Plasticity and Multiplicity of Trophic Modes in the Dinoflagellate Karlodinium and Their Pertinence to Population Maintenance and Bloom Dynamics

Abstract

As the number of mixotrophic protists has been increasingly documented, “mixoplankton”, a third category separated from the traditional categorization of plankton into “phytoplankton” and “zooplankton”, has become a new paradigm and research hotspot in aquatic plankton ecology. While species of dinoflagellates are a dominant group among all recorded members of mixoplankton, the trophic modes of Karlodinium, a genus constituted of cosmopolitan toxic species, were reviewed due to their representative features as mixoplankton and harmful algal blooms (HABs)-causing dinoflagellates. Among at least 15 reported species in the genus, three have been intensively studied for their trophic modes, and all found to be phagotrophic. Their phagotrophy exhibits multiple characteristics: (1) omnivority, i.e., they can ingest a variety of preys in many forms; (2) flexibility in phagotrophic mechanisms, i.e., they can ingest small preys by direct engulfment and much bigger preys by myzocytosis using a peduncle; (3) cannibalism, i.e., species including at least K. veneficum can ingest the dead cells of their own species. However, for some recently described and barely studied species, their tropical modes still need to be investigated further regarding all of the above-mentioned aspects. Mixotrophy of Karlodinium plays a significant role in the population dynamics and the formation of HABs in many ways, which thus deserves further investigation in the aspects of physiological ecology, environmental triggers (e.g., levels of inorganic nutrients and/or presence of preys), energetics, molecular (genes and gene expression regulations) and biochemical (e.g., relevant enzymes and signal molecules) bases, origins, and evaluation of the advantages of being a phagotroph.

Mucus-Trap-Assisted Feeding Is a Common Strategy of the Small Mixoplanktonic Prorocentrum pervagatum and P. cordatum (Prorocentrales, Dinophyceae)

“…Prior to the direct observations of Prorocentrum peduncular feeding by Larsson et al (2022), and in the present study, Transmission Electron Microscopy (TEM) of the intracellular microtubular baskets within various species of Prorocentrum [ 32 , 33 ] including P. cordatum [ 29 , 34 ] suggested the capability of peduncular feeding in this genus. More observations are required to confirm if direct engulfment, as described by Jeong et al [ 7 ] for four planktonic Prorocentrum species, and thus multiple feeding mechanisms, exists within the Prorocentrales (similar to the diversity in Karlodinium [ 35 ]), or if peduncle feeding is the predominant form also for other species of Prorocentrum . Accordingly, for our in silico investigations we assumed that some Prorocentrum cells are able to feed without using a mucus trap to physically restrain their prey, though it is not clear from our work that such an event can actually occur for P. pervagatum and P. cordatum .…”

Review of Harmful Algal Blooms (HABs) Causing Marine Fish Kills: Toxicity and Mitigation

“…It was previously categorized as Gymnodinium or Gyrodinium until the now-famous genus was identified. This genus has 15 recognized species as of 2020, of which 6 species have been proven to be toxic (K. armiger, K. azanzae, K. conicum, K. corsicum, K. digitatum, and K. veneficum) [93]. Notably, K. veneficum has been linked to innumerable HAB events and mass fish kills [94][95][96].…”

Taxonomy and Ecology of Marine Algae

“…Yang et al [14] reviewed Karlodinium due to their representative features as mixoplankton and harmful algal blooms (HABs)-causing dinoflagellates. Their phagotrophy exhibits multiple characteristics: (1) omnivority, i.e., they can ingest a variety of preys in many forms; (2) flexibility in phagotrophic mechanisms, i.e., they can ingest small preys by direct engulfment and much bigger preys by myzocytosis using a peduncle; (3) cannibalism, i.e., species including at least K. veneficum can ingest the dead cells of their own species.…”