Protist Interactions and Community Structure During Early Autumn in the Kerguelen Region (Southern Ocean)

Sassenhagen, Ingrid; Irion, Solène; Jardillier, Ludwig; Moreira, David; Christaki, Urania

doi:10.1016/j.protis.2019.125709

Cited by 27 publications

(29 citation statements)

References 93 publications

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“…The wide spectrum of infection suggested for Syndiniales Group I might indicate low host-specificity and explain why we found this group associated with all zooplankton (Sassenhagen et al 2020;Guillou et al 2008). An alternative explanation for the presence of Group I in all zooplankton groups is based on previous investigations where Syndiniales Group I was found associated with cercozoans (Dolven et al 2007;Clarke et al 2019;Sassenhagen et al 2020), taxa that we found often abundant both in the water and associated with all zooplankton (Fig. 1a, c).…”

Section: Discussionmentioning

confidence: 68%

“…This suggests that the wide spectrum of infection of Group I is potentially linked to the ingestion of cercozoan by all zooplankton consumers. However, it has recently been suggested that Syndiniales Group I might infect diatoms, and Syndiniales associated with Cercozoa might be the result of predation on infected diatoms (Sassenhagen et al 2020), emphasizing the high complexity of the biotic interactions that we found in plankton communities. Our observations might also support this hypothesis because diatoms were shared as prey by all the zooplankton consumers (Zamora-Terol et al 2020), in particular Thalassiosira, one of the genera suggested by Sassenhagen et al 2020 to be infected by Syndiniales Group I.…”

Section: Discussionmentioning

confidence: 76%

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Molecular evidence of host-parasite interactions between zooplankton and Syndiniales

2020

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Although parasitism is one of the most prevalent interactions in nature, studies of aquatic food webs rarely include parasites. Syndiniales (Dinophyceae, Alveolata) is a diverse parasitic group of dinoflagellates, common in all marine environments, and are described as dominant components of pelagic ecosystems. However, their temporal dynamics, prevalence, and host-specificity are poorly known. Using DNA metabarcoding to explore trophic interactions of zooplankton, we found a high proportion of Syndiniales sequence reads associated with the targeted consumers. We observed the occurrence of Syndiniales in copepods, cladocerans, appendicularians, and polychaete larvae, ranging between 11 and 36% relative read abundance, encompassing 11 main putative clades. Zooplankton–Syndiniales interactions showed variability in occurrence across the taxa, but also certain host-specificity. The study suggests that the observed copepod–Syndiniales interactions can be both direct parasitic infections and the result of trophic transmission through potentially infected prey by Syndiniales. Given the quantitative importance of Syndiniales and zooplankton in marine environments, our findings emphasize that their interactions should be recognized as key players in the structure and connectivity of plankton food webs.

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Section: Discussionmentioning

confidence: 68%

Section: Discussionmentioning

confidence: 76%

Molecular evidence of host-parasite interactions between zooplankton and Syndiniales

2020

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“…In particular, Eucampia antarctica cells and CRS observed above the plateau were not silicifying and likely corresponded to a remnant population that accumulated at the base of the mixed layer prior to the cruise. The relatively low percentage of crunched frustules (5 ± 3 %) suggests that selective grazing had little impact on shaping communities, while parasites could have controlled population dynamics prior to the cruise since elevated relative abundances of free Syndiniales spores was suggested by environmental sequencing (Sassenhagen et al, 2020).…”

Section: Kerguelen Areamentioning

confidence: 99%

The structure of diatom communities constrains biogeochemical properties in surface waters of the Southern Ocean (Kerguelen Plateau)

Lafond

Leblanc

Justine

et al. 2020

Journal of Marine Systems

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In the context of climate change, understanding the ecological processes controlling the functioning and the efficiency of the biological pump is of primary importance. Plankton community structure and species-specific properties are often invoked as likely to affect biogeochemistry and the export of organic and biogenic material to the ocean interior. Although a major player in this respect, diatoms are still viewed as a single functional type whose diversity is generally overlooked. Here we examine that question, building on the results achieved during the MOBYDICK expedition, which occurred in the vicinity of the Kerguelen Islands (Southern Ocean) in late summer, a time window corresponding to the demise of the annually recurrent phytoplankton blooms already known to be controlled by iron availability. The Si/C/N stoichiometry of the particulate matter was studied in conjunction with the different diatom community structures, their physiological states, as well as their species-specific carbon contents and silicification degrees. Our results show that diatoms outside the iron-fertilized plateau were more heavily silicified, due to the combined effects of both taxonomic composition of the resident community and a direct physiological response to iron stress, resulting in higher Si:C elemental ratios in diatoms as well as in the bulk particulate matter. Despite low silicic acid concentrations, large chains of weakly silicified Corethron inerme were able to grow in the upper mixed layer above the plateau, while in adjacent high nutrient low chlorophyll (HNLC) waters, communities were dominated by Fragilariopsis spp., Cylindrotheca closterium and the centric genera Actinocyclus/Thalassiosira spp. Depth was also an important factor shaping diatom communities, with the presence of a deep and inactive assemblage located within the pycnocline gradient, both on-and offplateau, which likely resulted from the differential sinking and accumulation of species previously grown at the surface. In HNLC waters, below the mixed layer, detrital frustules of the heavily silicified species Fragilariopsis kerguelensis carried mostly Si, while above the plateau, Eucampia antarctica and Chaetoceros spp. (resting spores and vegetative stages) were efficient vectors of both Si and C to the deeper layers. Our study shows that the stoichiometry of the biological pump cannot be considered solely as a simple response to a single limiting factor (here iron) highlighting the importance of a species-centered approach in order to finely resolve biogeochemical fluxes and improve our understanding of the biological pump.

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“…Positive interactions that were detected between these groups remain ambiguous, as there has yet to be empirical evidence of Syndiniales infecting diatoms. However, Syndiniales have been shown to positively associate with diatoms in other co-occurrence networks or single-cell studies (15,16,66), and diatoms are known hosts of other parasitic protists and fungi (8,47), which warrants further investigation into their infection dynamics.…”

Section: Discussionmentioning

confidence: 99%

“…Additional omics tools, such as transcriptomics, may be used to inform in situ parasitehost interactions, distinguishing between different stages of Syndiniales (e.g., intracellular trophont versus free-living dinospores) based on patterns in gene expression and testing how core genes involved in parasitic infection (e.g., host recognition or attachment) may be differentially expressed under certain abiotic or biotic conditions (69). Indeed, 18S profiling of a larger size fraction (e.g., Ͻ200 m) cannot distinguish between Syndiniales sequences derived from trophont or dinospore stages, and so fractionation of 18S samples (e.g., Ͻ5 m) may be useful to examine the relative abundance of Syndiniales across multiple size fractions (66). In all, these alternative techniques will be important to complement future 18S amplicon studies and verify temporal patterns and parasite-host interactions proposed via co-occurrence networks.…”

Section: Discussionmentioning

confidence: 99%

Temporal Variability and Ecological Interactions of Parasitic Marine Syndiniales in Coastal Protist Communities

Anderson

Harvey

2020

mSphere

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Syndiniales are a ubiquitous group of protist parasites that infect and kill a wide range of hosts, including harmful bloom-forming dinoflagellates. Despite the importance of parasitism as an agent of plankton mortality, parasite-host dynamics remain poorly understood, especially over time, hindering the inclusion of parasitism in food web and ecosystem models. For a full year in the Skidaway River Estuary (Georgia), we employed weekly 18S rRNA sampling and co-occurrence network analysis to characterize temporal parasite-host infection dynamics of Syndiniales. Over the year, Syndiniales exhibited strong temporal variability, with higher relative abundance from June to October (7 to 28%) than other months in the year (0.01% to 6%). Nonmetric dimensional scaling of Syndiniales composition revealed tight clustering in June to October that coincided with elevated temperatures (23 to 31°C), though in general, abiotic factors poorly explained composition (canonical correspondence analysis [CCA] and partial least-squares [PLS]) and were less important in the network than biotic relationships. Syndiniales amplicon sequence variants (ASVs) were well represented in the co-occurrence network (20% of edges) and had significant positive associations (Spearman r > 0.7), inferred to be putative parasite-host relationships, with known dinoflagellate hosts (e.g., Akashiwo and Gymnodinium) and other protist groups (e.g., ciliates, radiolarians, and diatoms). Positive associations rarely involved a single Syndiniales and dinoflagellate species, implying flexible parasite-host infection dynamics. These findings provide insight into the temporal dynamics of Syndiniales over a full year and reinforce the importance of single-celled parasites in driving plankton population dynamics. Further empirical work is needed to confirm network interactions and to incorporate parasitism within the context of ecosystem models. IMPORTANCE Protist parasites in the marine alveolate group, Syndiniales, have been observed within infected plankton host cells for decades, and recently, global-scale efforts (Tara Ocean exploration) have confirmed their importance within microbial communities. Yet, protist parasites remain enigmatic, particularly with respect to their temporal dynamics and parasite-host interactions. We employed weekly 18S amplicon surveys over a full year in a coastal estuary, revealing strong temporal shifts in Syndiniales parasites, with highest relative abundance during warmer summer to fall months. Though influenced by temperature, Syndiniales population dynamics were also driven by a high frequency of biological interactions with other protist groups, as determined through co-occurrence network analysis. Parasitic interactions implied by the network highlighted a range of confirmed (dinoflagellates) and putative (diatoms) interactions and suggests parasites may be less selective in their preferred hosts. Understanding parasite-host dynamics over space and time will improve our ability to include parasitism as a loss term in microbial food web models.

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Protist Interactions and Community Structure During Early Autumn in the Kerguelen Region (Southern Ocean)

Cited by 27 publications

References 93 publications

Molecular evidence of host-parasite interactions between zooplankton and Syndiniales

Molecular evidence of host-parasite interactions between zooplankton and Syndiniales

The structure of diatom communities constrains biogeochemical properties in surface waters of the Southern Ocean (Kerguelen Plateau)

Temporal Variability and Ecological Interactions of Parasitic Marine Syndiniales in Coastal Protist Communities

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