Impact of Marine Aquaculture on the Microbiome Associated with Nearby Holobionts: The Case of Patella caerulea Living in Proximity of Sea Bream Aquaculture Cages.

Giorgia Palladino,Silvia Turroni,Arianna Mancuso,Elena Biagi,Fiorella Prada,Simone Rampelli,Grazia Marina Quero,Marco Candela,Margherita Musella,Daniel Scicchitano,Anne Mette Seyfarth

doi:10.3390/microorganisms9020455

Giorgia Palladino, Silvia Turroni + Show 9 more

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https://doi.org/10.3390/microorganisms9020455

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Abstract

Aquaculture plays a major role in the coastal economy of the Mediterranean Sea. This raises the issue of the impact of fish cages on the surrounding environment. Here, we explore the impact of aquaculture on the composition of the digestive gland microbiome of a representative locally dwelling wild holobiont, the grazer gastropod Patella caerulea, at an aquaculture facility located in Southern Sicily, Italy. The microbiome was assessed in individuals collected on sea bream aquaculture cages and on a rocky coastal tract located about 1.2 km from the cages, as the control site. Patella caerulea microbiome variations were explained in the broad marine metacommunity context, assessing the water and sediment microbiome composition at both sites, and characterizing the microbiome associated with the farmed sea bream. The P. caerulea digestive gland microbiome at the aquaculture site was characterized by a lower diversity, the loss of microorganisms sensitive to heavy metal contamination, and by the acquisition of fish pathogens and parasites. However, we also observed possible adaptive responses of the P. caerulea digestive gland microbiome at the aquaculture site, including the acquisition of putative bacteria able to deal with metal and sulfide accumulation, highlighting the inherent microbiome potential to drive the host acclimation to stressful conditions.

Highlights

The P. caerulea digestive glands (DG) microbiome was characterized by a lower diversity with respect to environmental communities (Figure 2B), the trend did not always reach the statistical significance
The P. caerulea DG microbiome was characterized by a lower diversity with respect to environmental communities (Figure 2B), the trend did not always reach the statistical significance (Wilcoxon rank-sum test controlled for multiple testing using false discovery rate (FDR); limpets vs. sedsediment p-value ≤ 0.05, limpets vs. seawater p-value 0.09 and 0.2 for Faith PD index and iment p-value ≤ 0.05, limpets vs. seawater p-value 0.09 and 0.2 for Faith PD index and observed number ofnumber observedofASVs, respectively)
The health and functionality of the marine and coastal ecosystems are tightly linked to the resident environmental microbiomes, as well as to the ones associated with local holobionts

Summary

Introduction

Consequences are shifts in nutrients and carbon fluxes, pH decline, and oxygen depletion in the sea floor, resulting in ammonia and hydrogen sulfide accumulation [4,8]. Such conditions modify the benthic assemblages of fauna and seagrass, affecting the whole food web [9]. It has been demonstrated that the proximity of fish farming cages affects the survival of grazers and other macro-fauna trophic groups, even further than the mere sedimentation zone [1,10]

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