Margalefidinium polykrikoides

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Photo taken with DIC microscopy of a typical flagellated Margalefidinium polykrikoides with view of sulcus. Image credit: Nina McVay.

Classification

Higher Order Taxa

Eukaryota; Sar; Alveolata; Dinophyceae; Gymnodiniales; Gymnodiniaceae

Species

Margalefidinium polykrikoides
Previously known as Cochlodinium polykrikoides.

Description and Significance

M. polykrikoides is a cyst-forming, photosynthetic, and mixotrophic marine dinoflagellate— first observed in Puerto Rico (Lopez-Cortes et al 2019, Hattenrath-Lehmann et al 2019). The genus Cochlodinium was established in the late nineteenth century, and C. polykrikoides was recently reassigned to the genus Margalefidinium (Lopez-Cortes et al 2019).

Genome Structure

M. polykrikoides is ranked as the 5th largest among dinoflagellates, with a nuclear genome size estimated between 100.97 Gb -110.54 Gb via flow cytometry (Hong et al 2016). Increased amounts of gene copies, repetitive sequences, and multiple noncoding DNA elements (pseudogenes, etc.) may be responsible for this extremely large genome as well as their complex physiological and metabolic characteristics (Hong et al 2016). The nuclear state is considered a "dinokaryon" where the chromosomes are continuously condensed and fail to decondense during interphase (Fensome et al 1999).

Cell Structure, Metabolism and Life Cycle

This dinoflagellate is single-celled with an ellipsoidal shape. It measures between 25-40µm in length and has a reddish-orange pigment (Gomez et al 2017). A red, kidney-shaped eyespot facing the dorsal side of the cell allows for light detection (Gomez et al 2017). The nucleus is located anteriorly in the cell (Gomez et al 2017). M. polykrikoides has both a longitudinal flagellum which acts a rudder and a transverse flagellum which provides the main driving force which propels the dinoflagellate through the water column (Gomez et al 2017, Miyasaka et al 2004).

M. polykrikoides utilizes both organic phosphorus and nitrogen compounds but prefers NH4+ rather than NO2− and NO3-; during periods of high NH4+ concentration it has the highest growth rate (Liu et al 2021). M. polykrikoides is largely photosynthetic but during periods of nutrient scarcity, the dinoflagellate also feeds on planktonic prey to sustain the population (Aquino-Cruz et al 2020). Jeong et al reports one of the earliest recorded incidents of this dinoflagellate engulfing small phytoplankton via the sulcus (2004). In some California assemblages, high affinity for nutrient uptake is reported (Kudela et al 2008). M. polykrikoides is also capable of responding to eutrophication (Kudela et al 2008).

Reactive Oxygen Species (ROS) are created during various metabolic and biochemical processes, but is mostly found in chloroplasts, peroxisomes, and mitochondria (Aquino-Cruz et al 2020).

The lifecycle consists of a few distinct stages: resting cyst, vegetative, temporary cyst, gametes, planozygote, chains depending on nutrient availability and water temperatures (Tang and Gobler 2012). From the resting cyst, germination occurs. During the germination process, reorganization of cell contents can be observed. Then, the protoplasm transforms into a motile cell with both transverse and longitudinal flagella and the motile cell emerges from the resting cyst (Li et al 2020, Tang and Gobler 2012). The opposite was also observed, where the reorganized cell contents are released via amoeboid motion and then it transforms into a motile, “germling” cell (Li et al 2020). Once in the motile stage, a germling cell can reproduce, asexually to form vegetative cells, sexually with punitive gametes, or form chains (Liu et al 2020). The chains of 2+ cells are used to enhance motility and maintain surface positions in warm, low-viscosity water (Griffith et al 2019).

Four major points to the lifecycle were extracted from the paper by Li et al, as follows (2020). The resting cyst has a distinct germination process where a mature, motile cell is visible inside the cyst before emergence. The chain forming cells can produce temporary cysts can reproduce without asexual or sexual reproduction. Gamete fusion produces a planozygote which can be divided into single cells. M. polykrikoides sexuality is considered homothallic mating behavior.

Ecology and Pathogenesis

M. polykrikoides is a harmful algal bloom (HAB) species, responsible for red tides, that inhabits warm offshore, tropical, and subtropical waters (Liu et al 2021, Hong et al 2016). Its ideal temperature range is 23-27°C but remains viable down to temperatures as low as 12.5°C (Liu et al 2021). Culture experiments reports survival at 11°C, but viability in the field at this temperature is unknown (Kudela et al 2008). Additionally, this dinoflagellate is a euryhaline and therefore adapted to moderate salinities between 30-33 (Liu et al 2021). Blooms are associated with increased nutrients in surface coastal waters due to runoff from rivers during periods of high rainfall (Lopez-Cortes et al 2019). A study with high-throughput amplicon sequencing suggest that bloom-patches of M. polykrikoides are rich in dinoflagellates and poor in diatoms (Hattenrath-Lehmann et al 2019). A high concentration of this algae is found at the surface during daylight hours and around 20m deep during the night, allowing them to reach nutrient-rich bottom water when surface water nutrients are depleted (Griffith et al 2019).

M. polykrikoides toxicity involves reactive oxygen species (ROS), hemolytic and neurotoxic-like substances, hemagglutinins, and extracellular mucoid polysaccharide substances (Liu et al 2021, Lopez-Cortes et al 2019). Though the mechanism(s) for their toxicity is unknown, there is a suggested route of ichthyotoxicity. M. polykrikoides enters the gills normally via respiration and then the cells lyse and release their ROS and free polyunsaturated fatty acids. This causes lipid peroxidation and physiological disturbances, resulting in death (Lopez Cortes et al 2019). The ROS and hemolytic and neurotoxic-like substances are responsible for mass mortalities of marine organisms in Latin America, with an economic impact of up to 140 million USD lost in agriculture industries (Lopez-Cortes et al 2019). This dinoflagellate has been reported to affect several animals such as shrimp, coral, eels, octopuses, gastropods, crabs, and fish (Lopez-Cortes et al 2019). Reports of mass blooms are commonly reported in Asia, Europe, and North America and are now, with increasing frequency, in Latin America (Aquino-Cruz et al 2020). CuSO4 (a biocide) may be a suitable treatment for growth restriction due to its ability to significantly decrease the dinoflagellate’s photosynthetic efficiency, though it also activates mitochondrial genes and antioxidant systems which might compensate for the decreased photosynthetic efficiency (Guo et al 2016).