Mixotrophy stirs up our understanding of marine food webs.

Mixotrophy among planktonic eukaryotic organisms is broadly defined as the combined use of photosynthetic and heterotrophic nutrition within a single organism. The conventional view of species as either phototrophic (capable of producing energy and carbon for growth using only inorganic compounds and light) or heterotrophic (wholly dependent on preformed organic material for nutrition) is a preconception rooted in the fact that most terrestrial species can easily be divided into “plants” or “animals.” Indeed, the diversity of terrestrial organisms that combine photosynthetic and heterotrophic nutrition ismostly relegated to a dozen or so genera of carnivorous plants that capture and digest insects and other small creatures for the nutrients they contain, but also capture light energy via photosynthesis. In contrast to life on land, mixotrophic nutrition is widespread among single-celled and multicellular organisms comprising the ocean’s plankton. The ecological significance for the species that possess this behavior has not been lost on biologists who have endeavored to document and understand mixotrophy, but its importance to pelagic food-web structure and function has not yet become entrained into mathematical models of marine ecosystems. In PNAS, Ward and Follows (1) address this disparity, and provide one of the first attempts to incorporate mixotrophic nutrition into biogeochemical models of oceanic food webs. The authors use their model to estimate the impact thatmixotrophy has on food-web structure, the efficiency of carbon transfer to higher trophic levels, and the sinking of carbon into the deep ocean. Mixotrophic nutrition among planktonic species in the ocean occurs throughout many phylogenetic groups and plankton size classes, and takes a variety of forms and strategies (Fig. 1). For example, numerous species from most algal classes in the nanoplankton size class (2–20 μm) possess the ability to consume minute prey (usually bacteria), although there is great variance in the degree to which different mixotrophic species blend phototrophic and heterotrophic abilities into their nutritional repertoire (Fig. 1 A and B). Some species are nearly completely autotrophic, whereas many others are efficient predators and use photosynthesis only to prolong survival in the absence of food (2). Predatory phytoflagellates are ubiquitous in the lighted waters of marine and freshwater ecosystems. They generally constitute a significant numerical fraction of the phytoplankton community, and are an important source of bacterial mortality, particularly in oligotrophic environments (3). Many bloom-forming harmful algae are also able to consume prey. It has been speculated that mixotrophic nutrition is a factor that may explain the ability of these algae to dominate phytoplankton communities (4). Many heterotrophic dinoflagellates and ciliates in the microplankton size class (20–200 μm) exhibit mixotrophy by conducting kleptochloroplastidy, a process that involves the ingestion and digestion of algal prey, but also retention of the chloroplasts of the prey in a photosynthetically functional state (Fig. 1 D–F). The effectiveness of these species in maintaining the function of their “stolen” chloroplasts varies from the nearly autotrophic ciliateMesodinium rubrum (Fig. 1D and E) to more-transient associations in which chloroplasts lose function within a few days and must be replaced by the ingestion of additional prey. The nutrition of these mixotrophs complicates the description of food-web structure in pelagic ecosystems, but also provides endless subjects for studying the evolutionary history of organelle acquisition and stabilization in eukaryotes, a vibrant subject of research at this time (5). Intimate symbiotic associations between heterotrophic planktonic organisms and microalgae represent another form of mixed nutrition in the plankton. Symbiotic associations between ciliates (Fig. 1C), or many species of Rhizaria (Foraminifera, Acantharia, Radiolaria) (Fig. 1G and J–L) in the microand macroplankton size classes (20 μm to >1 mm) occur in all oceans but are particularly common in tropical and subtropical oceans. Rhizarian skeletal remains inmarine sediments are extensively used in paleoclimatology, and the life histories and abundances of many of these species are intimately tied to the algal species that these organisms harbor as endosymbionts within their cytoplasm (6, 7). These large “holobionts” constitute intimate and productive partnerships in which the feeding activity of the host provides energy, whereas carbon and