Reduced Antioxidant Response of the Fan Mussel Pinna nobilis Related to the Presence of Haplosporidium pinnae.

Antonio Box,Salud Deudero,Silvia Tejada,Silvia Tejada,Silvia Tejada,José María Valencia,José María Valencia,Xavier Capó,Gaetano Catanese,Gaetano Catanese,Amalia Grau,Antoni Sureda,Antoni Sureda

doi:10.3390/pathogens9110932

Abstract

The endemic fan mussel (Pinna nobilis) in the Mediterranean Sea is at high risk of disappearance due to massive mortality events. The aim of the study was to evaluate the antioxidant response of P. nobilis collected in the Balearic Islands (Western Mediterranean) before and after the mass mortality event. Individuals collected before (between 2011 and 2012) and after (between 2016 and 2017) the event were analyzed by histological, molecular, and biochemical methods to compare pathogenic loads and biochemical responses. All the individuals collected during 2016–2017 presented symptoms of the disease and were positive for Haplosporidium pinnae, while acid-fast bacteria or/and Gram-negative bacteria were detected in some individuals of both sampling periods. The activities of the antioxidant enzymes catalase and superoxide dismutase in the gills were significantly lower in P. nobilis affected with the parasite compared to those in the asymptomatic ones, while levels of malondialdehyde, as an indicator of lipid peroxidation, were higher in infected individuals. When analyzing the differential effects of H. pinnae and Mycobacterium sp. on P. nobilis, it was observed that significant effects on biomarkers were only observed in the presence of H. pinnae. Co-infection of P. nobilis by H. pinnae with other pathogens such as Mycobacterium sp. constitutes a serious problem due to its high mortality rate in the Balearic Island waters. This concerning situation for P. nobilis is favored by a reduction in antioxidant defenses related to H. pinnae infection that induces oxidative stress and cell damage.

Highlights

The fan mussel Pinna nobilis (Linnaeus, 1758) is a Mediterranean endemic bivalve and one of the largest bivalves in the world, reaching up to 120 cm in length [1]
The results of the histological and molecular biology analyses evidenced the absence of H. pinnae in the P. nobilis individuals collected between 2011 and 2012, when the mass mortality event had not been reported on the west coast of Mallorca yet
Mycobacterium sp. and Gram-negative bacteria were detected in both sampling periods (Table 1, Figure 2)

Summary

Introduction

The fan mussel Pinna nobilis (Linnaeus, 1758) is a Mediterranean endemic bivalve and one of the largest bivalves in the world, reaching up to 120 cm in length [1]. P. nobilis populations have progressively decreased due to anthropogenic impacts, mainly related to the destruction of their habitats and anchorages [3,4]. This species was included in Annex II of the Barcelona Convention (1992) and in Annex IV of the EU Habitats Directive [5]. Other authors described a probable association with other pathogens to the mortality of the fan mussels, such as Mycobacterium sp. [9,10]

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Discussion

Conclusion