Small pigmented eukaryotes play a major role in carbon cycling in the P‐depleted western subtropical North Atlantic, which may be supported by mixotrophy

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 CO2 than picocyanobacteria, accounting for roughly half of the volumetric CO2 fixation by the microbial phytoplankton, or a third of the total primary production. Cell‐specific PO4 assimilation 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 PO4 than small eukaryotes, indicating different strategies to cope with PO4 limitation. Our results underline an imbalance in the CO2 : PO4 uptake 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−1 h−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 PO4 was added during experimental incubations, indicating that feeding rate by P‐Euk is regulated by PO4 availability. This may be in response to the higher cost associated with assimilating PO4 by phagocytosis compared to osmotrophy.

Seasonal and Geographical Transitions in Eukaryotic Phytoplankton Community Structure in the Atlantic and Pacific Oceans

“…Our findings support the outcomes of models that a synergistic coupling exists between prey ingestion for nutrients, and photosynthetic acquisition of carbon and energy, which enables mixotrophs to be successful in stable oligotrophic gyres (Duhamel et al, 2019;Edwards, 2019). Mixotrophic behavior also has consequences when assimilated into global food web models, shifting biomass to larger size classes and thereby enhancing sinking carbon flux (Ward and Follows, 2016).…”

“…The phylogenetic affiliations of predatory mixotrophs remain poorly characterized, especially in offshore oligotrophic waters. Identification based on FISH showed high rates of bacterivory by haptophytes in the Mediterranean Sea, as well as cryptophytes and dinoflagellates (Unrein et al, 2014), the latter two being well recognized mixotrophic groups, including in oligotrophic ocean regions (Stoecker, 1999;Duhamel et al, 2019). By the same approach, haptophytes and chrysophytes (another stramenopile lineage) were found to feed on Prochlorococcus in the Atlantic subtropical gyres (Hartmann et al, 2013).…”

“…The relative importance of predatory mixotrophs may vary with depth, for example a Sargasso Sea study found that 50% of photosynthetic nanoflagellates consumed prey in the surface mixed layer, while only 0.5% ingested prey in the DCM (Arenovski et al, 1995). Further, based on modeling studies, the combination of high light intensities and low availability of dissolved nutrients (as would occur in the surface) has been suggested to favor mixotrophs over photoautotrophic algae in oligotrophic surface waters (Duhamel et al, 2019;Edwards, 2019).…”

Exploring the Trophic Spectrum: Placing Mixoplankton Into Marine Protist Communities of the Southern North Sea

“…We determined that in inorganic nutrient-depleted, seasonally stratified, predominantly offshore environments, mixoplankton periodically constitute up to 25% (classification A -documented mixoplankton), over 75% (classification B -proven mixoplankton), or around 50% (classification C -environmentally-defined mixoplankton) of the protist community. An oligotrophic environment is clearly associated with mixoplankton (Troost et al, 2005;Hartmann et al, 2012;Stoecker and Lavrentyev, 2018;Duhamel et al, 2019;Livanou et al, 2019). However, comparing the determined percentages with current literature is more difficult.…”

“…Most of these studies did not include the role of mixoplankton. However, there have been various local (e.g., Stoecker et al, 1989;Löder et al, 2012;Duhamel et al, 2019) and even specific global (Harrison et al, 2011) studies of certain mixoplankton groups. More recently, Leles et al (2017Leles et al ( , 2019 and Faure et al (2019) presented the first comprehensive analyses on the global biogeography of mixoplankton.…”