Bacteriomic Profiling of Branchial Lesions Induced by Neoparamoeba perurans Challenge Reveals Commensal Dysbiosis and an Association with Tenacibaculum dicentrarchi in AGD-Affected Atlantic Salmon (Salmo salar L.).

Joel Slinger,James W Wynne,Mark B Adams

doi:10.3390/microorganisms8081189

Abstract

Amoebic gill disease is a parasitic condition that commonly affects marine farmed Atlantic salmon. The causative agent, Neoparamoeba perurans, induces a marked proliferation of the gill mucosa and focal superficial necrosis upon branchial lesions. The effect that amoebic branchialitis has upon gill associated commensal bacteria is unknown. A 16S rRNA sequencing approach was employed to profile changes in bacterial community composition, within amoebic gill disease (AGD)-affected and non-affected gill tissue. The bacterial diversity of biopsies with and without diseased tissue was significantly lower in the AGD-affected fish compared to uninfected fish. Furthermore, within the AGD-affected tissue, lesions appeared to contain a significantly higher abundance of the Flavobacterium, Tenacibaculum dicentrarchi compared to adjunct unaffected tissues. Quantitative PCR specific to both N. perurans and T. dicentrarchi was used to further examine the co-abundance of these known fish pathogens. A moderate positive correlation between these pathogens was observed. Taken together, the present study sheds new light on the complex interaction between the host, parasite and bacterial communities during AGD progression. The role that T. dicentrarchi may play in this complex relationship requires further investigation.

Highlights

The outer gill surface of teleost fish represents a unique and dynamic landscape where microbial antigens within the external milieu attempt to invade the mucosal interface, whilst the host immune system attempts to overcome these continuous insults [1,2]
Gross clinical signs of amoebic gill disease (AGD) including raised multifocal lesions on the gill surface were observed in AGD affected fish (Figure 1)
Gill lesions indicative of AGD were not observed in salmon unexposed to N. perurans

Summary

Introduction

The outer gill surface of teleost fish represents a unique and dynamic landscape where microbial antigens within the external milieu attempt to invade the mucosal interface, whilst the host immune system attempts to overcome these continuous insults [1,2]. A delicate balance exists between commensal and opportunistic pathogens, under certain conditions such as disease or poor environmental conditions this microbial balance can be lost, leading to a dysbiosis where opportunistic species dominate [4]. Regular aquaculture operations can influence bacterial communities, with soy-based dietary additives [8] and husbandry practices such as seawater transfer and handling [9,10] having significant impacts on the internal and external microbiota in respective in vivo studies with Atlantic salmon. Commensal probiotic treatments can provide some microbial resilience to finfish, as observed in both black molly (Poecilia sphenops) and Arctic char (Salvelinus alpinus), when a probiotic additive was seen to lessen the detrimental impact of two significant pathogenic bacterial species, Vibrio anguillarum and Flavobacterium psychrophilum respectively [11,12]

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