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.

Long-term response of coastal macrofauna communities to de-eutrophication and sea level rise mediated habitat changes (1980s versus 2018)

“…Reduced riverine nutrient input led to de-eutrophication processes such as decreases in primary production and phytoplankton biomass or quality as well as decreasing copepod abundance in the south-eastern North Sea ( Van der Wal, 2010;Boersma et al, 2015;Capuzzo et al, 2017;Van Beusekom et al, 2017;Van Beusekom et al, 2019;Desmit et al, 2020;Xu et al, 2020). Although a parallel increasing water temperature might cause a higher phytoplankton primary production, it also causes faster turnover rates of nutrients by the microbial loop in the water column (Glibert and Mitra, 2022). This process leads to a faster nutrient depletion in the water column.…”

Planktonic prey size selection reveals an emergent keystone predator effect and niche partitioning

“…Overall, this study’s model formulation includes flexible grazing behavior based on first principles, which allowed us to investigate the impact of top-down processes in structuring the community without the level of prescription common in planktonic grazer models. The framework shown here could be used to accommodate more complex interactions and processes, such as different resource acquisition strategies and feeding modes [ 54 , 84 ] and changes in nutrient content of prey [ 24 , 85 ] or trade-offs between phytoplankton competitive ability and grazer defenses, including mixotrophic species [ 86 ]. These detailed representations of complex grazer dynamics have highlighted important, grazer mediated forcing functions that structure phytoplankton communities, which have ramifications for biogeochemical cycles.…”

Light‐dependent niche differentiation in two mixotrophic bacterivores

“…Despite our conceptual understanding on how mixotrophic nanoflagellates are able to successfully compete with their specialized competitors, at present we are largely unaware regarding the phenotypic plasticity of relevant traits within this important functional group (but see Wilken et al ., 2019). This adds up to the uncertainties of recent modelling approaches involving mixotrophy (Flynn and Mitra, 2009; Berge et al ., 2017; Leles et al ., 2018), which struggle with the insufficient empirical basis for model assumptions and parameterizations (Glibert and Mitra, 2022). In order to understand how mixotrophs compete with each other and which factors drive niche differentiation of different mixotrophs in the vertical water column, i.e.…”