Interactions between Filter-Feeding Bivalves and Toxic Diatoms: Influence on the Feeding Behavior of Crassostrea gigas and Pecten maximus and on Toxin Production by Pseudo-nitzschia.

Aurore Sauvey,Marie Pavie,Hélène Hégaret,Bertrand Le Roy,Christophe Lelong,Orianne Jolly,Françoise Denis,Juliette Fauchot

doi:10.3390/toxins13080577

Abstract

Among Pseudo-nitzschia species, some produce the neurotoxin domoic acid (DA), a source of serious health problems for marine organisms. Filter-feeding organisms—e.g., bivalves feeding on toxigenic Pseudo-nitzschia spp.—are the main vector of DA in humans. However, little is known about the interactions between bivalves and Pseudo-nitzschia. In this study, we examined the interactions between two juvenile bivalve species—oyster (Crassostrea gigas) and scallop (Pecten maximus)—and two toxic Pseudo-nitzschia species—P. australis and P. fraudulenta. We characterized the influence of (1) diet composition and the Pseudo-nitzschia DA content on the feeding rates of oysters and scallops, and (2) the presence of bivalves on Pseudo-nitzschia toxin production. Both bivalve species fed on P. australis and P. fraudulenta. However, they preferentially filtered the non-toxic Isochrysis galbana compared to Pseudo-nitzschia. The presence of the most toxic P. australis species resulted in a decreased clearance rate in C. gigas. The two bivalve species accumulated DA in their tissues (up to 0.35 × 10−3 and 5.1 × 10−3 µg g−1 for C. gigas and P. maximus, respectively). Most importantly, the presence of bivalves induced an increase in the cellular DA contents of both Pseudo-nitzschia species (up to 58-fold in P. fraudulenta in the presence of C. gigas). This is the first evidence of DA production by Pseudo-nitzschia species stimulated in the presence of filter-feeding bivalves. The results of this study highlight complex interactions that can influence toxin production by Pseudo-nitzschia and accumulation in bivalves. These results will help to better understand the biotic factors that drive DA production by Pseudo-nitzschia and bivalve contamination during Pseudo-nitzschia blooms.

Highlights

The pennate diatoms Pseudo-nitzschia are cosmopolitan [1,2,3]
I. galbana and P. fraudulenta cell concentrations decreased over time in all replicates in the presence of C. gigas (Figure 1A), whereas they increased in the absence of oysters
The reciprocal influence between P. fraudulenta/P. australis and C. gigas/P. maximus observed in the present study shows that further metabolomics studies are needed to explore the mechanisms and the chemical cues associated with the stimulation of domoic acid (DA) production and the alteration of the feeding behavior during bivalve/Pseudo-nitzschia interactions

Summary

Introduction

The pennate diatoms Pseudo-nitzschia are cosmopolitan [1,2,3]. About 60 species are currently described, and some of them are considered toxic, i.e., able to produce a neurotoxin—domoic acid (DA) [4,5]. About 60 species are currently described, and some of them are considered toxic, i.e., able to produce a neurotoxin—. DA is transferred to various organisms within marine food webs when toxic Pseudo-nitzschia species are ingested by bivalves (mussels, oysters, scallops), zooplankton (copepods), or planktivorous fish [1,3]. These marine organisms serve as vectors of the toxin to higher levels of the food web. Do Pseudo-nitzschia species produce DA, but they excrete it in their environment, e.g., [8,9,10]. Exposure to dissolved DA (dDA) can have negative effects on the development of marine life [11,12,13]

Objectives

Methods

Results

Discussion

Conclusion