Metabolic plasticity of mixotrophic algae is key for their persistence in browning environments

Abstract

Light availability is the main regulator of primary production, shaping photosynthetic communities and their production of ecologically important biomolecules. In freshwater ecosystems, increasing dissolved organic carbon concentrations, commonly known as browning, leads to lower light availability and the proliferation of mixotrophic phytoplankton. Here, a mixotrophic algal species (Cryptomonas sp.) was grown under five increasing dissolved organic carbon concentrations to uncover the plastic responses behind the success of mixotrophs in browning environments and their effect in the availability of nutritionally important biomolecules. In addition to the browning treatments, phototrophic, heterotrophic and mixotrophic growth conditions were used as controls. Despite reduced light availability, browning did not impair algal growth compared to phototrophic conditions. Comparative transcriptomics showed that genes related to photosynthesis were down-regulated, whereas phagotrophy gene categories (phagosome, lysosome, and endocytosis) were up-regulated along the browning gradient. Stable isotope analysis of phospholipid fractions validated these results, highlighting that the studied mixotroph increases its reliance on heterotrophic processes with browning. Metabolic pathway reconstruction using transcriptomic data suggests that organic carbon is acquired through phagotrophy and used to provide energy in conjunction with photosynthesis. Although metabolic responses to browning were observed, essential fatty acid content was similar between treatments while sterol content was slightly higher upon browning. Altogether, our results provide a mechanistic model of how a mixotrophic algae responds to browning and how such responses affect the availability of nutritionally essential biomolecules for higher trophic levels.