Heterotrophic bacteria trigger transcriptome remodelling in the photosynthetic picoeukaryote Micromonas commoda

Abstract

Marine biogeochemical cycles are built on interactions between surface ocean microbes, particularly those connecting phytoplankton primary producers to heterotrophic bacteria. Details of these associations are not well understood, especially in the case of direct influences of bacteria on phytoplankton physiology. Here we catalogue how the presence of three marine bacteria (Ruegeria pomeroyi DSS-3, Stenotrophomonas sp. SKA14 and Polaribacter dokdonensis MED152) individually and uniquely impact gene expression of the picoeukaryotic alga Micromonas commoda RCC 299. We find a dramatic transcriptomic remodelling by M. commoda after 8 h in co-culture, followed by an increase in cell numbers by 56 h compared with the axenic cultures. Some aspects of the algal transcriptomic response are conserved across all three bacterial co-cultures, including an unexpected reduction in relative expression of photosynthesis and carbon fixation pathways. Expression differences restricted to a single bacterium are also observed, with the Flavobacteriia P. dokdonensis uniquely eliciting changes in relative expression of algal genes involved in biotin biosynthesis and the acquisition and assimilation of nitrogen. This study reveals that M. commoda has rapid and extensive responses to heterotrophic bacteria in ways that are generalizable, as well as in a taxon specific manner, with implications for the diversity of phytoplankton-bacteria interactions ongoing in the surface ocean.

FIGURE 1

(A) Cell abundances of Micromonas commoda based on flow cytometric analysis for co‐cultures and axenic cultures. (B) Inorganic nutrient measurements in spent media of experimental cultures at the 8 h time point. Average values for all data are shown with error bars representing the standard deviation of biological replicates, n = 4.

FIGURE 2

Micromonas commoda genes differentially expressed between the axenic and co‐culture treatments. Genes displayed have putative annotations in key pathways. The log₂ fold change of each gene is indicated by the colour gradient, with blue representing transcript depletion and red representing transcript enrichment in the co‐cultures compared with the axenic cultures. Genes with asterisks had statistically significant differential expression (DESeq2, adjusted p‐value <0.01, n = 3 or 4). Gene names in black font represent those with a shared directionality of log₂ fold change within the row (either positive or negative) for all co‐culture treatments. The number of significantly differentially expressed genes out of the total genes in the M. commoda genome annotated as part of a pathway is indicated by the numbers on the left‐hand side for each pathway cluster.

FIGURE 3

Examples of shared and unique Micromonas commoda transcriptional responses to the presence of heterotrophic bacteria. (A) Shared response to all three bacteria in expression of light harvesting reactions of photosynthesis and the Calvin cycle. (B) Unique response to Polaribacter dokdonensis in expression of nitrogen acquisition and assimilation. Functional components represented in red indicate enriched expression in co‐cultures and in blue indicate depleted expression. Components represented in grey showed no differential expression. Transporter localization within the M. commoda cell depicted in (B) is based on information from McDonald et al. (2010), with asterisks indicating inconsistencies between annotation tools used in prediction.