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

Abstract

Populations of the toxigenic marine dinoflagellate Alexandrium are composed of multiple genotypes that display phenotypic variation for traits known to influence top-down processes, such as the ability to lyse co-occurring competitors and prospective grazers. We performed a detailed molecular analysis of species interactions to determine how different genotypes perceive and respond to other species. In a controlled laboratory culture study, we exposed two A. fundyense strains that differ in their capacity to produce lytic compounds to the dinoflagellate grazer Polykrikos kofoidii, and analyzed transcriptomic changes during this interaction. Approximately 5% of all analyzed genes were differentially expressed between the two Alexandrium strains under control conditions (without grazer presence) with fold-change differences that were proportionally higher than those observed in grazer treatments. Species interactions led to the genotype-specific expression of genes involved in endocytotic processes, cell cycle control and outer membrane properties, and signal transduction and gene expression regulatory processes followed similar patterns for both genotypes. The genotype-specific trait changes observed in this study exemplify the complex responses to chemically mediated species interactions within the plankton and their regulation at the gene level.

Figure 1

Differentially expressed genes between control cultures of the two Alexandrium fundyense genotypes. Fold-changes and total number of differentially expressed genes for Alex2 (left) and Alex5 (right).

Figure 2

Growth rates for Alexandrium fundyense and Polykrikos kofoidii and schematic representation of the experimental set-up. The relative growth rates of Alex2 and Alex5 treatment versus control cultures, as well as for P. kofoidii cultures, are given as percentage cell population increases over 4 days. The experimental set-up shows the partition of A. fundyense and P. kofoidii cells in the cage and a surrounding compartment.

Figure 3

Cell concentration of Alex5 and Polykrikos kofoidii inside the cage. Panel (a) shows the cell concentrations and standard deviations (n=3) for Alex5 and P. kofoidii when surrounded by Alex2 cultures; panel (b) shows the cell numbers and s.d. (n=3) for Alex5 and P. kofoidii when surrounded by Alex5 cultures.

Figure 4

Differentially expressed genes and their time-dependent abundances for Alex2 and Alex5 in response to grazer presence. Genes presented here only exhibited changes in expression in the grazer treatment and not in the respective control. Selected differentially expressed genes are grouped into categories (a–d). The area of a circle represents the number of genes per category and per time point. (a) Secondary metabolic processes; (b) cell cycle control and genetic information storage and processing; (c) intracellular vesicle-associated processes; (d) signal processing and modification.

Figure 5

Abundance of selected significantly enriched Pfam protein families and domains at various time points. The Pfam families and domains are grouped into categories, as described for Figure 4. The varying shades of grey represent the number of genes within the respective Pfam domain/family. Scales are shown below each diagram. The three circles represent different analysis times: inner circle, 48 h; middle, 72 h; outer circle, 96 h. Pfam domains/families in bold italic font were significantly enriched in both genotypes.