Temporal pesticide dynamics alter specific eukaryotic taxa in a coastal transition zone.

Land use change and anthropogenic forcing can drastically alter the rates and patterns of sediment transport and modify biodiversity and ecosystem functions in coastal transition zones, such as the coastal ecosystems. Molecular studies of sediment extracted DNAs provide information on currently living organisms within the upper layers or buried from various periods of time, but might also provide knowledge on species dynamics, replacement and turnover. In this study, we evaluated the eukaryotic communities of a marine core that present a shift in soil erosion that was linked to glyphosate usage and correlated to chlordecone resurgence since 2000. We show differences in community composition between samples from the second half of the last century and those from the last two decades. Temporal analyses of the relative abundance, alpha diversity, and beta diversity for the two periods demonstrated different temporal dynamics depending on the considered taxonomic group. In particular, Ascomycetes showed a decrease in abundance over the most recent period associated with changes in community membership but not community structure. Two photosynthetic groups, Bacillariophyceae and Prasinophytes clade VII, showed a different pattern with an increase in abundance since the beginning of the 21st century with a decrease in diversity and evenness to form more heterogeneous communities dominated by a few abundant OTUs. Altogether, our data reveal that agricultural usages such as pesticide use can have long-term and species-dependent implications for microeukaryotic coastal communities on a tropical island.

Arsenic and chlordecone contamination and decontamination toxicokinetics in Sargassum sp.

Massive Sargassum sp. beachings have been occurring on Caribbean shores since 2011. The sargassum involved in such events are S. fluitans and S. natans, two drifting species whose proliferation has been observed in the southern North Atlantic Ocean. Both for reasons of environmental and sanitary assessment and repurposing, Sargassum sp. that is ashore piled up on beaches and decaying must be studied. Studies are required because of the concerning content of pelagic arsenic reported in the literature. They are also needed owing to Sargassum sp. contamination subsequent to historical pollution in the French West Indies by chlordecone, an insecticide used against the banana weevil Cosmopolites sordidus. The present study aims to describe the contamination and decontamination toxicokinetics of arsenic and chlordecone for Sargassum sp. stranding on shores and shallows in the Caribbean, in order to support the decision-making of the authorities involved. In situ and in mesocosm experiments performed in the present study show that Sargassum sp. contamination by chlordecone is mainly done after 2 h of exposition and reaches equilibrium after a day of exposure in polluted water, but BCF study suggests that the phenomenon is not actively supported (passive soption only). Arsenic transudation is intense in the case of immerged algae both. Half of the arsenic content is transudated after 13 h at sea and will transudate until vestigial arsenic concentration. Sargassum sp. contamination by arsenic, due to phytoaccumulation offshore, is broadly homogeneous before decay, and then leaks lead rapidly to a decrease in concentration in Sargassum sp. necromass, questioning the subsequent contamination of the coastal environment.

Sargassum Differentially Shapes the Microbiota Composition and Diversity at Coastal Tide Sites and Inland Storage Sites on Caribbean Islands.

Rafts of drifting pelagic Sargassum that are circulating across the Atlantic Ocean are complex ecosystems composed of a large number of associated species. Upon massive stranding, they lead to various socio-environmental issues including the inflow of contaminants and human health concerns. In this study, we used metabarcoding approaches to examine the differences in both the eukaryotic- and prokaryotic-associated communities from Sargassum present in two islands of the Lesser Antilles, namely Guadeloupe and Martinique. We detected significant differences in microbial community structure and composition between landing Sargassum, the surrounding seawater, and Sargassum from inland storage sites. In total we identified 22,214 prokaryotic and 17,679 eukaryotic OTUs. Among them, functional prediction analyses revealed a number of prokaryotes that might contribute to organic matter decomposition, nitrogen cycling and gas production, including sulfate-reducing bacteria at coastal landing sites, and methanogenic archaea at inland storage sites. We also found that Metazoan was the most abundant group in Sargassum samples, with nematode clades that presented exclusive or specific richness and abundance patterns depending on their Sargassum substrate. Together, these molecular inventories of the micro- and meiofauna communities provide baseline information for further characterization of trophic interactions, algal organic matter decomposition and nutrient transfers at coastal and inland storage sites.

Kakila database: Towards a FAIR community approved database of cetacean presence in the waters of the Guadeloupe Archipelago, based on citizen science.

BACKGROUND: In the French West Indies, more than 20 species of cetaceans have been observed over the last decades. The recognition of this hotspot of biodiversity of marine mammals, observed in the French Exclusive Economic Zone of the West Indies, motivated the French government to create in 2010 a marine protected area (MPA) dedicated to the conservation of marine mammals: the Agoa Sanctuary. Threats that cetacean populations face are multiple, but well-documented. Cetacean conservation can only be achieved if relevant and reliable data are available, starting by occurrence data. In the Guadeloupe Archipelago and in addition to some data collected by the Agoa Sanctuary, occurrence data are mainly available through the contribution of citizen science and of local stakeholders (i.e. non-profit organisations (NPO) and whale-watchers). However, no observation network has been coordinated and no standards exist for cetacean presence data collection and management. NEW INFORMATION: In recent years, several whale watchers and NPOs regularly collected cetacean observation data around the Guadeloupe Archipelago. Our objective was to gather datasets from three Guadeloupean whale watchers, two NPOs and the Agoa Sanctuary, that agreed to share their data. These heterogeneous data went through a careful process of curation and standardisation in order to create a new extended database, using a newly-designed metadata set. This aggregated dataset contains a total of 4,704 records of 21 species collected in the Guadeloupe Archipelago from 2000 to 2019. The database was called Kakila ("who is there?" in Guadeloupean Creole). The Kakila database was developed following the FAIR principles with the ultimate objective of ensuring sustainability. All these data were transferred into the PNDB repository (Pöle National de Données de Biodiversité, Biodiversity French Data Hub, https://www.pndb.fr).In the Agoa Sanctuary and surrounding waters, marine mammals have to interact with increasing anthropogenic pressure from growing human activities. In this context, the Kakila database fulfils the need for an organised system to structure marine mammal occurrences collected by multiple local stakeholders with a common objective: contribute to the knowledge and conservation of cetaceans living in the French Antilles waters. Much needed data analysis will enable us to identify high cetacean presence areas, to document the presence of rarer species and to determine areas of possible negative interactions with anthropogenic activities.

Physical properties of epilithic river biofilm as a new lead to perform pollution bioassessments in overseas territories.

Chlordecone (CLD) levels measured in the rivers of the French West Indies were among the highest values detected worldwide in freshwater ecosystems, and its contamination is recognised as a severe health, environmental, agricultural, economic, and social issue. In these tropical volcanic islands, rivers show strong originalities as simplified food webs, or numerous amphidromous migrating species, making the bioindication of contaminations a difficult issue. The objective of this study was to search for biological responses to CLD pollution in a spatially fixed and long-lasting component of the rivers in the West Indies: the epilithic biofilm. Physical properties were investigated through complementary analyses: friction, viscosity as well as surface adhesion were analyzed and coupled with measures of biofilm carbon content and exopolymeric substance (EPS) production. Our results have pointed out a mesoscale chemical and physical reactivity of the biofilm that can be correlated with CLD contamination. We were able to demonstrate that epilithic biofilm physical properties can effectively be used to infer freshwater environmental quality of French Antilles rivers. The friction coefficient is reactive to contamination and well correlated to carbon content and EPS production. Monitoring biofilm physical properties could offer many advantages to potential users in terms of effectiveness and ease of use, rather than more complex or time-consuming analyses.

Analysis of interdomain taxonomic patterns in urban street mats.

Streets are constantly crossed by billions of vehicles and pedestrians. Their gutters, which convey stormwater and contribute to waste management, and are important for human health and well-being, probably play a number of ecological roles. Street surfaces may also represent an important part of city surface areas. To better characterize the ecology of this yet poorly explored compartment, we used filtration and DNA metabarcoding to address microbial community composition and assembly across the city of Paris, France. Diverse bacterial and eukaryotic taxonomic groups were identified, including members involved in key biogeochemical processes, along with a number of parasites and putative pathogens of human, animals and plants. We showed that the beta diversity patterns between bacterial and eukaryotic communities were correlated, suggesting interdomain associations. Beta diversity analyses revealed the significance of biotic factors (cohesion metrics) in shaping gutter microbial community assembly and, to a lesser extent, the contribution of abiotic factors (pH and conductivity). Co-occurrences analysis confirmed contrasting non-random patterns both within and between domains of life, specifically when comparing diatoms and fungi. Our results highlight microbial coexistence patterns in streets and reinforce the need to further explore biodiversity in urban ground transportation infrastructures.

Three-dimensional structural evolution of the cuttlefish Sepia officinalis shell from embryo to adult stages.

The cuttlefish shell is an internal structure with a composition and general organization unique among molluscs. Its formation and the structure-function relation are explored during Sepia officinalis development, using computerized axial tomography scanning (CAT-scan) three-dimensional analyses coupled to physical measurements and modelling. In addition to the evolution of the overall form, modifications of the internal structure were identified from the last third embryonic stages to adult. Most of these changes can be correlated to life cycle stages and environmental constraints. Protected by the capsule during embryonic life, the first internal chambers are sustained by isolated pillars formed from the dorsal to the ventral septum. After hatching, the formation of pillars appears to be a progressive process from isolated points to interconnected pillars forming a wall-delineated labyrinthine structure. We analysed the interpillar space, the connectivity and the tortuosity of the labyrinth. The labyrinthine pillar network is complete just prior to the wintering migration, probably to sustain the need to adapt to high pressure and to allow buoyancy regulation. At that time, the connectivity in the pillar network is compensated by an increase in tortuosity, most probably to reduce liquid diffusion in the shell. Altogether these results suggest adjustment of internal calcified structure development to both external forces and physiological needs.

Adhesive gland transcriptomics uncovers a diversity of genes involved in glue formation in marine tube-building polychaetes.

Tube-building sabellariid polychaetes are hermatypic organisms capable of forming vast reefs in highly turbulent marine habitats. Sabellariid worms assemble their tube by gluing together siliceous and calcareous clastic particles using a polyelectrolytic biocement. Here, we performed transcriptomic analyses to investigate the genes that are differentially expressed in the parathorax region, which contains the adhesive gland and tissues, from the rest of the body. We found a large number of candidate genes to be involved in the composition and formation of biocement in two species: Sabellaria alveolata and Phragmatopoma caudata. Our results indicate that the glue is likely to be composed by a large diversity of cement-related proteins, including Poly(S), GY-rich, H-repeat and miscellaneous categories. However, sequences divergence and differences in expression profiles between S. alveolata and P. caudata of cement-related proteins may reflect adaptation to the type of substratum used to build their tube, and/or to their habitat (temperate vs tropical, amplitude of pH, salinity …). Related to the L-DOPA metabolic pathways and linked with the genes that were differentially expressed in the parathorax region, we found that tyrosinase and peroxidase gene families may have undergone independent expansion in the two Sabellariidae species investigated. Our data also reinforce the importance of protein modifications in cement formation. Altogether these new genomic resources help to identify novel transcripts encoding for cement-related proteins, but also important enzymes putatively involved in the chemistry of the adhesion process, such as kinases, and may correspond to new targets to develop biomimetic approaches. STATEMENTS OF SIGNIFICANCE: The diversity of bioadhesives elaborated by marine invertebrates is a tremendous source of inspiration to develop biomimetic approaches for biomedical and technical applications. Recent studies on the adhesion system of mussel, barnacle and sea star had highlighted the usefulness of high-throughput RNA sequencing in accelerating the development of biomimetic adhesives. Adhesion in sandcastle worms, which involves catechol and phosphate chemistries, polyelectrolyte complexes, supramolecular architectures, and a coacervation process, is a useful model to develop multipurpose wet adhesives. Using transcriptomic tools, we have explored the diversity of genes encoding for structural and catalytic proteins involved in cement formation of two sandcastle worm species, Sabellaria alveolata and Phragmatopoma caudata. The important genomic resource generated should help to design novel "blue" adhesives.

Aquatic urban ecology at the scale of a capital: community structure and interactions in street gutters.

In most cities, streets are designed for collecting and transporting dirt, litter, debris, storm water and other wastes as a municipal sanitation system. Microbial mats can develop on street surfaces and form microbial communities that have never been described. Here, we performed the first molecular inventory of the street gutter-associated eukaryotes across the entire French capital of Paris and the non-potable waters sources. We found that the 5782 OTUs (operational taxonomic units) present in the street gutters which are dominated by diatoms (photoautotrophs), fungi (heterotrophs), Alveolata and Rhizaria, includes parasites, consumers of phototrophs and epibionts that may regulate the dynamics of gutter mat microbial communities. Network analyses demonstrated that street microbiome present many species restricted to gutters, and an overlapping composition between the water sources used for street cleaning (for example, intra-urban aquatic networks and the associated rivers) and the gutters. We propose that street gutters, which can cover a significant surface area of cities worldwide, potentially have important ecological roles in the remediation of pollutants or downstream wastewater treatments, might also be a niche for growth and dissemination of putative parasite and pathogens.

Eye Development in Sepia officinalis Embryo: What the Uncommon Gene Expression Profiles Tell Us about Eye Evolution.

In metazoans, there is a remarkable diversity of photosensitive structures; their shapes, physiology, optical properties, and development are different. To approach the evolution of photosensitive structures and visual function, cephalopods are particularly interesting organisms due to their most highly centralized nervous system and their camerular eyes which constitute a convergence with those of vertebrates. The eye morphogenesis in numerous metazoans is controlled mainly by a conserved Retinal Determination Gene Network (RDGN) including pax, six, eya, and dac playing also key developmental roles in non-retinal structures and tissues of vertebrates and Drosophila. Here we have identified and explored the role of Sof-dac, Sof-six1/2, Sof-eya in eye morphogenesis, and nervous structures controlling the visual function in Sepia officinalis. We compare that with the already shown expressions in eye development of Sof-otx and Sof-pax genes. Rhodopsin is the pigment responsible for light sensitivity in metazoan, which correlate to correlate visual function and eye development. We studied Sof-rhodopsin expression during retina differentiation. By in situ hybridization, we show that (1) all of the RDGN genes, including Sof-pax6, are expressed in the eye area during the early developmental stages but they are not expressed in the retina, unlike Sof-otx, which could have a role in retina differentiation; (2) Sof-rhodopsin is expressed in the retina just before vision gets functional, from stage 23 to hatching. Our results evidence a role of Sof-six1/2, Sof-eya, and Sof-dac in eye development. However, the gene network involved in the retinal photoreceptor differentiation remains to be determined. Moreover, for the first time, Sof-rhodopsin expression is shown in the embryonic retina of cuttlefish suggesting the evolutionary conservation of the role of rhodopsin in visual phototransduction within metazoans. These findings are correlated with the physiological and behavioral observations suggesting that S. officinalis is able to react to light stimuli from stage 25 of organogenesis on, as soon as the first retinal pigments appear.

Physiological adjustments and transcriptome reprogramming are involved in the acclimation to salinity gradients in diatoms.

Salinity regimes in estuaries and coastal areas vary with river discharge patterns, seawater evaporation, the morphology of the coastal waterways and the dynamics of marine water mixing. Therefore, microalgae have to respond to salinity variations at time scales ranging from daily to annual cycles. Microalgae may also have to adapt to physical alterations that induce the loss of connectivity between habitats and the enclosure of bodies of water. Here, we integrated physiological assays and measurements of morphological plasticity with a functional genomics approach to examine the regulatory changes that occur during the acclimation to salinity in the estuarine diatom Thalassiosira weissflogii. We found that cells exposed to different salinity regimes for a short or long period presented adjustments in their carbon fractions, silicon pools, pigment concentrations and/or photosynthetic parameters. Salinity-induced alterations in frustule symmetry were observed only in the long-term (LT) cultures. Whole transcriptome analyses revealed a down-regulation of nuclear and plastid encoded genes during the LT response and identified only a few regulated genes that were in common between the ST and LT responses. We propose that in diatoms, one strategy for acclimating to salinity gradients and maintaining optimal cellular fitness could be a reduction in the cost of transcription.

First proteomic analyses of the dorsal and ventral parts of the Sepia officinalis cuttlebone.

Protein compounds constituting mollusk shells are known for their major roles in the biomineralization processes. These last years, a great diversity of shell proteins have been described in bivalves and gastropods allowing a better understanding of the calcification control by organic compounds and given promising applications in biotechnology. Here, we analyzed for the first time the organic matrix of the aragonitic Sepia officinalis shell, with an emphasis on protein composition of two different structures: the dorsal shield and the chambered part. Our results highlight an organic matrix mainly composed of polysaccharide, glycoprotein and protein compounds as previously described in other mollusk shells, with quantitative and qualitative differences between the dorsal shield and the chamber part. Proteomic analysis resulted in identification of only a few protein compounds underlining the lack of reference databases for Sepiidae. However, most of them contain domains previously characterized in matrix proteins of aragonitic shell-builder mollusks, suggesting ancient and conserved mechanisms of the aragonite biomineralization processes within mollusks. BIOLOGICAL SIGNIFICANCE: The cuttlefish's inner shell, better known under the name "cuttlebone", is a complex mineral structure unique in mollusks and involved in tissue support and buoyancy regulation. Although it combines useful properties as high compressive strength, high porosity and high permeability, knowledge about organic compounds involved in its building remains limited. Moreover, several cuttlebone organic matrix studies reported data very different from each other or from other mollusk shells. Thus, this study provides 1) an overview of the organization of the main mineral structures found in the S. officinalis shell, 2) a reliable baseline about its organic composition, and 3) a first descriptive proteomic approach of organic matrices found in the two main parts of this shell. These data will contribute to the general knowledge about mollusk biomineralization as well as in the identification of protein compounds involved in the Sepiidae shell calcification.

Multiparametric analyses reveal the pH-dependence of silicon biomineralization in diatoms.

Diatoms, the major contributors of the global biogenic silica cycle in modern oceans, account for about 40% of global marine primary productivity. They are an important component of the biological pump in the ocean, and their assemblage can be used as useful climate proxies; it is therefore critical to better understand the changes induced by environmental pH on their physiology, silicification capability and morphology. Here, we show that external pH influences cell growth of the ubiquitous diatom Thalassiosira weissflogii, and modifies intracellular silicic acid and biogenic silica contents per cell. Measurements at the single-cell level reveal that extracellular pH modifications lead to intracellular acidosis. To further understand how variations of the acid-base balance affect silicon metabolism and theca formation, we developed novel imaging techniques to measure the dynamics of valve formation. We demonstrate that the kinetics of valve morphogenesis, at least in the early stages, depends on pH. Analytical modeling results suggest that acidic conditions alter the dynamics of the expansion of the vesicles within which silica polymerization occurs, and probably its internal pH. Morphological analysis of valve patterns reveals that acidification also reduces the dimension of the nanometric pores present on the valves, and concurrently overall valve porosity. Variations in the valve silica network seem to be more correlated to the dynamics and the regulation of the morphogenesis process than the silicon incorporation rate. These multiparametric analyses from single-cell to cell-population levels demonstrate that several higher-level processes are sensitive to the acid-base balance in diatoms, and its regulation is a key factor for the control of pattern formation and silicon metabolism.

Genome-wide transcriptome analyses of silicon metabolism in Phaeodactylum tricornutum reveal the multilevel regulation of silicic acid transporters.

BACKGROUND: Diatoms are largely responsible for production of biogenic silica in the global ocean. However, in surface seawater, Si(OH)(4) can be a major limiting factor for diatom productivity. Analyzing at the global scale the genes networks involved in Si transport and metabolism is critical in order to elucidate Si biomineralization, and to understand diatoms contribution to biogeochemical cycles. METHODOLOGY/PRINCIPAL FINDINGS: Using whole genome expression analyses we evaluated the transcriptional response to Si availability for the model species Phaeodactylum tricornutum. Among the differentially regulated genes we found genes involved in glutamine-nitrogen pathways, encoding putative extracellular matrix components, or involved in iron regulation. Some of these compounds may be good candidates for intracellular intermediates involved in silicic acid storage and/or intracellular transport, which are very important processes that remain mysterious in diatoms. Expression analyses and localization studies gave the first picture of the spatial distribution of a silicic acid transporter in a diatom model species, and support the existence of transcriptional and post-transcriptional regulations. CONCLUSIONS/SIGNIFICANCE: Our global analyses revealed that about one fourth of the differentially expressed genes are organized in clusters, underlying a possible evolution of P. tricornutum genome, and perhaps other pennate diatoms, toward a better optimization of its response to variable environmental stimuli. High fitness and adaptation of diatoms to various Si levels in marine environments might arise in part by global regulations from gene (expression level) to genomic (organization in clusters, dosage compensation by gene duplication), and by post-transcriptional regulation and spatial distribution of SIT proteins.