Trojan horses in the marine realm: characterizing protistan parasite ecology in coastal waters

Protists are taxonomically and metabolically diverse drivers of energy and nutrient flow in the marine environment, with recent research suggesting significant roles in global carbon cycling throughout the water column. Top-down controls on planktonic protists include grazing and parasitism, processes that both contribute to nutrient transfer and biogeochemical cycling in the global ocean. Recent global surveys of eukaryotic small subunit ribosomal RNA molecular signatures have highlighted the fact that parasites belonging to the marine alveolate order Syndiniales are both abundant and ubiquitous in coastal and open ocean environments, suggesting a major role for this taxon in marine food webs. Two coastal sites, Saanich Inlet (Vancouver Island, BC) and Salt Pond (Falmouth, MA, USA) were selected as model ecosystems to examine the impacts of Syndinian parasitism on protist communities. Data presented in this thesis combines high-resolution sampling, water chemistry (including nutrients) analyses, molecular marker gene analyses, fluorescence in situ hybridization, and modeling to address key knowledge gaps regarding syndinian ecology. Information is presented on previously undescribed putative host taxa, the prevalence of syndinian parasites and infections on different hosts in coastal waters, and a framework for modeling host-parasite interactions based on field observations.

Biomolecular Composition of Sea Ice Microalgae and Its Influence on Marine Biogeochemical Cycling and Carbon Transfer through Polar Marine Food Webs

Microalgae growing on the underside of sea ice are key primary producers in polar marine environments. Their nutritional status, determined by their macromolecular composition, contributes to the region’s biochemistry and the unique temporal and spatial characteristics of their growth makes them essential for sustaining polar marine food webs. Here, we review the plasticity and taxonomic diversity of sea ice microalgae macromolecular composition, with a focus on how different environmental conditions influence macromolecular production and partitioning within cells and communities. The advantages and disadvantages of methodologies for assessing macromolecular composition are presented, including techniques that provide high throughput, whole macromolecular profile and/or species-specific resolution, which are particularly recommended for future studies. The directions of environmentally driven macromolecular changes are discussed, alongside anticipated consequences on nutrients supplied to the polar marine ecosystem. Given that polar regions are facing accelerated rates of environmental change, it is argued that a climate change signature will become evident in the biochemical composition of sea ice microalgal communities, highlighting the need for further research to understand the synergistic effects of multiple environmental stressors. The importance of sea ice microalgae as primary producers in polar marine ecosystems means that ongoing research into climate-change driven macromolecular phenotyping is critical to understanding the implications for the regions biochemical cycling and carbon transfer.

Bacterial lifestyle switch in response to algal metabolites

Unicellular algae, termed phytoplankton, greatly impact the marine environment by serving as the basis of marine food webs and by playing central roles in biogeochemical cycling of elements. The interactions between phytoplankton and heterotrophic bacteria affect the fitness of both partners. It is becoming increasingly recognized that metabolic exchange determines the nature of such interactions, but the underlying molecular mechanisms remain underexplored. Here, we investigated the molecular and metabolic basis for the bacterial lifestyle switch, from coexistence to pathogenicity, in Sulfitobacter D7 during its interaction with Emiliania huxleyi, a cosmopolitan bloom-forming phytoplankter. To unravel the bacterial lifestyle switch, we profiled bacterial transcriptomes in response to infochemicals derived from algae in exponential and stationary growth, which induced the Sulfitobacter D7 coexistence and pathogenicity lifestyles, respectively. We found that algal dimethylsulfoniopropionate (DMSP) was a pivotal signaling molecule that mediated the transition between the lifestyles. However, the coexisting and pathogenic lifestyles were evident only in the presence of additional algal metabolites. In the pathogenic mode, Sulfitobacter D7 upregulated flagellar motility and many transport systems, presumably to maximize assimilation of E. huxleyi-derived metabolites released by algal cells upon cell death. Specifically, we discovered that algae-produced benzoate promoted the growth of Sulfitobacter D7, and negated the DMSP-inducing lifestyle switch to pathogenicity, demonstrating that benzoate is important for maintaining the coexistence of algae and bacteria. We propose that bacteria can sense the physiological status of the algal host through changes in the metabolic composition, which will determine the bacterial lifestyle during the interactions.

Global ecomorphological restructuring of dominant marine reptiles prior to the K/Pg mass extinction

Mosasaurid squamates were the dominant amniote predators in marine ecosystems during most of the Late Cretaceous. Evidence from multiple sites worldwide of a global mosasaurid community restructuring across the Campanian-Maastrichtian transition may have wide-ranging implications for the evolution of diversity of these top oceanic predators. In this study, we use a suite of biomechanical traits and functionally descriptive ratios to investigate how the morphofunctional disparity of mosasaurids evolved through time and space prior to the Cretaceous-Palaeogene (K/Pg) mass extinction. Our results suggest that the worldwide taxonomic turnover in mosasaurid community composition from Campanian to Maastrichtian is reflected by a notable increase in morphofunctional disparity on a global scale, but especially driven the North American record. Ecomorphospace occupation becomes more polarised during the late Maastrichtian, as the morphofunctional disparity of mosasaurids plateaus in the Southern Hemisphere and decreases in the Northern Hemisphere. We show that these changes are not associated with strong modifications in mosasaurid size, but rather with the functional capacities of their skulls, and that mosasaurid morphofunctional disparity was in decline in several provincial communities before the K/Pg mass extinction. Our study highlights region-specific patterns of disparity evolution, and the importance of assessing vertebrate extinctions both globally and regionally. Ecomorphological differentiation in mosasaurid communities, coupled with declines in other formerly abundant marine reptile groups, indicates widespread restructuring of higher trophic levels in marine food webs was well underway when the K-Pg mass extinction took place.

Gut content metabarcoding reveals potential importance of fisheries discards consumption in marine fauna

Fisheries discards have become a source of concern for the perennation of marine resources. To reduce discards, the European Union adopted a Landing Obligation under the reform of its Common Fisheries Policy. However, food web consequences of reducing discards remain uncertain since their degree and pathway of reintegration are understudied. We used multi-marker DNA metabarcoding of gut contents and an ecological network approach to quantify marine fauna reliance on discarded fish and functional importance of discard consumers in coastal fishing grounds. We show that potential discard consumption is widespread across fish and invertebrates, but particularly important for decapods which were also pinpointed as functionally important. Potential discard consumption may represent up to 66% of all interactions involving fish prey in the reconstructed network. We highlight that discard reliance may be more important than previously assessed in some fishing areas and support functionally important taxa. While reducing discarding remains a conservation priority, it is crucial to understand discards reintegration in marine food webs to anticipate changes in the context of an ecosystem approach to fisheries management.

Viral Production in Seawater Filtered Through 0.2-μm Pore-Size Filters: A Hidden Biogeochemical Cycle in a Neglected Realm

Viral production is a key parameter for assessing virus-mediated biogeochemical cycles. One widely used method for the determination of viral production, called the virus reduction assay, reduces viral abundance, while maintaining bacterial abundance, using 0.2-μm pore-size filters. Viral production is estimated from the increase of viral abundance during incubation. We hypothesized that small-cell-sized bacterial communities can pass through 0.2-μm filters and drive viral production, representing a missing fraction of viral production that is missed by the virus reduction assay. Coastal seawater was filtered through 0.2-μm filters and diluted with virus-free seawater. Viral production in the <0.2-μm filtrate was estimated from changes in viral abundance determined through flow cytometry. We found that viruses were produced in the <0.2-μm communities, which were strongly enriched with low nucleic acid content bacteria. Estimated viral production in the <0.2-μm filtrates accounted for up to 43% of total viral production and 10% of dissolved organic carbon production mediated by viral lysis of bacterial cells. By not considering viral production in these <0.2-μm communities, the virus reduction assay may underestimate viral production. Virus–bacteria interactions in <0.2-μm communities may represent a significant and overlooked role of viruses in marine food webs and carbon fluxes.

Presence of DNA from Chlamydia-like organisms in the nasal cavities of grey seal pups (Halichoerus grypus) and three different substrates present in a breeding colony

Background Chlamydia-like organisms (CLO) have been found to be present in many environmental niches, including human sewage and agricultural run-off, as well as in a number of aquatic species worldwide. Therefore, monitoring their presence in sentinel wildlife species may be useful in assessing the wider health of marine food webs in response to habitat loss, pollution and disease. We used nasal swabs from live (n = 42) and dead (n = 50) pre-weaned grey seal pups and samples of differing natal substrates (n = 8) from an off-shore island devoid of livestock and permanent human habitation to determine if CLO DNA is present in these mammals and to identify possible sources. Results We recovered CLO DNA from 32/92 (34.7%) nasal swabs from both live (n = 17) and dead (n = 15) seal pups that clustered most closely with currently recognised species belonging to three chlamydial families: Parachlamydiaceae (n = 22), Rhabdochlamydiaceae (n = 6), and Simkaniaceae (n = 3). All DNA positive sediment samples (n = 7) clustered with the Rhabdochlamydiaceae. No difference was found in rates of recovery of CLO DNA in live versus dead pups suggesting the organisms are commensal but their potential as opportunistic secondary pathogens could not be determined. Conclusion This is the first report of CLO DNA being found in marine mammals. This identification warrants further investigation in other seal populations around the coast of the UK and in other areas of the world to determine if this finding is unique or more common than shown by this data. Further investigation would also be warranted to determine if they are present as purely commensal organisms or whether they could also be opportunistic pathogens in seals, as well as to investigate possible sources of origin, including whether they originated as a result of anthropogenic impacts, including human waste and agricultural run-off.

Who Is Where in Marine Food Webs? A Trait-Based Analysis of Network Positions

Networks of trophic interactions provide a lot of information on the functioning of marine ecosystems. Beyond feeding habits, three additional traits (mobility, size, and habitat) of various organisms can complement this trophic view. The combination of traits and food web positions are studied here on a large food web database. The aim is a better description and understanding of ecological roles of organisms and the identification of the most important keystone species. This may contribute to develop better ecological indicators (e.g., keystoneness) and help in the interpretation of food web models. We use food web data from the Ecopath with Ecosim (EwE) database for 92 aquatic ecosystems. We quantify the network position of organisms by 18 topological indices (measuring centrality, hierarchy, and redundancy) and consider their three, categorical traits (e.g., for mobility: sessile, drifter, limited mobility, and mobile). Relationships are revealed by multivariate analysis. We found that topological indices belong to six different categories and some of them nicely separate various trait categories. For example, benthic organisms are richly connected and mobile organisms occupy higher food web positions.

Distribution, diet and relationships of the invasive ctenophore Mnemiopsis leidyi with anchovies and zooplankton, in the northeastern Adriatic Sea

Blooms of invasive ctenophore Mnemiopsis leidyi can have massive consequences on fish stocks and marine food webs. The distribution, abundance and diet of this ctenophore were investigated in the northeastern (NE) Adriatic between 2016 and 2019. The abundance of M. leidyi was determined daily along the coast of Rovinj (Croatia), and its spatial distribution monitored by visual census from research vessels and by pelagic trawl during acoustic surveys in September of each year. Mesozooplankton samples were collected along the western coast of Istria by vertical tows from the bottom to the surface. Spatial distribution and abundance of anchovy (Engraulis encrasicolus) assemblages were determined by geo-referenced hydro-acoustic sampling using a scientific echosounder. Large swarms of M. leidyi covering several km2 were regularly reported between July and November extending up to 25 NM from the western coast of the Istrian peninsula and reaching maximum offshore densities of 270 individuals per m2. The abundance of anchovy in the areas where M. leidyi was present evidently decreased. The content of M. leidyi’s digestive tract and plankton samples consisted both mainly of cladocerans, copepods, pteropods, echinodermata and bivalvia larvae. Results indicate that M. leidyi may accumulate and increase its abundance in the stagnant and trophically rich areas of the northern Adriatic gyres, spreading to the surrounding larger areas with currents. We assume that M. leidyi presence correlates with a decrease in anchovy population due to competition for food (zooplankton). Our findings support the importance of implementing an international monitoring program throughout the Adriatic Sea and demonstrate the ability of current MEDIAS surveys to detect changes in the pelagic ecosystem throughout surveyed areas.