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

IntroductionMarteilia 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...

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Main Authors: Nicolas Mérou, Cyrielle Lecadet, Martin Ubertini, Stéphane Pouvreau, Isabelle Arzul
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-06-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2023.1154484/full
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author Nicolas Mérou
Nicolas Mérou
Cyrielle Lecadet
Martin Ubertini
Stéphane Pouvreau
Isabelle Arzul
author_facet Nicolas Mérou
Nicolas Mérou
Cyrielle Lecadet
Martin Ubertini
Stéphane Pouvreau
Isabelle Arzul
author_sort Nicolas Mérou
collection DOAJ
description IntroductionMarteilia 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.MethodsWe 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.ResultsM. 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.DiscussionThe 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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spelling doaj.art-9dd4719ee3dc4037a2e2add9ff569d9e2023-06-13T04:28:19ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882023-06-011310.3389/fcimb.2023.11544841154484Environmental distribution and seasonal dynamics of Marteilia refringens and Bonamia ostreae, two protozoan parasites of the European flat oyster, Ostrea edulisNicolas Mérou0Nicolas Mérou1Cyrielle Lecadet2Martin Ubertini3Stéphane Pouvreau4Isabelle Arzul5Adaptation et Santé des Invertébrés Marins (ASIM), Ifremer, La Tremblade, FrancePOS3IDON, R&D Department, Saint Malo, FranceAdaptation et Santé des Invertébrés Marins (ASIM), Ifremer, La Tremblade, FrancePOS3IDON, R&D Department, Saint Malo, FranceLaboratoire 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, FranceAdaptation et Santé des Invertébrés Marins (ASIM), Ifremer, La Tremblade, FranceIntroductionMarteilia 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.MethodsWe 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.ResultsM. 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.DiscussionThe 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.https://www.frontiersin.org/articles/10.3389/fcimb.2023.1154484/fullMarteilia refringensBonamia ostreaeOstrea edulisparasitelife-cycleintegrated field study
spellingShingle Nicolas Mérou
Nicolas Mérou
Cyrielle Lecadet
Martin Ubertini
Stéphane Pouvreau
Isabelle Arzul
Environmental distribution and seasonal dynamics of Marteilia refringens and Bonamia ostreae, two protozoan parasites of the European flat oyster, Ostrea edulis
Frontiers in Cellular and Infection Microbiology
Marteilia refringens
Bonamia ostreae
Ostrea edulis
parasite
life-cycle
integrated field study
title Environmental distribution and seasonal dynamics of Marteilia refringens and Bonamia ostreae, two protozoan parasites of the European flat oyster, Ostrea edulis
title_full Environmental distribution and seasonal dynamics of Marteilia refringens and Bonamia ostreae, two protozoan parasites of the European flat oyster, Ostrea edulis
title_fullStr Environmental distribution and seasonal dynamics of Marteilia refringens and Bonamia ostreae, two protozoan parasites of the European flat oyster, Ostrea edulis
title_full_unstemmed Environmental distribution and seasonal dynamics of Marteilia refringens and Bonamia ostreae, two protozoan parasites of the European flat oyster, Ostrea edulis
title_short Environmental distribution and seasonal dynamics of Marteilia refringens and Bonamia ostreae, two protozoan parasites of the European flat oyster, Ostrea edulis
title_sort environmental distribution and seasonal dynamics of marteilia refringens and bonamia ostreae two protozoan parasites of the european flat oyster ostrea edulis
topic Marteilia refringens
Bonamia ostreae
Ostrea edulis
parasite
life-cycle
integrated field study
url https://www.frontiersin.org/articles/10.3389/fcimb.2023.1154484/full
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