Abstract

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.

Highlights

  • Diatoms have co-occurred with marine bacteria for millions of years

  • We tested the physiological response of S. robusta to short- and long-chained acyl homoserine lactones (AHLs), including C6-HSL, OH-C6-HSL, oxo-C6-HSL, C14-HSL, OH-C14-HSL, and oxo-C14-HSL with a DMSO treatment serving as control (Figures 1, 2)

  • Quorum sensing compounds released by bacteria do play an important role as signaling compounds among conspecific cells but are documented to be involved in interkingdom signaling between bacteria and eukaryotes

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Summary

Introduction

Diatoms have co-occurred with marine bacteria for millions of years. A suite of diatom-bacteria interactions have been described, ranging from pathogenic bacteria inducing diatom cell lysis to mutualistic relationships (Amin et al, 2012; Meyer et al, 2017; Seymour et al, 2017). The majority of diatoms’ satellite bacteria, isolated from field and laboratory cultures, belong to the phyla Proteobacteria and Bacteroidetes (Schäfer et al, 2002; Grossart et al, 2005; Amin et al, 2012; Buchan et al, 2014; Green et al, 2015). The most extensively studied class of bacterial QS molecules are N-acyl homoserine lactones (AHLs). These molecules consist of a lactone ring coupled to an acyl chain, which can vary in length from 4 up to 18 carbon atoms (Hmelo, 2017; Waters and Bassler, 2005). AHLs can have a substitution at the C3 position of the acyl chain in the form of a hydroxyl- or keto-group (Waters and Bassler, 2005), further contributing to the functional diversity of these compounds in bacterial signaling

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