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Background Progressive climate-induced ocean acidification (OA) impacts marine life in ways that are difficult to predict but are likely to become exacerbated over generations. Although marine fishes can balance internal acid-base homeostasis efficiently, indirect ionic regulation effects that alter neurosensory systems can result in behavioural abnormalities. In marine invertebrates, OA can also affect immune system function, but whether this is the case in marine fishes of ecological and commercial importance is not yet understood. Farmed fish are highly susceptible to disease outbreak yet strategies for overcoming such threats in the wake of OA are wanting. Here, we exposed two generations of the European sea bass (Dicentrarchus labrax) to end-of-century predicted CO2 levels (IPCC RCP8.5), with parents being exposed for four years and their offspring for two years. Our design included a transcriptomic analysis of the olfactory rosette (collected from the F1 offspring) and a viral challenge (exposing F1 offspring to betanodavirus) where we assessed survival rates. Results We discovered long-term intergenerational molecular trade-offs in both sensory and immune systems. Specifically, RNA-Seq analysis of the olfactory rosette, the peripheral olfactory organ, from two-year-old F1 offspring revealed extensive regulation in genes involved in ion transport and neuronal signalling, including GABAergic signalling. We also detected extensive OA-induced intergenerational up-regulation of genes associated with odour transduction, synaptic plasticity, neuron excitability and wiring and down-regulation of genes involved in energy metabolism. In addition, intergenerational exposure to OA induced up-regulation of genes involved in innate antiviral immunity (pathogen recognition receptors and interferon-stimulated genes) in combination with down-regulation of the protein biosynthetic machinery. Consistently, OA-exposed F1 fish challenged with betanodavirus, which causes damage to the nervous system of marine fish, had acquired improved resistance. Conclusion F1 exposed to OA-intergenerational acclimation showed superior viral resistance, though as their metabolic and odour transduction programs were altered, odour-mediated behaviours might be consequently altered. Our results reveal that trade-offs in adaptive plastic responses is a core feature of the olfactory epithelium transcriptome in OA-exposed fish, suggesting that intergenerational plasticity propagate with progressive exposure to OA and will have important consequences for how cultured and wild fish interacts with its environment.

To evaluate the stability and resilience1 of coastal ecosystem communities to perturbations that occurred during the Anthropocene,2 pre-industrial biodiversity baselines inferred from paleoarchives are needed.3,4 The study of ancient DNA (aDNA) from sediments (sedaDNA)5 has provided valuable information about past dynamics of microbial species6, 7, 8 and communities9, 10, 11, 12, 13, 14, 15, 16, 17, 18 in relation to ecosystem variations. Shifts in planktonic protist communities might significantly affect marine ecosystems through cascading effects,19, 20, 21 and therefore the analysis of this compartment is essential for the assessment of ecosystem variations. Here, sediment cores collected from different sites of the Bay of Brest (northeast Atlantic, France) allowed ca. 1,400 years of retrospective analyses of the effects of human pollution on marine protists. Comparison of sedaDNA extractions and metabarcoding analyses with different barcode regions (V4 and V7 18S rDNA) revealed that protist assemblages in ancient sediments are mainly composed of species known to produce resting stages. Heavy-metal pollution traces in sediments were ascribed to the World War II period and coincided with community shifts within dinoflagellates and stramenopiles. After the war and especially from the 1980s to 1990s, protist genera shifts followed chronic contaminations of agricultural origin. Community composition reconstruction over time showed that there was no recovery to a Middle Ages baseline composition. This demonstrates the irreversibility of the observed shifts after the cumulative effect of war and agricultural pollutions. Developing a paleoecological approach, this study highlights how human contaminations irreversibly affect marine microbial compartments, which contributes to the debate on coastal ecosystem preservation and restoration.

WOS:000661079300001; Bioinformatic analysis of eDNA metabarcoding data is a crucial step toward rigorously assessing biodiversity. Many programs are now available for each step of the required analyses, but their relative abilities at providing fast and accurate species lists have seldom been evaluated. We used simulated mock communities and real fish eDNA metabarcoding data to evaluate the performance of 13 bioinformatic programs and pipelines to retrieve fish occurrence and read abundance using the 12S mt rRNA gene marker. We used four indices to compare the outputs of each program with the simulated samples: sensitivity, F-measure, root-mean-square error (RMSE) on read relative abundances, and execution time. We found marked differences among programs only for the taxonomic assignment step, both in terms of sensitivity, F-measure and RMSE. Running time was highly different between programs for each step. The fastest programs with best indices for each step were assembled into a pipeline. We compared this pipeline to pipelines constructed from existing toolboxes (OBITools, Barque, and QIIME 2). Our pipeline and Barque obtained the best performance for all indices and appear to be better alternatives to highly used pipelines for analysing fish eDNA metabarcoding data when a complete reference database is available. Analysis on real eDNA metabarcoding data also indicated differences for taxonomic assignment and execution time only. This study reveals major differences between programs during the taxonomic assignment step. The choice of algorithm for the taxonomic assignment can have a significant impact on diversity estimates and should be made according to the objectives of the study.

International audience; Elevated amounts of atmospheric CO2 are causing ocean acidification (OA) that may affect marine organisms including fish species. While several studies carried out in fish revealed that OA induces short term dysfunction in sensory systems including regulation of neurons activity in olfactory epithelium, information on the effects of OA on other physiological processes and actors is scarcer. In the present study we focused our attention on a European sea bass (Dicentrarchus labrax) sghC1q gene, a member of the C1q-domain-containing (C1qDC) protein family. In vertebrates, C1qDC family includes actors involved in different physiological processes including immune response and synaptic organization. Our microsynteny analysis revealed that this sghC1q gene is the orthologous gene in European sea bass to zebrafish (Danio rerio) cbln11 gene. We cloned the full length cbln11 mRNA and identified the different domains (the signal peptide, the coiled coil region and the globular C1q domain) of the deduced protein sequence. Investigation of mRNA expression by qPCR and in situ hybridization revealed that cbln11 gene is especially expressed in the non-sensory epithelium of the olfactory rosette at larval and adult stages. The expression of cbln11 mRNA was analysed by qPCR in the first generation (FO) of European sea bass broodstock exposed since larval stages to water pH of 8.0 (control) or 7.6 (predicted for year 2100) and in their offspring (F1) maintained in the environmental conditions of their parents. Our results showed that cbln11 mRNA expression level was lower in larvae exposed to OA then up-regulated at adult stage in the olfactory rosette of F0 and that this up-regulation is maintained under OA at larval and juvenile stages in F1. Overall, this work provides evidence of a transgenerational inheritance of OA-induced up-regulation of cbln11 gene expression in European sea bass. Further studies will investigate the potential immune function of cbln11 gene and the consequences of these regulations, as well as the possible implications in terms of fitness and adaptation to OA in European sea bass.

International audience; Deciphering the ecology of marine obligate hydrocarbonoclastic bacteria (MOHCB) is of crucial importance for understanding their success in occupying distinct niches in hydrocarbon-contaminated marine environments after oil spills. In marine coastal sediments, MOHCB are particularly subjected to extreme fluctuating conditions due to redox oscillations several times a day as a result of mechanical (tide, waves and currents) and biological (bioturbation) reworking of the sediment. The adaptation of MOHCB to the redox oscillations was investigated by an experimental ecology approach, subjecting a hydrocarbon-degrading microbial community to contrasting oxygenation regimes including permanent anoxic conditions, anoxic/oxic oscillations and permanent oxic conditions. The most ubiquitous MOHCB, Alcanivorax and Cycloclasticus, showed different behaviors, especially under anoxic/oxic oscillation conditions, which were more favorable for Alcanivorax than for Cycloclasticus. The micro-diversity of 16S rRNA gene transcripts from these genera revealed specific ecotypes for different oxygenation conditions and their dynamics. It is likely that such ecotypes allow the colonization of distinct ecological niches that may explain the success of Alcanivorax and Cycloclasticus in hydrocarbon-contaminated coastal sediments during oil-spills.