Life Cycle Stages and Evidence of Sexual Reproduction in the Marine DinoflagellateProrocentrum minimum(Dinophyceae, Prorocentrales)

Abstract

Prorocentrum minimum is a potentially toxic marine dinoflagellate that often forms massive blooms in estuarine and coastal sea waters. In this study, the life cycle of P. minimum was investigated and sexual reproduction in culture was described for the first time. Morphology of the mitotic stages was revised and several distinguishing features from sexual steps were described. The sexual reproductive stages were observed in the stationary culture and compared with a well‐studied closely related species, Prorocentrum micans. Prorocentrum minimum has a haplontic life cycle and homothallic sexual process. The gametes were isogamous and morphologically indistinguishable from the vegetative cells. Unlike P. micans, P. minimum isogametes fused, but did not conjugate, partially reorganizing their cell coverings. Newly formed planozygotes were distinguished by their irregular shape and a large asymmetrically located nucleus. No long‐term resting cyst stages (hypnozygotes) were documented. The late planozygotes underwent meiosis and formed tetrads of cells. The second meiotic division could be delayed or arrested in one of the daughter nuclei leading to formation of trinucleate cells with three pairs of flagella. So, similar to P. micans, P. minimum may have two possible scenarios of sexual division: (a) formation of a four‐cell stage through two successive divisions or (b) asynchronous divisions of the zygote. Changes in the DNA content were confirmed by quantitative image cytometry.

Direct Evidence Of Sex In Symbiodiniaceae And A Hypothesis About Meiosis

“…This first description of a complete nuclear progression compatible with sex in Symbiodiniaceae, ranging from the identification of putative zygotes to the formation of dyads, triads and tetrads, aligns with a meiotic two-step process already described in other dinoflagellates (e.g. 29,45,46 ). Below, we highlight key DNA content and cell morphology observations that allow us to establish differences between mitosis and meiosis in Symbiodiniaceae cells, compare our hypothesis for sex in Symbiodiniaceae to the sexual stages reported in other dinoflagellate species, and highlight outstanding questions regarding the conditions that promote Symbiodiniaceae sex.…”

“…1B.2); this reproductive strategy has been observed in most studied dinoflagellates. For example, Prorocentrum micans and Prorocentrum minimum form tetrads as a final meiotic product 29 . Additionally, asynchronous divisions of the zygote in these Prorocentrum species also lead to the formation of triads 29 .…”

“…For example, Prorocentrum micans and Prorocentrum minimum form tetrads as a final meiotic product 29 . Additionally, asynchronous divisions of the zygote in these Prorocentrum species also lead to the formation of triads 29 . It should be noted that some free-living dinoflagellates (e.g., members of the genus Alexandrium) produce chains of cells during two consecutive mitotic divisions.…”

“…Despite these advances, sexuality remains difficult to identify in most dinoflagellate species due to (i) morphological similarities between sexual and vegetative stages; and (ii) the potential for co-occurrence of 2C DNA content stages derived from both mitosis (haploid) and gamete fusion (diploid) within the same population of cells. Given this, a general consensus has emerged that the detection of a 4-fold DNA content stage, which is formed during meiosis (but not mitosis), is key to identifying sex in dinoflagellates [25][26][27][28][29] .…”

Putative Meiotic Toolkit in the Dinoflagellate Prorocentrum cordatum: Additional Evidence for Sexual Process from Transcriptome

“…Prorocentrum minimum (Pavillard) Schiller) (Velikova and Larsen 1999) was long considered to reproduce only asexually (Honsell and Talarico 1985;Lebour 1925). We recently described the sexual process in the life cycle of this organism (Berdieva et al 2020).…”