Search

© 2019 John Wiley & Sons Ltd Aim: Most protist plankton are mixotrophic, with potential to engage in photoautotrophy and phagotrophy; however, the ecology of these organisms has been misdiagnosed for over a century. A large proportion of these organisms are constitutive mixotrophs (CMs), with an innate ability to photosynthesize. Here, for the first time, an analysis is presented of the biogeography of CMs across the oceans. Location: Global marine ecosystems. Time period: 1970–2018. Major taxa studied: Marine planktonic protists. Methods: Records for CM species, primarily from the Ocean Biogeographic Information System (OBIS), were grouped by taxonomy and size to evaluate sampling efforts across Longhurst's oceanic provinces. Biases were evaluated through nonparametric tests and multivariate analysis. Biogeographies of CMs from OBIS data were compared with data from studies that specifically targeted these organisms. Results: Constitutive mixotrophs of different taxonomic groups, across all size ranges, are ubiquitous. However, strong database biases were detected with respect to organism size, taxonomic groups and region. A strong bias was seen towards dinophytes. Species < 20 µm, especially non-dinophytes, were least represented, with their recorded distribution limited to coastal regions and to temperate and polar seas. Studies specifically targeting these organisms revealed their distribution to be much wider. Such biases are likely to have occurred owing to a failure to capture and correctly identify these organisms in routine sampling protocols. Main conclusions: Constitutive mixotrophs are dominant members of organisms traditionally termed “phytoplankton”. However, lack of routine protocols for measuring phagotrophy in “phytoplankton” protists has led to widespread misrepresentation of the fundamental nature of marine planktonic primary producers; most express both “animal-like” and “plant-like” nutrition. Our results have implications for studies of the glo

© 2017 The Author(s) Published by the Royal Society. All rights reserved. This first comprehensive analysis of the global biogeography of marine proti-stan plankton with acquired phototrophy shows these mixotrophic organisms to be ubiquitous and abundant; however, their biogeography differs markedly between different functional groups. These mixotrophs, lacking a constitutive capacity for photosynthesis (i.e. non-constitutive mixotrophs, NCMs), acquire their phototrophic potential through either integration of prey-plastids or through endosymbiotic associations with photosynthetic microbes. Analysis of field data reveals that 40–60% of plankton traditionally labelled as (non-phototrophic) microzooplankton are actually NCMs, employing acquired phototrophy in addition to phagotrophy. Specialist NCMs acquire chloroplasts or endosymbionts from specific prey, while generalist NCMs obtain chloroplasts from a variety of prey. These contrasting functional types of NCMs exhibit distinct seasonal and spatial global distribution patterns. Mixotrophs reliant on ‘stolen’ chloroplasts, controlled by prey diversity and abundance, dominate in high-biomass areas. Mixotrophs harbouring intact symbionts are present in all waters and dominate particularly in oligotrophic open ocean systems. The contrasting temporal and spatial patterns of distribution of different mixotroph functional types across the oceanic provinces, as revealed in this study, challenges traditional interpretations of marine food web structures. Mixotrophs with acquired phototrophy (NCMs) warrant greater recognition in marine research.

The traditional view of the planktonic food web describes consumption of inorganic nutrients by photoautotrophic phytoplankton, which in turn supports zooplankton and ultimately higher trophic levels. Pathways centred on bacteria provide mechanisms for nutrient recycling. This structure lies at the foundation of most models used to explore biogeochemical cycling, functioning of the biological pump, and the impact of climate change on these processes. We suggest an alternative new paradigm, which sees the bulk of the base of this food web supported by protist plankton communities that are mixotrophic-combining phototrophy and phagotrophy within a single cell. The photoautotrophic eukaryotic plankton and their heterotrophic microzooplankton grazers dominate only during the developmental phases of ecosystems (e.g. spring bloom in temperate systems). With their flexible nutrition, mixotrophic protists dominate in more-mature systems (e.g. temperate summer, established eutrophic systems and oligotrophic systems); the more-stable water columns suggested under climate change may also be expected to favour these mixotrophs. We explore how such a predominantly mixotrophic structure affects microbial trophic dynamics and the biological pump. The mixotroph-dominated structure differs fundamentally in its flow of energy and nutrients, with a shortened and potentially more efficient chain from nutrient regeneration to primary production. Furthermore, mixotrophy enables a direct conduit for the support of primary production from bacterial production. We show how the exclusion of an explicit mixotrophic component in studies of the pelagic microbial communities leads to a failure to capture the true dynamics of the carbon flow. In order to prevent a misinterpretation of the full implications of climate change upon biogeochemical cycling and the functioning of the biological pump, we recommend inclusion of multi-nutrient mixotroph models within ecosystem studies. © 2014 Author(s).

The classic portrayal of plankton is dominated by phytoplanktonic primary producers and zooplanktonic secondary producers. In reality, many if not most plankton traditionally labelled as phytoplankton or microzooplankton should be identified as mixotrophs, contributing to both primary and secondary production. Mixotrophic protists (i.e. single-celled eukaryotes that perform photosynthesis and graze on particles) do not represent a minor component of the plankton, as some form of inferior representatives of the past evolution of protists; they represent a major component of the extant protist plankton, and one which could become more dominant with climate change. The implications for this mistaken identification, of the incorrect labelling of mixotrophs as " phytoplankton" or "microzooplankton", are great. It extends from the (mis)use of photopigments as indicators of primary production performed by strict photoautotrophs rather than also (co)locating mixotrophic activity, through to the inadequacy of plankton functional type descriptions in models (noting that mixotrophic production in the individual organism is not a simple sum of phototrophy and heterotrophy). We propose that mixotrophy should be recognized as a major contributor to plankton dynamics, with due effort expended in field and laboratory studies, and should no longer be side-lined in conceptual food webs or in mathematical models. © 2012 The Author 2012. Published by Oxford University Press. All rights reserved.

The haptophyte PrymnesiuM parvum Carter is toxic and frequently responsible for harmful algal blooms in coastal waters. It is a mixotrophic species having the capability to feed on various planktonic microorganisms. It is frequently suggested that mixotrophic algae may obtain inorganic nutrients through phagotrophy and that nutrient depletion should then lead to increased food uptake. To study this, we investigated the feeding activity of P. parvum in semi-continuous, nutrient-limited cultures, using the cryptophyte Rhodomonas baltica as prey. P. parvum showed to be an active predator under all conditions investigated. After 2 h of incubation with prey, 40% of P. parvum cells were either feeding or contained recently formed food vacuoles. However, under the conditions used, no difference in feeding activity was found between treatments. On the contrary, the feeding activity was similar in P. parvum cultures that had been grown under N-limiting, P-limiting, N- and P-limiting, as well as under nutrient-replete conditions. It cannot be excluded that P. parvum under limiting nutrient conditions may acquire nutrients to be used in photosynthetic growth through phagotrophy. It is evident, however, that the species also feeds when inorganic nutrients are present in concentrations sufficient to support maximum phototrophic growth.