From webs, loops, shunts, and pumps to microbial multitasking: Evolving concepts of marine microbial ecology, the mixoplankton paradigm, and implications for a future ocean

Abstract

Emerging knowledge of mixoplankton—ubiquitous microbes that employ phototrophy and phagotrophy synergistically in one cell—reshapes our knowledge of the flow of materials and energy, with wide-reaching impacts on marine productivity, biodiversity, and sustainability. Conceptual models of microbial interactions have evolved from food-chains, where carbon-fixing phytoplankton are conceived as being grazed solely by zooplankton that, in turn, support fisheries and higher trophic levels, to microbial webs, loops, and shunts, as knowledge about abundance, activity, and roles of marine microbial organisms—as well as the complexity of their interactions—has increased. In a future world, plankton that depend on a single strategy for acquiring nutrition (photo-autotrophy or phago-heterotrophy) may be disadvantaged with increasing temperatures and ocean acidification impacting vital rates, thermal stratification decreasing water column nutrient exchange, and anthropogenic pollution shifting amounts, forms, and proportions of nutrients. These conditions can lead to stoichiometric imbalances that may promote mixoplanktonic species with an increasing likelihood of harmful blooms. Such changes in plankton species composition alters the interconnectivity of oceanic microbes with direct consequences on biogeochemical cycling, trophic dynamics, and ecosystem services. Here, the implications of the mixoplankton paradigm relative to traditional concepts of microbial oceanography in a globally-changing, anthropogenically-impacted world are explored.