Abstract
The co-cultivation of the alphaproteobacterium Dinoroseobacter shibae with the dinoflagellate Prorocentrum minimum is characterized by a mutualistic phase followed by a pathogenic phase in which the bacterium kills aging algae. Thus it resembles the “Jekyll-and-Hyde” interaction that has been proposed for other algae and Roseobacter. Here, we identified key genetic components of this interaction. Analysis of the transcriptome of D. shibae in co-culture with P. minimum revealed growth phase dependent changes in the expression of quorum sensing, the CtrA phosphorelay, and flagella biosynthesis genes. Deletion of the histidine kinase gene cckA which is part of the CtrA phosphorelay or the flagella genes fliC or flgK resulted in complete lack of growth stimulation of P. minimum in co-culture with the D. shibae mutants. By contrast, pathogenicity was entirely dependent on one of the extrachromosomal elements of D. shibae, the 191 kb plasmid. The data show that flagella and the CtrA phosphorelay are required for establishing mutualism and prove a cell density dependent killing effect of D. shibae on P. minimum which is mediated by an unknown factor encoded on the 191 kb plasmid.
Highlights
Members of the Roseobacter clade within the Alphaproteobacteria often dominate bacterial communities associated to marine algae (Gonzalez et al, 2000; Riemann et al, 2000; Alavi et al, 2001; Allgaier et al, 2003; Tujula et al, 2010; Ankrah et al, 2014; Chen et al, 2015)
For the biosynthesis of roseobacticides in P. inhibens, three precursor molecules are needed, namely phenylacetic acid, a plant growth promoter synthesized by the bacterium, p-coumaric acid derived from aging alga, and cysteine derived from the algal osmolyte DMSP which can be used as a carbon source by the bacterium
In our previous work we demonstrated that population dynamics of P. minimum in the co-culture with D. shibae exhibited a mutualistic phase where both partners profit from each other and a pathogenic phase where D. shibae kills aging dinoflagellate cells (Wang et al, 2014a)
Summary
Members of the Roseobacter clade within the Alphaproteobacteria often dominate bacterial communities associated to marine algae (Gonzalez et al, 2000; Riemann et al, 2000; Alavi et al, 2001; Allgaier et al, 2003; Tujula et al, 2010; Ankrah et al, 2014; Chen et al, 2015). An algicidal compound termed roseobacticide is produced by Phaeobacter inhibens BS107 in the presence of p-coumaric acid, a degradation product of lignin released by aging coccolithophores like Emiliania huxleyi (Seyedsayamdost et al, 2011a,b). The relationship between the coccolithophore E. huxleyi and P. inhibens might shift from a mutualistic stage, where the bacteria protect the algae from other bacteria through the synthesis of TDA, to a pathogenic stage where algal lysis is induced by the roseobacticides. For the biosynthesis of roseobacticides in P. inhibens, three precursor molecules are needed, namely phenylacetic acid, a plant growth promoter synthesized by the bacterium, p-coumaric acid derived from aging alga, and cysteine derived from the algal osmolyte DMSP which can be used as a carbon source by the bacterium. While each of these molecules is beneficial in the mutualistic phase, they might be combined to make toxins in the pathogenic phase (Seyedsayamdost et al, 2014)
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