On the Strategy of "Eating Your Competitor": A Mathematical Analysis of Algal Mixotrophy

Abstract

Recent experimental evidence indicates the importance in some pelagic systems of mixotrophic protists that combine photosynthetic ability with the ability to ingest bacteria. If both bacteria and phytoplankton are mineral nutrient limited, this should provide the mixotrophs with the double benefit of combining removal of their competitor with ingestion of the limiting nutrient in pelleted form. It is the objective of this study to expand the classical theories of competition and predation to explore the effect on the microbial food web of one trophic group possessing both strategies. In a chemostat scenario, we analyzed the two—species situation of a mixotroph preying on mineral—nutrient—limited bacteria, and also the situations when the mixotroph in addition has to compete with specialized photoautotrophic and phagotrophic protists, each superior to the mixotroph in their specialized nutritional modes. In the mixotroph—bacteria relationship, somewhat paradoxically, high predatory abilities will reduce the quantitative importance of predation in the mixotroph's nutrition. The reason is a strong reduction in prey abundance, allowing the mixotroph to survive as a photoautotroph despite its low competitive ability. In the three—species case with mixotrophs, bacteria, and specialized phagotrophs, it is shown that the mixotroph can compensate for a "price" paid in reduced affinity for bacterial prey by a sufficiently high affinity for mineral nutrients. In the other three—species case where the mixotroph has to compete with a specialized photoautotroph, the situation is more complex; there is an optimum value for the mixotroph's predatory ability at which mixotroph biomass is maximized. In the general situation with all four species (bacteria, mixotrophs, and specialized auto— and phagotrophs) potentially present, different mixotrophic strategies will alter the equilibrium composition of the consortium, with the mixotroph being most successful with a high affinity for nutrients and an intermediate affinity for bacteria. In the simple form used here, the model predicts no equilibrium with all four species simultaneously present. The theory is in principle directly applicable to laboratory experimentation.

The role of mixotrophic protists in the biological carbon pump

“…In the simulations presented here, the MNFs did not win by eating their competitors (eating the HNFs or nonphagotrophic microalgae; cf. Thingstad et al, 1996). Instead, they succeeded through a combination of cooperative nutrition and, especially in the low-P simulations, through having a disadvantageous stoichiometric content (i.e.…”

“…they are auxotrophic; Croft et al, 2006). Furthermore, osmotrophy alone does not have a direct powerful impact on trophic dynamics, as does the act of killing and engulfing a prey item through phagocytosis (Thingstad et al, 1996).…”

Modelling the plankton groups of the deep, peri-alpine Lake Bourget

“…Following many decades of dichotomous classi cation of planktonic organisms as`autotrophs' and`heterotrophs' (Flynn et al, 2012), importance of mixotrophy in ecosystem functioning has been increasingly recognized (Mitra et al, 2014, and references therein). Mixotrophy has been addressed mainly by theoretical work so far (e.g., Thingstad et al, 1997;Flynn and Mitra, 2009;Crane and Grover, 2010;Berge et al, 2017). The recent work of Ward and Follows (2016) constitutes the rst example where mixotrophy is resolved in a global ocean model.…”

Modeling Plankton Mixotrophy: A Mechanistic Model Consistent with the Shuter-Type Biochemical Approach

“…Mitra and Flynn (2010) have indeed shown that descriptions integrating physiological processes, with some degree of feedback to modulate the processes of phototrophy and heterotrophy, are needed to properly represent the qualitative behavior of mixotrophs. Among existing mixotrophic models, only those of Stickney et al (2000) and the "perfect beast" of Flynn and Mitra (2009) take the interactions between the two trophic modes into account; the others rely on additive descriptions of phototrophy and heterotrophy (Thingstad et al, 1996;Baretta-Bekker et al, 1998;Jost et al, 2004;Hammer and Pitchford, 2005;Crane and Grover, 2010;Ward et al, 2011;Våge et al, 2013).…”

“…Most interest has been leveled at the potential impact of mixotrophs on the microbial food web structure and functioning, and the conditions under which mixotrophs may likely coexist with strict phototrophs and heterotrophs (Thingstad et al, 1996;BarettaBekker et al, 1998;Stickney et al, 2000;Jost et al, 2004;Hammer and Pitchford, 2005;Hood et al, 2006;Flynn and Mitra, 2009;Crane and Grover, 2010;Ward et al, 2011;Våge et al, 2013). By far the greater effort has been applied to CM organisms.…”