Mixotrophic protists and a new paradigm for marine ecology: where does plankton research go now?

Abstract

Many protist plankton are mixotrophs, combining phototrophy and phagotrophy. Their role in freshwater and marine ecology has emerged as a major developing feature of plankton research over recent decades. To better aid discussions, we suggest these organisms are termed “mixoplankton”, as “planktonic protist organisms that express, or have potential to express, phototrophy and phagotrophy”. The term “phytoplankton” then describes phototrophic organisms incapable of phagotrophy. “Protozooplankton” describes phagotrophic protists that do not engage in acquired phototrophy. The complexity of the changes to the conceptual base of the plankton trophic web caused by inclusion of mixoplanktonic activities are such that we suggest that the restructured description is termed the “mixoplankton paradigm”. Implications and opportunities for revision of survey and fieldwork, of laboratory experiments and of simulation modelling are considered. The main challenges are not only with taxonomic and functional identifications, and with measuring rates of potentially competing processes within single cells, but with decades of inertia built around the traditional paradigm that assumes a separation of trophic processes between different organisms. In keeping with the synergistic nature of cooperative photo- and phagotrophy in mixoplankton, a comprehensive multidisciplinary approach will be required to tackle the task ahead.

The planktonic protist interactome: where do we stand after a century of research?

“…Predator-prey interactions constituted the majority of entries in PIDA. We acknowledge that separating predation into categories represents a simplified version of how predator-prey interactions are in nature, where e.g., mixotrophy is challenging old paradigms [39][40][41][42]. However, for simplicity, we here divided predation into three different categories depending on the type of prey involved: herbivory (grazing on autotrophic/chloroplast containing eukaryotic algae), bacterivory (feeding on autotrophic and/ or heterotrophic bacteria) or 'carnivory' (predation on other heterotrophic protists).…”

Caveats on the use of rotenone to estimate mixotrophic grazing in the oceans

“…Mixotrophy is a globally ubiquitous nutritional strategy 5,6 that defies the traditional auto-and heterotroph classification by combining both nutritional modes 7 and can be found among phylogenetically diverse organisms whose sizes occupy four orders of magnitude 8 . Mixotrophy is traditionally defined as the use of both inorganic and organic C-forms but can also include the incorporation of other nutrients 7 .…”

“…By definition, the passive uptake of dissolved organic C sources by some photoautotrophs such as diatoms 9 can be regarded as mixotrophy, although this trait is not useful for discriminating among trophic strategies 4 . Thus, for the purpose of clarity, this paper will hereafter only address phago-mixotrophs, which have recently been termed mixoplankton 8 . Mixoplankton can be divided according to their physiological traits of chloroplast acquisition into two major groups, the Constitutive and the Non-Constitutive mixoplankton (CM and NCM, respectively) 10 .…”

“…Indeed, mixoplankton may affect the stability of the food web 14 while enhancing predators' gross growth efficiencies and nutrient cycling 7,10 , which have consequences on models' forecasting abilities. In addition, despite knowing that mixotrophy is abundant, it is still very difficult to quantify the degree of functional mixotrophy in a given microplankton assemblage 8 . Indeed, the traditional methods for estimating primary production in aquatic environments (such as 14 C) do not disentangle the contribution of pure autotrophs and mixoplankton 8,15 .…”

“…In addition, despite knowing that mixotrophy is abundant, it is still very difficult to quantify the degree of functional mixotrophy in a given microplankton assemblage 8 . Indeed, the traditional methods for estimating primary production in aquatic environments (such as 14 C) do not disentangle the contribution of pure autotrophs and mixoplankton 8,15 . Similarly, the methods aiming at measuring the grazing and secondary production by phagotrophs fail, once again, to discriminate the contribution of mixoplankton 8 .…”