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Constitutive mixoplankton—plastid–bearing microbial eukaryotes capable of both phototrophy and phagotrophy—are ubiquitous in marine ecosystems and facilitate carbon transfer to higher trophic levels within aquatic food webs, which supports enhanced sinking carbon flux. However, the regulation of the relative contribution of photosynthesis and prey consumption remains poorly characterized. We investigated the transcriptional dynamics behind this phenotypic plasticity in the prasinophyte green alga Pterosperma cristatum. Based on what is known of other mixoplankton species that cannot grow without photosynthesis (obligate phototrophs), we hypothesized that P. cristatum uses phagotrophy to circumvent the restrictions imposed on photosynthesis by nutrient depletion, to obtain nutrients from ingested prey, and to maintain photosynthetic carbon fixation. We observed an increase in feeding as a response to nutrient depletion, coinciding with an upregulation of expression for genes involved in essential steps of phagocytosis including prey recognition, adhesion and engulfment, transport and maturation of food vacuoles, and digestion. Unexpectedly, genes involved in the photosynthetic electron transfer chain, pigment biosynthesis, and carbon fixation were downregulated as feeding increased, implying an abatement of photosynthesis. Contrary to our original hypothesis, our results therefore suggest that depletion of inorganic nutrients triggered an alteration of trophic behavior from photosynthesis to phagotrophy in P. cristatum. While this behavior distinguishes P. cristatum from other groups of constitutive mixoplankton, its physiological response aligns with recent discoveries from natural microbial communities. These findings indicate that mixoplankton communities in nutrient-limited oceans can regulate photosynthesis against bacterivory based on nutrient availability.

 

Abstract Small pigmented eukaryotes (⩽ 5 µm) are an important, but overlooked component of global marine phytoplankton. The Amazon River plume delivers nutrients into the oligotrophic western tropical North Atlantic, shades the deeper waters, and drives the structure of microphytoplankton (> 20 µm) communities. For small pigmented eukaryotes, however, diversity and distribution in the region remain unknown, despite their significant contribution to open ocean primary production and other biogeochemical processes. To investigate how habitats created by the Amazon river plume shape small pigmented eukaryote communities, we used high-throughput sequencing of the 18S ribosomal RNA genes from up to five distinct small pigmented eukaryote cell populations, identified and sorted by flow cytometry. Small pigmented eukaryotes dominated small phytoplankton biomass across all habitat types, but the population abundances varied among stations resulting in a random distribution. Small pigmented eukaryote communities were consistently dominated by Chloropicophyceae (0.8–2 µm) and Bacillariophyceae (0.8–3.5 µm), accompanied by MOCH-5 at the surface or by Dinophyceae at the chlorophyll maximum. Taxonomic composition only displayed differences in the old plume core and at one of the plume margin stations. Such results reflect the dynamic interactions of the plume and offshore oceanic waters and suggest that the resident small pigmented eukaryote diversity was not strongly affected by habitat types at this time of the year. 

While algal phago-mixotrophs play a major role in aquatic microbial food webs, their diversity remains poorly understood. Recent studies have indicated several species of prasinophytes, early diverging green algae, to be able to consume bacteria for nutrition. To further explore the occurrence of phago-mixotrophy in green algae, we conducted feeding experiments with live fluorescently labeled bacteria stained with CellTracker Green CMFDA, heat-killed bacteria stained with 5-(4,6-dichlorotriazin-2-yl) aminofluorescein (DTAF), and magnetic beads. Feeding was detected via microscopy and/or flow cytometry in five strains of prasinophytes when provided with live bacteria: Pterosperma cristatum NIES626, Pyramimonas parkeae CCMP726, Pyramimonas parkeae NIES254, Nephroselmis pyriformis RCC618, and Dolichomastix tenuilepis CCMP3274. No feeding was detected when heat-killed bacteria or magnetic beads were provided, suggesting a strong preference for live prey in the strains tested. In parallel to experimental assays, green algal bacterivory was investigated using a gene-based prediction model. The predictions agreed with the experimental results and suggested bacterivory potential in additional green algae. Our observations underline the likelihood of widespread occurrence of phago-mixotrophy among green algae, while additionally highlighting potential biases introduced when using prey proxy to evaluate bacterial ingestion by algal cells.