Changes in planktonic microbial components in interaction with juvenile oysters during a mortality episode in the Thau lagoon (France)

Abstract

Oysters modify the planktonic microbial community structure by their filtration and NH 4 excretion activities. While many studies have been conducted on this subject with adult oysters, none had been carried out in situ with juveniles. Pacific oyster juveniles (Magallana gigas, previously Crassostrea gigas) died massively all over the world since 2008 in relation with OsHV-1 infection. During mortality episodes, sick and dead oysters are not separated from healthy live ones, and left to decay in the surrounding environment, with unknown consequences for the nutrient cycle and planktonic microbial components (PMC). The present study aimed to elucidate for the first time the interactions between oyster juveniles and PMC during a mortality episode. Innovative 425-L pelagic chambers were deployed weekly in situ around oyster lanterns along a stocking-density gradient in the Thau Mediterranean lagoon (France) before, during and after an oyster mortality episode, from April to May 2015. This study reveals (i) significant changes of planktonic microbial community structure during mortality episodes, with a proliferation of picoplankton (<3 μm) and ciliates (Balanion sp., Uronema sp.) within 2 weeks when mortality rates and numbers of moribund juvenile oysters were highest. These changes were probably induced by oyster tissue leaching, decomposition and mineralization, which probably began during the moribund period, as suggested by an increase of PO 4 concentration and N:P ratio decrease, (ii) oyster juveniles mainly retained 3-20 μm plankton. In contrast to adults, picophytoplankton and small heterotrophic flagellates (<3 μm) were significantly depleted in the presence of oyster juveniles. Depletion of picoplankton occurred only at the starting of the mortality episode and during the moribund phase. (iii) Oyster juvenile filtration and mortality shifted the planktonic microbial structure toward a heterotrophic microbial system, where ciliates and heterotrophic flagellates acted as a trophic link between picoplankton and oysters. The next stage of our investigation is to examine the effect of a mortality episode on pathogen fluxes in the water column, exploring their relationships with planktonic Please note that this is an author-produced PDF of an article accepted for publication following peer review. The definitive publisher-authenticated version is available on the publisher Web site.components and dead oyster flesh. Highlights► The planktonic microbial components (PMC) change during OsHV-1 oyster juvenile mortality. ► Picophytoplankton and ciliates increase during infection and mortality periods. ► Filtration and mortality of juvenile oysters shift PMC toward a heterotrophic system.

In situ characterisation of pathogen dynamics during a Pacific oyster mortality syndrome episode

“…Although many studies have explored disease-controlling factors (Petton et al, 2013(Petton et al, , 2015aWhittington et al, 2015a) and the consequences of infection for oysters (Corporeau et al, 2014;Green et al, 2015Green et al, , 2016Tamayo et al, 2014), few have investigated the consequences of these mortality events for the environment. Indeed, unlike in most other animal production industries, sick and dead individuals are not separated from conspecifics in shellfish farms, but remain in the rearing environment until their flesh totally disappears (Richard et al 2017(Richard et al , 2019. The mortality of oyster juveniles has been shown to increase ammonium and phosphate fluxes at the oyster interface (Richard et al, 2017) and to reduce the N/P ratio due to decomposition of the flesh (Richard et al, 2017(Richard et al, , 2019.…”

“…Indeed, unlike in most other animal production industries, sick and dead individuals are not separated from conspecifics in shellfish farms, but remain in the rearing environment until their flesh totally disappears (Richard et al 2017(Richard et al , 2019. The mortality of oyster juveniles has been shown to increase ammonium and phosphate fluxes at the oyster interface (Richard et al, 2017) and to reduce the N/P ratio due to decomposition of the flesh (Richard et al, 2017(Richard et al, , 2019. Oyster mortality has been also shown to induce changes in microbial planktonic components during the infection and mortality peak, with proliferation of picophytoplankton and heterotrophic ciliates (Balanion, Uronema) (Richard et al, 2019).…”

“…The mortality of oyster juveniles has been shown to increase ammonium and phosphate fluxes at the oyster interface (Richard et al, 2017) and to reduce the N/P ratio due to decomposition of the flesh (Richard et al, 2017(Richard et al, , 2019. Oyster mortality has been also shown to induce changes in microbial planktonic components during the infection and mortality peak, with proliferation of picophytoplankton and heterotrophic ciliates (Balanion, Uronema) (Richard et al, 2019). Ciliates may proliferate in response to a bacterial proliferation associated with decaying oyster tissue (Richard et al, 2019).…”

“…Oyster mortality has been also shown to induce changes in microbial planktonic components during the infection and mortality peak, with proliferation of picophytoplankton and heterotrophic ciliates (Balanion, Uronema) (Richard et al, 2019). Ciliates may proliferate in response to a bacterial proliferation associated with decaying oyster tissue (Richard et al, 2019). Beyond disturbing the ecosystem, the fact sick and dead individuals remain in the environment could also favour cross-contamination and disease spread.…”

Impact of oysters as top predators on microbial food web dynamics: a modelling approach with parameter optimisation

“…Bivalve activities exert a non-neutral influence on coastal ecosystems (e.g., Dupuy et al 1999, 2000, Chapelle et al 2000, Mostajir et al 2015, and an increase in the number of shellfish farms in specific areas will certainly impact their nearby ecosystems. The roles of bivalves can be summarised by three main functions (Richard et al 2019): filtration (Dupuy et al 2000, Trottet et al 2008, excretion (Mazouni 2004, Richard et al 2007, Jansen et al 2011, and biodeposition (Callier et al 2006, 2009, Robert et al 2013. Filtration by oysters selectively removes suspended living or non-living particles from the water column (Gosling 2015, Bayne 2017.…”