the nutrient silicate. Throughout the life cycle of the model diatom Seminavis robusta nutrient-starved cells localize sources of silicate by combined chemokinetic and chemotactic motility. However, with an increasing need for sex to restore the initial cell size, a change in behavior favoring the attraction-pheromone-guided search for a mating partner takes place. When sex becomes inevitable to prevent cell death, safeguard mechanisms are abandoned, and cells prioritize the search for mating partners. Such selection processes help to explain biofilm organization and to understand species interactions in complex communities.

SUBMITTER: Bondoc KGV

PROVIDER: S-EPMC6331598 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Decision-making of the benthic diatom Seminavis robusta searching for inorganic nutrients and pheromones.

Bondoc Karen Grace V KGV Lembke Christine C Lang Stefan N SN Germerodt Sebastian S Schuster Stefan S Vyverman Wim W Pohnert Georg G

The ISME journal 20181009 2

Microorganisms encounter a diversity of chemical stimuli that trigger individual responses and influence population dynamics. However, microbial behavior under the influence of different incentives and microbial decision-making is poorly understood. Benthic marine diatoms that react to sexual attractants as well as to nutrient gradients face such multiple constraints. Here, we document and model behavioral complexity and context-sensitive responses of these motile unicellular algae to sex pherom ...[more]

PMID: 30301945

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Project description:In aquatic habitats, diatoms are frequently found in association with Proteobacteria, many members of which employ cell-to-cell communication via N-acyl homoserine lactones (AHLs). It has been suggested that diatoms could distinguish between beneficial and algicidal bacteria in their surroundings by sensing AHLs. Although some microalgae can interfere with AHL signaling, e.g., by releasing AHL mimics or degrading them, molecular responses to AHLs in microalgae are still unclear. Therefore, we tested the effects of short-chained AHLs, i.e., N-hexanoyl homoserine lactone (C6-HSL), N-3-hydroxyhexanoyl homoserine lactone (OH-C6-HSL), and N-3-oxohexanoyl homoserine lactone (oxo-C6-HSL) and long-chained AHLs, i.e., N-tetradecanoyl homoserine lactone (C14-HSL), N-3-hydroxytetradecanoyl homoserine lactone (OH-C14-HSL), and N-3-oxotetradecanoyl homoserine lactone (oxo-C14-HSL), on growth of the benthic diatom Seminavis robusta. All tested short-chained AHLs did not affect diatom growth, while long-chained AHLs promoted (C14-HSL) or inhibited (OH-C14-HSL and oxo-C14-HSL) growth. To investigate the physiological effects of these long-chained AHLs in more detail, an RNA-seq experiment was performed during which S. robusta was treated with the growth-promoting C14-HSL and the growth-inhibiting oxo-C14-HSL. One tetramic acid was also tested (TA14), a structural rearrangement product of oxo-C14-HSL, which also induced growth inhibition in S. robusta. After 3 days of treatment, analysis revealed that 3,410 genes were differentially expressed in response to at least one of the compounds. In the treatment with the growth-promoting C14-HSL many genes involved in intracellular signaling were upregulated. On the other hand, exposure to growth-inhibiting oxo-C14-HSL and TA14 triggered a switch in lipid metabolism towards increased fatty acid degradation. In addition, oxo-C14-HSL led to downregulation of cell cycle genes, which is in agreement with the stagnation of cell growth in this treatment. Combined, our results indicate that bacterial signaling molecules with high structural similarity induce contrasting physiological responses in S. robusta.

Dataset Information

Decision-making of the benthic diatom Seminavis robusta searching for inorganic nutrients and pheromones.

Publications

Decision-making of the benthic diatom Seminavis robusta searching for inorganic nutrients and pheromones.

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