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      Environmental distribution and seasonal dynamics of Marteilia refringens and Bonamia ostreae, two protozoan parasites of the European flat oyster, Ostrea edulis

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          Abstract

          Introduction

          Marteilia refringens and Bonamia ostreae are protozoan parasites responsible for mortalities of farmed and wild flat oysters Ostrea edulis in Europe since 1968 and 1979, respectively. Despite almost 40 years of research, the life-cycle of these parasites is still poorly known, especially regarding their environmental distribution.

          Methods

          We carried out an integrated field study to investigate the dynamics of M. refringens and B. ostreae in Rade of Brest, where both parasites are known to be present. We used real-time PCR to monitor seasonally over four years the presence of both parasites in flat oysters. In addition, we used previously developed eDNA based-approaches to detect parasites in planktonic and benthic compartments for the last two years of the survey.

          Results

          M. refringens was detected in flat oysters over the whole sampling period, sometimes with a prevalence exceeding 90%. It was also detected in all the sampled environmental compartments, suggesting their involvement in parasite transmission and overwintering. In contrast, B. ostreae prevalence in flat oysters was low and the parasite was almost never detected in planktonic and benthic compartments. Finally, the analysis of environmental data allowed describing the seasonal dynamics of both parasites in Rade of Brest: M. refringens was more detected in summer and fall than in winter and spring, contrary to B. ostreae which showed higher prevalence in winter and spring.

          Discussion

          The present study emphasizes the difference between M. refringens and B. ostreae ecology, the former presenting a wider environmental distribution than the latter, which seems closely associated to flat oysters. Our findings highlight the key role of planktonic and benthic compartments in M. refringens transmission and storage or potential overwintering, respectively. More generally, we provide here a method that could be useful not only to further investigate non cultivable pathogens life-cycle, but also to support the design of more integrated surveillance programs.

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          Most cited references61

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              Environmental DNA.

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                Author and article information

                Contributors
                Journal
                Front Cell Infect Microbiol
                Front Cell Infect Microbiol
                Front. Cell. Infect. Microbiol.
                Frontiers in Cellular and Infection Microbiology
                Frontiers Media S.A.
                2235-2988
                13 June 2023
                2023
                : 13
                : 1154484
                Affiliations
                [1] 1 Adaptation et Santé des Invertébrés Marins (ASIM), Ifremer , La Tremblade, France
                [2] 2 POS3IDON, R&D Department , Saint Malo, France
                [3] 3 Laboratoire des Sciences de l’Environnement Marin (LEMAR), Unité Mixte de Recherche (UMR) 6539 Ifremer/Université de Bretagne Occidentale (UBO)/Institut de Recherche pour le Développement (IRD)/Centre National de la Recherche Scientifique (CNRS) , Ifremer, Argenton-en-Landunvez, France
                Author notes

                Edited by: Ana Born-Torrijos, Royal Netherlands Institute for Sea Research (NIOZ), Netherlands

                Reviewed by: Maria M. Costa, Instituto de Investigaciones Marinas, Spain; Anush Kosakyan, University of Modena and Reggio Emilia, Italy

                *Correspondence: Isabelle Arzul, Isabelle.Arzul@ 123456ifremer.fr
                Article
                10.3389/fcimb.2023.1154484
                10293890
                9bfe92bb-9483-4a72-98e2-85240d1f5582
                Copyright © 2023 Mérou, Lecadet, Ubertini, Pouvreau and Arzul

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 30 January 2023
                : 16 May 2023
                Page count
                Figures: 7, Tables: 1, Equations: 0, References: 69, Pages: 14, Words: 7106
                Funding
                We also thank the European Union Reference Laboratory for Molluscs Diseases (EURL for Molluscs Diseases), the French National Research Agency (ANR) project ENVICOPAS (15-CE35-0004) and the European Maritime Affairs and Fisheries Fund (FEAMP) project (n° FEAMP 17/2215675) Flat Oyster REcoVERy project (FOREVER) for funding this research.
                Categories
                Cellular and Infection Microbiology
                Original Research
                Custom metadata
                Parasite and Host

                Infectious disease & Microbiology
                marteilia refringens,bonamia ostreae,ostrea edulis,parasite,life-cycle,integrated field study,edna

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