Phylogeography and Diversity Among Populations of the Toxigenic Benthic Dinoflagellate Prorocentrum From Coastal Reef Systems in Mexico

Abstract

The marine dinoflagellate genus Prorocentrum Ehrenberg comprises many species occupying primarily benthic or epiphytic habitats, particularly in tropical and sub-tropical waters. Despite concerted efforts to establish phylogenetic associations, there remain unresolved issues in defining morphospecies and membership in species complexes. The study described herein addressed the inter- and infraspecific relationships of members of the Prorocentrum lima and Prorocentrum hoffmannianum species complexes (PLSC and PHSC, respectively) by applying multivariate approaches in morphotaxonomy, molecular phylogenetics and chemodiversity to establish affinities among multiple clonal isolates. Morphotaxonomic analysis showed consistency with classical morphospecies descriptors, and high variability in cell size and dimensions, but did not challenge current species complex concepts. Phylogenetic analysis of ITS/5.8S rDNA sequences from isolates from the Gulf of California, Caribbean Sea, and Gulf of Mexico coasts compared with archived global GenBank sequences served to define five consistent clades with separation of the PLSC and PHSC. Secondary structure modeling of ITS2 rRNA variation based on compensatory base changes (CBC) was effective in resolving details of the respective species complexes and even indicated putative incipient or cryptic speciation due to potential hybridization barriers. This study represents the largest (n = 67 isolates) chemodiversity analysis of polyketide-derived toxins associated with diarrheic shellfish poisoning (DSP) from a benthic dinoflagellate genus. Relative composition of some analogs (OA, OA-D8, DTX1, DTX1a, and DTX1a-D8), including two new undescribed isomers, distinguished P. lima from P. hoffmannianum sensu lato, but without clear associations with substrate type or geographical origin. Although all P. lima and most (one exception) P. hoffmannianum were toxigenic, the total cell toxin content could not be linked at the species level. This research demonstrates that clonal chemodiversity in toxin composition cannot yet be effectively applied to define ecological niches or species interactions within local assemblages. Phylogenetic analysis of the ITS/5.8 rDNA, particularly when combined with secondary structure modeling, rather than only a comparison of LSU rDNA sequences, is a more powerful approach to identify cryptic speciation and to resolve species complexes within benthic dinoflagellate groups.

Temporal and spatial distribution of epibenthic dinoflagellates in the Kattegat-Skagerrak, NE Atlantic–Focus on Prorocentrum lima and Coolia monotis

“…foraminosum and P. cf. hoffmannianum are, however, potentially toxigenic, as producers of dinophysistoxin-1 (DTX1), other DTXs ( Cembella et al., 2021 ), unknown “fast-acting toxin” (perhaps prorocentrolide) and okadaic acid (OA) ( Aikman et al., 1993 ; Kameneva et al., 2015 ).…”

“…The genus has undergone frequent recent taxonomic revisions, leading to species reassignment of strains previously analysed for toxin content ( Chomerat et al. 2019 ; Cembella et al., 2021 ). Furthermore, early reports of cell toxicity were based on non-specific bioassays (“DSP-like symptoms”) or fluorescence-derivatization methods for DSP toxins but capable of detecting only OA and DTX1.…”

A review on marine benthic dinoflagellates in Mexico

“…In Mexican coastal waters, the most common Prorocentrum species, preliminarily identified as P. lima and P. hoffmannianum M.A. Faust, turned out to be species complexes that are not fully resolved from morphological criteria on a global basis (Cembella et al, 2021).…”

“…The validity of Prorocentrum rhathymum has caused endless discussion among researchers ever since the publication of the original description of P. mexicanum by Osorio-Tafall (1942) (Cortés-Altamirano & Sierra-Beltrán, 2003;Litaker et al, 2011;Gómez et al, 2017; for further references, see Cembella et al, 2021). Cortés-Altamirano & Sierra-Beltrán (2003) later separated these species.…”

“…A study on phylogeography and diversity of the Prorocentrum lima and P. hoffmannianum species complexes, including P. mexicanum/P. rhathymum, was published by Cembella et al (2021). In this work, 69 strains were identified to species, based on morphology and selected sequences that included the LSU, SSU and ITS regions of rDNA, with complementary base-pair analysis of secondary structures.…”