The mixotroph Ochromonas tuberculata may invade and suppress specialist phago- and phototroph plankton communities depending on nutrient conditions

Abstract

Mixotrophic organisms combine light, mineral nutrients, and prey as supplementary resources. Based on theoretical assumptions and field observations, we tested experimentally the hypothesis that mixotrophs may invade established plankton communities depending on the trophic status of the system, and investigated possible effects on food web structure, species diversity, and nutrient dynamics. To test our hypothesis, we inoculated the mixotrophic nanoflagellate Ochromonas tuberculata into established planktonic food webs, consisting of specialist phototrophs, specialist phagotrophs, and bacteria at different supplies of soluble inorganic nutrients and dissolved organic carbon. Oligotrophic systems facilitated the invasion of O. tuberculata in two different ways. First, the combination of photosynthesis and phagotrophy gave mixotrophs a competitive advantage over specialist phototrophs and specialist phagotrophs. Second, low nutrient supplies supported the growth of small plankton organisms that fell into the food size spectrum of mixotrophs. Conversely, high nutrient supplies prevented O. tuberculata from successfully invading the food webs. Two important conclusions were derived from our experiments. First, in contrast to a paradigm of ecology, specialization may not necessarily be the most successful strategy for survival under stable conditions. Indeed, the use of several resources with lower efficiency can be an equally, or even more, successful strategy in nature. Second, when limiting nutrients promote the growth of bacterio- and picophytoplankton, invading mixotrophs may have a habitat-ameliorating effect for higher trophic levels, gauged in terms of food quantity and quality. Using given resources more efficiently, O. tuberculata generated higher biomasses and expressed an increased nutritional value for potential planktivores, due to decreased cellular carbon to phosphorus (C:P) ratios compared to specialized plankton taxa. Our findings may help to explain why energy transfer efficiency between phytoplankton and higher trophic levels is generally higher in oligotrophic systems than in nutrient rich environments.

Coexistence of mixotrophs, autotrophs, and heterotrophs in planktonic microbial communities

“…In common with previous work on mixotrophs, we assume that they are less competitive than specialist zooflagellates for bacterial prey, and less competitive than specialist algae for inorganic resources. This assumption is consistent with observations that mixotrophs tend to dominate over specialist nutritional types only under limitation by multiple resources that favors generalists (Rothhaupt, 1996;Tittel et al, 2003;Katechakis and Stibor, 2006).…”

Chrysophytes and other protists in High Arctic lakes: molecular gene surveys, pigment signatures and microscopy

“…Another potential adaptation to low nutrients and periodic light limitation is phagotrophic mixotrophy, whereby nutrients and energy can be obtained from bacterial prey, circumventing direct energy dependency on solar radiation and the reliance on dissolved inorganic nutrients (Raven 2009). A number of studies have documented that phototrophic chrysophytes prey on bacterial or algal cells (Bird and Kalff 1986;Rothhaupt 1996;Katechakis and Stibor 2006). Hence, when nutrients are scarce at the end of the growing season, as in Lake A (Veillette et al 2011), chrysophyte mixotrophy would be favoured.…”

Mixotrophic Activity and Diversity of Antarctic Marine Protists in Austral Summer

“…When abundant, mixotrophs likely are an important food source for higher trophic levels. Mixotrophs generally have lower carbon to nutrient ratios (C:N, C:P) than strict phototrophs (Katechakis and Stibor, 2006), and protists with low ratios are considered to be better quality food for higher trophic levels (Sterner, 1990;Hessen et al, 2002;Bukovinszky et al, 2012). The quality of phytoplankton food could impact zooplankton growth and reproduction, which in turn would affect fish and other marine vertebrates.…”