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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. 

Abstract 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. 

Coevolution—reciprocal evolutionary change between interacting lineages (Thompson, 1994; see Glossary)—is thought to have played a profound role in the evolution of Life on Earth. From similar patterns across the wings of unrelated lineages of butterflies (Hoyal Cuthill and Charleston, 2015), egg mimicry of “cheating” brood parasites (Davies, 2010), to the role of animal pollinators in driving the diversification of flowering plants (Kay and Sargent, 2009), to the ubiquity of sexual reproduction and sexual conflicts (Hamilton, 2002; Arnqvist and Rowe, 2005; King et al., 2009), the formation of the eukaryotic cell (Martin et al., 2015; Imachi et al., 2020), and even the origin of living organisms themselves (Mizuuchi and Ichihashi, 2018), evolutionary changes among interacting lineages have played profound and important roles in the history of Life. This Grand Challenges inaugural contribution encompasses eclectic opinions of the editorial board as to what are the next frontiers of coevolution research in the 21st century. Coevolutionary biology is a field that has garnered a lot of attention in recent years, in part as a result of technical advances in nucleotide sequencing and bioinformatics in the burgeoning field of host–microbial interactions. Many seminal studies of coevolution examined reciprocal evolutionary change between two or a few interacting macroscopic species that imposed selective pressures on one another (e.g., insect or bird pollinators and their flowering host plants). Understanding the contexts under which coevolution occurs, as opposed to scenarios in which each partner adapts independently to a particular environment (Darwin, 1862; Stiles, 1978) is important to elucidate coevolutionary processes. A whole spectrum of organismal interactions has been examined under the lens of coevolution, providing additional context, and nuance to ecological strategies traditionally categorized as ranging from beneficial to detrimental for participating species (Figure 1). In particular, a coevolutionary perspective has revealed that even “mutualisms” are not always fully beneficial or cooperative for the partners involved. Instead, the tendency to “cheat” permeates across symbiotic partnerships (Perez-Lamarque et al., 2020). Conversely, recent evidence suggests that non-lethal predation by co-evolved predators, which has traditionally been assumed to be entirely antagonistic, may provide sessile prey with some indirect benefit through enhanced opportunities to acquire beneficial symbiotic microorganisms (Grupstra et al., 2021). Herein, we discuss some of the recent areas of active research in coevolution, restricting our focus to coevolution between interacting species. 

Abstract We found that in the phosphate (PO₄)‐depleted western subtropical North Atlantic Ocean, small‐sized pigmented eukaryotes (P‐Euk; < 5 μm) play a central role in the carbon (C) cycling. Although P‐Euk were only ~ 5% of the microbial phytoplankton cell abundance, they represented at least two thirds of the microbial phytoplankton C biomass and fixed more CO₂than picocyanobacteria, accounting for roughly half of the volumetric CO₂fixation by the microbial phytoplankton, or a third of the total primary production. Cell‐specific PO₄assimilation rates of P‐Euk and nonpigmented eukaryotes (NP‐Euk; < 5 μm) were generally higher than of picocyanobacteria. However, when normalized to biovolumes, picocyanobacteria assimilated roughly four times more PO₄than small eukaryotes, indicating different strategies to cope with PO₄limitation. Our results underline an imbalance in the CO₂: PO₄uptake rate ratios, which may be explained by phagotrophic predation providing mixotrophic protists with their largest source of PO₄. 18S rDNA amplicon sequence analyses suggested that P‐Euk was dominated by members of green algae and dinoflagellates, the latter group commonly mixotrophic, whereas marine alveolates were the dominant NP‐Euk. Bacterivory by P‐Euk (0.9 ± 0.3 bacteria P‐Euk⁻¹h⁻¹) was comparable to values previously measured in the central North Atlantic, indicating that small mixotrophic eukaryotes likely exhibit similar predatory pressure on bacteria. Interestingly, bacterivory rates were reduced when PO₄was added during experimental incubations, indicating that feeding rate by P‐Euk is regulated by PO₄availability. This may be in response to the higher cost associated with assimilating PO₄by phagocytosis compared to osmotrophy.