Newly identified diversity of Dinomycetaceae (Rhizophydiales, Chytridiomycota), a family of fungal parasites of marine dinoflagellates.

We identified two new parasite species of Chytridiomycota isolated during blooms of the dinoflagellate Alexandrium minutum in the coastal Mediterranean Sea. Light and electron microscopy together with molecular characterization of the nuclear 18S, ITS, and 28S rDNA regions led to their identification as two new species, Dinomyces gilberthii and Paradinomyces evelyniae, both belonging to the family Dinomycetaceae, order Rhizophydiales. Dinomyces gilberthii differs from the previously described D. arenysensis by the presence of discharge papillae and the development of a drop-shaped sporangium. Paradinomyces evelyniae differs from the previously described P. triforaminorum by the prominent lipid globule present in early sporangia and by the pointed end producing a rhizoid. The two chytrids differed in their geographical distribution. Dinomyces gilberthii was detected in several Mediterranean habitats, including harbours and beaches, and was particularly prevalent during summer dinoflagellate blooms. Its widespread occurrence in coastal ecosystems suggested a high level of adaptability to this environment. Paradinomyces evelyniae had a more restricted distribution in the coastal-marine environment, occurring in harbour sediments and only occasionally in the water column during winter and early spring. Paradinomyces evelyniae has previously been detected in the Baltic Sea, suggesting that its distribution encompasses contrasting coastal environments, although its presence is rare.

The succession of epiphytic microalgae conditions fungal community composition: how chytrids respond to blooms of dinoflagellates.

This study aims to investigate the temporal dynamics of the epiphytic protist community on macroalgae, during the summer months, with a specific focus on fungi, and the interactions between zoosporic chytrid parasites and the proliferation of the dinoflagellates. We employed a combination of environmental sequencing techniques, incubation of natural samples, isolation of target organisms and laboratory experiments. Metabarcoding sequencing revealed changes in the dominant members of the epiphytic fungal community. Initially, fungi comprised < 1% of the protist community, mostly accounted for by Basidiomycota and Ascomycota, but with the emergence of Chytridiomycota during the mature phase of the biofilm, the fungal contribution increased to almost 30%. Chytridiomycota became dominant in parallel with an increase in the relative abundance of dinoflagellates in the community. Microscopy observations showed a general presence of chytrids following the peak proliferation of the dinoflagellate Ostreopsis sp., with the parasite, D. arenysensis as the dominant chytrid. The maximum infection prevalence was 2% indicating host-parasite coexistence. To further understand the in-situ prevalence of chytrids, we characterised the dynamics of the host abundance and prevalence of chytrids through co-culture. These laboratory experiments revealed intraspecific variability of D. arenysensis in its interaction with Ostreopsis, exhibiting a range from stable coexistence to the near-extinction of the host population. Moreover, while chytrids preferentially parasitized dinoflagellate cells, one of the strains examined displayed the ability to utilize pollen as a resource to maintain its viability, thus illustrating a facultative parasitic lifestyle. Our findings not only enrich our understanding of the diversity, ecology, and progression of epiphytic microalgal and fungal communities on Mediterranean coastal macroalgae, but they also shed light on the presence of zoosporic parasites in less-explored benthic habitats.

Cryo-electron microscopy of extracellular vesicles associated with the marine toxic dinoflagellate Alexandrium minutum.

Extracellular Vesicles (EVs) are likely an important strategy of transport and communication in marine microbial community. Their isolation and characterization from axenic culture of microbial eukaryotes represents a technological challenge not fully solved. Here, for the first time, we isolated EVs from a near-axenic culture of the toxic dinoflagellate Alexandrium minutum. Pictures of the isolated vesicles were done with Cryo TEM (Cryogenic Transmission Electron Microscopy). Based on their morphotype the EVs were clustered in five major groups (rounded, rounded electron-dense, lumen electron-dense, double and irregular) and each EV was measured resulting in an average size of 0.36 µm of diameter. Taking in account that in prokaryotes it has been demonstrated that EVs play an important role in the mechanism of toxicity, this descriptive work aims to be the first step to study the possible role of EVs in the toxicity of dinoflagellates.

The new chytridiomycete Paradinomyces triforaminorum gen. et sp. nov. co-occurs with other parasitoids during a Kryptoperidinium foliaceum (Dinophyceae) bloom in the Baltic Sea.

A new chytrid genus and species was isolated and cultured from samples obtained in the Baltic Sea during a dinoflagellate bloom event. This species is characterized by having a spherical sporangium without papillae and zoospores of 2-3 µm in diameter that are released through 3 discharge pores. Molecular phylogeny based on ribosomal operon showed its sister position to the Dinomyces cluster in Rhizophydiales. Zoospores lack fenestrated cisternae but contain a paracrystalline inclusion, found in a Rhizophydiales representative for the first time. Additionally, the kinetid features are uncommon for Rhizophydiales and only observed in Dinomyces representatives so far. These morphological features and its phylogenetic relationships justify the description of the new genus and speciesParadinomyces triforaminorum gen. nov. sp. nov. belonging to the family Dinomycetaceae. The chytrid was detected during a high-biomass bloom of the dinoflagellate Kryptoperidinium foliaceum. Laboratory experiments suggest this species is highly specific and demonstrate the impact it can have on HAB development. The chytrid co-occurred with three other parasites belonging to Chytridiomycota (Fungi) and Perkinsea (Alveolata), highlighting that parasitic interactions are common during HABs in brackish and marine systems, and these multiple parasites compete for similar hosts.

Dinoflagellate hosts determine the community structure of marine Chytridiomycota: Demonstration of their prominent interactions.

The interactions of parasitic fungi with their phytoplankton hosts in the marine environment are mostly unknown. In this study, we evaluated the diversity of Chytridiomycota in phytoplankton communities dominated by dinoflagellates at several coastal locations in the NW Mediterranean Sea and demonstrated the most prominent interactions of these parasites with their hosts. The protist community in seawater differed from that in sediment, with the latter characterized by a greater heterogeneity of putative hosts, such as dinoflagellates and diatoms, as well as a chytrid community more diverse in its composition and with a higher relative abundance. Chytrids accounted for 77 amplicon sequence variants, of which 70 were found exclusively among different blooming host species. The relative abundance of chytrids was highest in samples dominated by the dinoflagellate genera Ostreopsis and Alexandrium, clearly indicating the presence of specific chytrid communities. The establishment of parasitoid-host co-cultures of chytrids and dinoflagellates allowed the morphological identification and molecular characterization of three species of Chytridiomycota, including Dinomyces arenysensis, as one of the most abundant environmental sequences, and the discovery of two other species not yet described.

Long-term patterns of an interconnected core marine microbiota.

BACKGROUND: Ocean microbes constitute ~ 70% of the marine biomass, are responsible for ~ 50% of the Earth's primary production and are crucial for global biogeochemical cycles. Marine microbiotas include core taxa that are usually key for ecosystem function. Despite their importance, core marine microbes are relatively unknown, which reflects the lack of consensus on how to identify them. So far, most core microbiotas have been defined based on species occurrence and abundance. Yet, species interactions are also important to identify core microbes, as communities include interacting species. Here, we investigate interconnected bacteria and small protists of the core pelagic microbiota populating a long-term marine-coastal observatory in the Mediterranean Sea over a decade. RESULTS: Core microbes were defined as those present in > 30% of the monthly samples over 10 years, with the strongest associations. The core microbiota included 259 Operational Taxonomic Units (OTUs) including 182 bacteria, 77 protists, and 1411 strong and mostly positive (~ 95%) associations. Core bacteria tended to be associated with other bacteria, while core protists tended to be associated with bacteria. The richness and abundance of core OTUs varied annually, decreasing in stratified warmers waters and increasing in colder mixed waters. Most core OTUs had a preference for one season, mostly winter, which featured subnetworks with the highest connectivity. Groups of highly associated taxa tended to include protists and bacteria with predominance in the same season, particularly winter. A group of 13 highly-connected hub-OTUs, with potentially important ecological roles dominated in winter and spring. Similarly, 18 connector OTUs with a low degree but high centrality were mostly associated with summer or autumn and may represent transitions between seasonal communities. CONCLUSIONS: We found a relatively small and dynamic interconnected core microbiota in a model temperate marine-coastal site, with potential interactions being more deterministic in winter than in other seasons. These core microbes would be essential for the functioning of this ecosystem over the year. Other non-core taxa may also carry out important functions but would be redundant and non-essential. Our work contributes to the understanding of the dynamics and potential interactions of core microbes possibly sustaining ocean ecosystem function.

Seasonal niche differentiation among closely related marine bacteria.

Bacteria display dynamic abundance fluctuations over time in marine environments, where they play key biogeochemical roles. Here, we characterized the seasonal dynamics of marine bacteria in a coastal oligotrophic time series station, tested how similar the temporal niche of closely related taxa is, and what are the environmental parameters modulating their seasonal abundance patterns. We further explored how conserved the niche is at higher taxonomic levels. The community presented recurrent patterns of seasonality for 297 out of 6825 amplicon sequence variants (ASVs), which constituted almost half of the total relative abundance (47%). For certain genera, niche similarity decreased as nucleotide divergence in the 16S rRNA gene increased, a pattern compatible with the selection of similar taxa through environmental filtering. Additionally, we observed evidence of seasonal differentiation within various genera as seen by the distinct seasonal patterns of closely related taxa. At broader taxonomic levels, coherent seasonal trends did not exist at the class level, while the order and family ranks depended on the patterns that existed at the genus level. This study identifies the coexistence of closely related taxa for some bacterial groups and seasonal differentiation for others in a coastal marine environment subjected to a strong seasonality.

New Perkinsea Parasitoids of Dinoflagellates Distantly Related to Parviluciferaceae Members.

Perkinsea is a phylogenetic group of protists that includes parasites of distantly related hosts. However, its diversity is still mainly composed of environmental sequences, mostly obtained from freshwater environments. Efforts to isolate and culture parasitoids of dinoflagellates have led to the description of several phylogenetically closely related species constituting the Parviluciferaceae family. In this study, two new parasitoid species infecting dinoflagellates during recurrent coastal blooms are reported. Using the ribosomal RNA (rRNA) gene phylogenies, we show that both cluster within Perkinsea, one of them at the base of Parviluciferaceae and the other in a distinct branch unrelated to other described species. The establishment of host-parasite lab cultures of the latter allowed its morphological characterization, resulting in the formal description of Maranthos nigrum gen. nov., sp. nov. The life-cycle development of the two parasitoids is generally the same as that of other members of the Parviluciferaceae family but they differ in the features of the trophont and sporont stages, including the arrangement of zoospores during the mature sporangium stage and the lack of specialized structures that release the zoospores into the environment. Laboratory cross-infection experiments showed that the parasitoid host range is restricted to dinoflagellates, although it extends across several different genera. The maximum prevalence reached in the tested host populations was lower than in other Parviluciferaceae members. The findings from this study suggest that Perkinsea representatives infecting dinoflagellates are more widespread than previously thought.

Host preferences of coexisting Perkinsea parasitoids during coastal dinoflagellate blooms.

Parasites in aquatic systems are highly diverse and ubiquitous. In marine environments, parasite-host interactions contribute substantially to shaping microbial communities, but their nature and complexity remain poorly understood. In this study, we examined the relationship between Perkinsea parasitoids and bloom-forming dinoflagellate species. Our aim was to determine whether parasite-host species interactions are specific and whether the diversity and distribution of parasitoids are shaped by their dinoflagellate hosts. Several locations along the Catalan coast (NW Mediterranean Sea) were sampled during the blooms of five dinoflagellate species and the diversity of Perkinsea was determined by combining cultivation-based methods with metabarcoding of the V4 region of 18S rDNA. Most known species of Parviluciferaceae, and others not yet described, were detected, some of them coexisting in the same coastal location, and with a wide distribution. The specific parasite-host interactions determined for each of the studied blooms demonstrated the host preferences exhibited by parasitoids in nature. The dominance of a species within the parasitoid community is driven by the presence and abundances of its preferred host(s). The absence of parasitoid species, often associated with a low abundance of their preferred hosts, suggested that high infection rates are reached only under conditions that favour parasitoid propagation, especially dinoflagellate blooms.

Emerging Parasitic Protists: The Case of Perkinsea.

The last century has witnessed an increasing rate of new disease emergence across the world leading to permanent loss of biodiversity. Perkinsea is a microeukaryotic parasitic phylum composed of four main lineages of parasitic protists with broad host ranges. Some of them represent major ecological and economical threats because of their geographically invasive ability and pathogenicity (leading to mortality events). In marine environments, three lineages are currently described, the Parviluciferaceae, the Perkinsidae, and the Xcellidae, infecting, respectively, dinoflagellates, mollusks, and fish. In contrast, only one lineage is officially described in freshwater environments: the severe Perkinsea infectious agent infecting frog tadpoles. The advent of high-throughput sequencing methods, mainly based on 18S rRNA assays, showed that Perkinsea is far more diverse than the previously four described lineages especially in freshwater environments. Indeed, some lineages could be parasites of green microalgae, but a formal nature of the interaction needs to be explored. Hence, to date, most of the newly described aquatic clusters are only defined by their environmental sequences and are still not (yet) associated with any host. The unveiling of this microbial black box presents a multitude of research challenges to understand their ecological roles and ultimately to prevent their most negative impacts. This review summarizes the biological and ecological traits of Perkinsea-their diversity, life cycle, host preferences, pathogenicity, and highlights their diversity and ubiquity in association with a wide range of hosts.

Description of two new coexisting parasitoids of blooming dinoflagellates in the Baltic sea: Parvilucifera catillosa sp. nov. and Parvilucifera sp. (Perkinsea, Alveolata).

Perkinsea are a group of intracellular protist parasites that inhabit all types of aquatic environments and cause significant population declines of a wide variety of hosts. However, the diversity of this lineage is mostly represented by environmental rDNA sequences. Complete descriptions of Perkinsea that infect marine dinoflagellates have increased in recent literature due to the identification, isolation and culturing of representatives during bloom events, contributing to expand the knowledge on the diversity and ecology of the group. Shallow coastal areas in the Baltic Sea suffer seasonal dinoflagellate blooms. In summer 2016, two parasitoids were isolated during a Kryptoperidinium foliaceum bloom in the Baltic Sea. Morphological features and sequences of the small and large subunit of the ribosomal DNA gene revealed these two parasitoids were new species that belong to the genus Parvilucifera. This is the first time that Parvilucifera infections are reported in the Inner Baltic Sea. The first species, Parvilucifera sp. has some morphological and phylogenetic features in common with P. sinerae and P. corolla, although its ultrastructure could not be studied and the formal description could not be done. The second new species, named Parvilucifera catillosa, has several distinct morphological features in its zoospores (e.g. the presence of a rostrum), and in the shape and size of the apertures in the sporangium stage, which are larger and more protuberant than in the other species of the genus. Infections observed in the field and cross-infection experiments determined that the host range of both Parvilucifera species was restricted to dinoflagellates, each one showing a different host preference. The coexistence in the same environment by the two closely related parasitoids with very similar life cycles suggests that their niche separation is the preferred host.

Morphological and phylogenetic data do not support the split of Alexandrium into four genera.

A recently published study analyzed the phylogenetic relationship between the genera Centrodinium and Alexandrium, confirming an earlier publication showing the genus Alexandrium as paraphyletic. This most recent manuscript retained the genus Alexandrium, introduced a new genus Episemicolon, resurrected two genera, Gessnerium and Protogonyaulax, and stated that: "The polyphyly [sic] of Alexandrium is solved with the split into four genera". However, these reintroduced taxa were not based on monophyletic groups. Therefore this work, if accepted, would result in replacing a single paraphyletic taxon with several non-monophyletic ones. The morphological data presented for genus characterization also do not convincingly support taxa delimitations. The combination of weak molecular phylogenetics and the lack of diagnostic traits (i.e., autapomorphies) render the applicability of the concept of limited use. The proposal to split the genus Alexandrium on the basis of our current knowledge is rejected herein. The aim here is not to present an alternative analysis and revision, but to maintain Alexandrium. A better constructed and more phylogenetically accurate revision can and should wait until more complete evidence becomes available and there is a strong reason to revise the genus Alexandrium. The reasons are explained in detail by a review of the available molecular and morphological data for species of the genera Alexandrium and Centrodinium. In addition, cyst morphology and chemotaxonomy are discussed, and the need for integrative taxonomy is highlighted.

Assessment of microbial plankton diversity as an ecological indicator in the NW Mediterranean coast.

High-throughput sequencing of microbial assemblages has been proposed as an alternative methodology to the traditional ones used in marine monitoring and environmental assessment. Here, we evaluated pico- and nanoplankton diversity as ecological indicators in NW Mediterranean coastal waters by comparing their diversity in samples subjected to varying degrees of continental pressures. Using metabarcoding of the 16S and 18S rRNA genes, we explored whether alphadiversity indices, abundance of Operational Taxonomic Units and taxonomic groups (and their ratios) provide information on the ecological quality of coastal waters. Our results revealed that only eukaryotic diversity metrics and a limited number of prokaryotic and eukaryotic taxa displayed potential in assessing continental influences in our surveyed area, resulting thus in a restrained potential of microbial plankton diversity as an ecological indicator. Therefore, incorporating microbial plankton diversity in environmental assessment could not always result in a significant improvement of current marine monitoring strategies.

Quantifying long-term recurrence in planktonic microbial eukaryotes.

How much temporal recurrence is present in microbial assemblages is still an unanswered ecological question. Even though marked seasonal changes have been reported for whole microbial communities, less is known on the dynamics and seasonality of individual taxa. Here, we aim at understanding microbial recurrence at three different levels: community, taxonomic group and operational taxonomic units (OTUs). For that, we focused on a model microbial eukaryotic community populating a long-term marine microbial observatory using 18S rRNA gene data from two organismal size fractions: the picoplankton (0.2-3 µm) and the nanoplankton (3-20 µm). We have developed an index to quantify recurrence in particular taxa. We found that community structure oscillated systematically between two main configurations corresponding to winter and summer over the 10 years studied. A few taxonomic groups such as Mamiellophyceae or MALV-III presented clear recurrence (i.e., seasonality), whereas 13%-19% of the OTUs in both size fractions, accounting for ~40% of the relative abundance, featured recurrent dynamics. Altogether, our work links long-term whole community dynamics with that of individual OTUs and taxonomic groups, indicating that recurrent and non-recurrent changes characterize the dynamics of microbial assemblages.

Life histories of microalgal species causing harmful blooms: Haploids, diploids and the relevance of benthic stages.

In coastal and offshore waters, Harmful Algal Blooms (HABs) currently threaten the well-being of coastal countries. These events, which can be localized or involve wide-ranging areas, pose risks to human health, marine ecosystems, and economic resources, such as tourism, fisheries, and aquaculture. Dynamics of HABs vary from one site to another, depending on the hydrographic and ecological conditions. The challenge in investigating HABs is that they are caused by organisms from multiple algal classes, each with its own unique features, including different life histories. The complete algal life cycle has been determined in <1% of the described species, although elucidation of the life cycles of bloom-forming species is essential in developing preventative measures. The knowledge obtained thus far has confirmed the complexity of the algal life cycle, which is composed of discrete life stages whose morphology, ecological niche (plankton/benthos), function, and lifespan vary. The factors that trigger transitions between the different stages in nature are mostly unknown, but it is clear that an understanding of this process provides the key to effectively forecasting bloom recurrence, maintenance, and decline. Planktonic stages constitute an ephemeral phase of the life cycle of most species whereas resistant, benthic stages enable a species to withstand adverse conditions for prolonged periods, thus providing dormant reservoirs for eventual blooms and facilitating organismal dispersal. Here we review current knowledge of the life cycle strategies of major groups of HAB producers in marine and brackish waters. Rather than providing a comprehensive discussion, the objective was to highlight several of the research milestones that have changed our understanding of the plasticity and frequency of the different life cycle stages as well as the transitions between them. We also discuss the relevance of benthic and planktonic forms and their implications for HAB dynamics.

Evolutionary Trends of Perkinsozoa (Alveolata) Characters Based on Observations of Two New Genera of Parasitoids of dinoflagellates, Dinovorax gen. nov. and Snorkelia gen. nov.

Parasites are one of the ecologically most relevant groups of marine food webs, but their taxonomic and biological complexity hampers the assessment of their diversity and evolutionary trends. Moreover, the within-host processes that govern parasitoid infection, development and reproduction are often unknown. In this study, we describe a new species of a perkinsozoan endoparasitoid that infects the toxic dinoflagellate Dinophysis sacculus, by including observations of its morphology, ultrastructure, life-cycle development and phylogeny. The SSU rDNA sequence and main morphological features were also obtained for a second parasitoid species infecting the bloom-forming dinoflagellate Levanderina fissa. Phylogenetic analyses including the sequences obtained show that all known Perkinsozoa species infecting dinoflagellates cluster together. However, sequences of Parvilucifera prorocentri and those obtained in this study cluster at the base of the clade, while the rest of Parvilucifera representatives form a separated highly-supported cluster. These results, together with differing morphological characters like the formation of a germ-tube, the presence of trichocysts, or the heterochromatin presence in zoospores nucleus justify the erection of Dinovorax pyriformis gen. nov. et sp. nov., and Snorkelia prorocentri gen. nov. et comb. nov. (=Parvilucifera prorocentri). The morphological features and phylogenetic position of these parasitoids represent ancestral characters for the Perkinsozoa phylum, and also for Dinozoa clade, allowing the inference of the evolutionary framework of these Alveolata members.

In situ Occurrence, Prevalence and Dynamics of Parvilucifera Parasitoids during Recurrent Blooms of the Toxic Dinoflagellate Alexandrium minutum.

Dinoflagellate blooms are natural phenomena that often occur in coastal areas, which in addition to their large number of nutrient-rich sites are characterized by highly restricted hydrodynamics within bays, marinas, enclosed beaches, and harbors. In these areas, massive proliferations of dinoflagellates have harmful effects on humans and the ecosystem. However, the high cell density reached during blooms make them vulnerable to parasitic infections. Under laboratory conditions parasitoids are able to exterminate an entire host population. In nature, Parvilucifera parasitoids infect the toxic dinoflagellate Alexandrium minutum during bloom conditions but their prevalence and impact remain unexplored. In this study, we evaluated the in situ occurrence, prevalence, and dynamics of Parvilucifera parasitoids during recurrent blooms of A. minutum in a confined site in the NW Mediterranean Sea as well as the contribution of parasitism to bloom termination. Parvilucifera parasitoids were recurrently detected from 2009 to 2013, during seasonal outbreaks of A. minutum. Parasitic infections in surface waters occurred after the abundance of A. minutum reached 104-105 cells L-1, suggesting a density threshold beyond which Parvilucifera transmission is enhanced and the number of infected cells increases. Moreover, host and parasitoid abundances were not in phase. Instead, there was a lag between maximum A. minutum and Parvilucifera densities, indicative of a delayed density-dependent response of the parasitoid to host abundances, similar to the temporal dynamics of predator-prey interactions. The highest parasitoid prevalence was reached after a peak in host abundance and coincided with the decay phase of the bloom, when a maximum of 38% of the A. minutum population was infected. According to our estimates, Parvilucifera infections accounted for 5-18% of the total observed A. minutum mortality, which suggested that the contribution of parasitism to bloom termination is similar to that of other biological factors, such as encystment and grazing.

Morphological and molecular characterization of Bysmatrum subsalsum (Dinophyceae) from the western Mediterranean Sea reveals the existence of cryptic species.

Bysmatrum subsalsum is a cosmopolitan dinoflagellate species that inhabits marine and transitional habitats. Despite its wide distribution, information on the morphological variability, phylogeny and ecology of B. subsalsum is scarce. In this study, we provide morphological and molecular data on B. subsalsum strains and wild cells from different locations in the Mediterranean Basin. The dynamics of cell abundances and the associated environmental conditions during a field bloom are also described. Genetic sequences of B. subsalsum obtained in this study showed large intraspecific differences, clustering in two well-differentiated clades. Despite a certain degree of variation with respect to cell size, apical pore complex (APC) morphology and size, and cingulum displacement, cells from the two clades showed similar morphological traits. These findings indicated the occurrence of cryptic species. Comparisons of the morphology of our B. subsalsum specimens with the few descriptions available in the literature revealed larger than previously known intraspecific morphological variability. Phylogenetic trees inferred from the concatenated SSU, 5.8S-ITS, and LSU rRNA and the individual 5.8S-ITS regions suggested the inclusion of Bysmatrum in the Peridiniales and a close phylogenetic relationship with Peridinium sensu stricto. However, the low statistical support prevented the assignment of Bysmatrum to a particular family of Peridiniales. Ecological data obtained from a bloom in La Pletera salt marshes (Catalan Coast, Spain) suggested the species reaches high cell abundances at water temperatures >20°C and salinity levels >30. Our results add new information regarding the morphology, phylogeny, and ecology of B. subsalsum.

Life-cycle, ultrastructure, and phylogeny of Parvilucifera corolla sp. nov. (Alveolata, Perkinsozoa), a parasitoid of dinoflagellates.

Recent studies of marine protists have revealed parasites to be key components of marine communities. Here we describe a new species of the parasitoid genus Parvilucifera that was observed infecting the dinoflagellate Durinskia baltica in salt marshes of the Catalan coast (NW Mediterranean). In parallel, the same species was detected after the incubation of seawater from the Canary Islands (Lanzarote, NE Atlantic). The successful isolation of strains from both localities allowed description of the life cycle, ultrastructure, and phylogeny of the species. Its infection mechanism consists of a free-living zoospore that penetrates a dinoflagellate cell. The resulting trophont gradually degrades the dinoflagellate cytoplasm while growing in size. Once the host is consumed, schizogony of the parasitoid yields a sporocyte. After cytokinesis is complete, the newly formed zoospores are released into the environment and are ready to infect new host cells. A distinguishing feature of the species is the radial arrangement of its zoospores around the central area of the sporocyte during their formation. The species shows a close morphological similarity with other species of the genus, including P. infectans, P. sinerae, and P. rostrata.

A Game of Russian Roulette for a Generalist Dinoflagellate Parasitoid: Host Susceptibility Is the Key to Success.

Marine microbial interactions involving eukaryotes and their parasites play an important role in shaping the structure of phytoplankton communities. These interactions may alter population densities of the main host, which in turn may have consequences for the other concurrent species. The effect generalist parasitoids exert on a community is strongly dependent on the degree of host specificity. Parvilucifera sinerae is a generalist parasitoid able to infect a wide range of dinoflagellates, including toxic-bloom-forming species. A density-dependent chemical cue has been identified as the trigger for the activation of the infective stage. Together these traits make Parvilucifera-dinoflagellate hosts a good model to investigate the degree of specificity of a generalist parasitoid, and the potential effects that it could have at the community level. Here, we present for the first time, the strategy by which a generalist dinoflagellate parasitoid seeks out its host and determine whether it exhibits host preferences, highlighting key factors in determining infection. Our results demonstrate that in its infective stage, P. sinerae is able to sense potential hosts, but does not actively select among them. Instead, the parasitoids contact the host at random, governed by the encounter probability rate and once encountered, the chance to penetrate inside the host cell and develop the infection strongly depends on the degree of host susceptibility. As such, their strategy for persistence is more of a game of Russian roulette, where the chance of survival is dependent on the susceptibility of the host. Our study identifies P. sinerae as a potential key player in community ecology, where in mixed dinoflagellate communities consisting of hosts that are highly susceptible to infection, parasitoid preferences may mediate coexistence between host species, reducing the dominance of the superior competitor. Alternatively, it may increase competition, leading to species exclusion. If, however, highly susceptible hosts are absent from the community, the parasitoid population could suffer a dilution effect maintaining a lower parasitoid density. Therefore, both host community structure and host susceptibility will determine infectivity in the field.