Morphology and molecular phylogeny of epizoic araphid diatoms on marine zooplankton, including Pseudofalcula hyalina gen. & comb. nov. (Fragilariophyceae, Bacillariophyta)

Abstract

Some diatoms are able to colonize as epibionts on their potential zooplankton predators. Here, we report Pseudohimantidium pacificum living on the copepod Corycaeus giesbrechti and as a new finding on Oithona nana, Protoraphis atlantica living on the copepod Pontellopsis brevis, Protoraphis hustedtiana on the cypris larvae of barnacles, and Falcula hyalina on the copepod Acartia lilljeborgii. The epizoic diatoms were able to grow as free-living forms under culture conditions. Pseudohimantidium pacificum and P. atlantica appeared as the most derived species from their benthic diatom ancestors. The mucilage pad or stalk of the strains of these species showed important morphological distinction when compared with their epizoic forms. Barnacle larvae explore benthic habitats before settlement, and epibiosis on them is an example where P. hustedtiana profits from the host behavior for dispersal of its benthic populations. Molecular phylogenies based on the SSU rRNA and RuBisCO large subunit (rbcL) gene sequences revealed F. hyalina as an independent lineage within the Fragilariales (Tabularia, Catacombas, and others), consistent with its morphological distinction in the low number of rows (≤6) in the ocellulimbus, among other features. We propose the transfer of F. hyalina to the genus Pseudofalcula gen. nov. Molecular phylogeny suggests a single order for the members of the Cyclophorales and the Protoraphidales, and that the epibioses of araphid diatoms on marine zooplankton have been independently acquired several times. These clades are constituted of both epizoic and epiphytic/epilithic forms that evidence a recent acquisition of the epizoic modus vivendi.

Symbioses of Ciliates (Ciliophora) and Diatoms (Bacillariophyceae): Taxonomy and Host–Symbiont Interactions

“…Hernández-Becerril [51] reported that the valves of C. tetrastichon were less heavily silicified than the other member of the subgenus Phaeoceros. A reduction of the silicification has been also observed in other epizoic species as compared with benthic counterparts [31].…”

“…The live plankton concentrate was scanned in settling chambers with inverted microscopes. Detailed methods of collection and observations are described in Gómez et al [22,31]. References were used for the identification of diatoms [10], cyanobacteria [12], naked ciliates [21,22,32], and tintinnid ciliates based on the lorica features [3,4].…”

“…The diatoms of the order Fragilariales (=Thalassionematales), Licmophorales and Protoraphiales (=Cyclophorales) are phylogenetically closely related and contain most of the known genera of araphid epizoic diatoms (Licmophora, Protoraphis, Pseudofalcula, Pseudohimantidium, and Synedra) and also the free-floating genus Thalassionema [31]. The etymology of the name Fragilariopsis suggests an affinity with the araphid order Fragilariales.…”

“…Laboratory experiments are difficult due to the lack of these symbiotic ciliates in culture [13] and even some of the diatoms, therefore, hypotheses on the ecology of the consortia are speculative. Attempts to culture Chaetoceros dadayi, C. tetrastichon, and C. coarctatus have been unsuccessful, whereas other epizoic diatoms have been cultured with the same method [31]. The chains of F. doliolus modified their curvature between the free-living and symbiotic forms (Figure 1o-s).…”

Effects of Epibiotic Diatoms on the Productivity of the Calanoid Copepod Acartia tonsa (Dana) in Intensive Aquaculture Systems

“…However, occurrences of microalga epibiosis on copepods were mostly documented with particular focus on epibiont morphology, phylogeny, and distribution (Carman and Dobbs, 1997;Fernandes and Calixto-Feres, 2012;Li et al, 2014;Gómez et al, 2018;Nayak et al, 2021). The impacts of algal epibiosis on copepod reproduction were rarely investigated as yet.…”