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14 pages, 1725 KiB

Open AccessArticle

Evaluation of Low Temperature and Salinity as a Treatment of Atlantic Salmon against Amoebic Gill Disease

by Jemma Hudson, Mark Adams, Khattapan Jantawongsri, Tim Dempster and Barbara F. Nowak

Microorganisms 2022, 10(2), 202; https://doi.org/10.3390/microorganisms10020202 - 18 Jan 2022

Cited by 3 | Viewed by 1886

Abstract

Amoebic gill disease (AGD) is a significant health issue for Atlantic salmon farmed in a marine environment. While the disease is currently managed using freshwater or hydrogen peroxide baths, there is a need to develop other treatments. The aims of this study were [...] Read more.

Amoebic gill disease (AGD) is a significant health issue for Atlantic salmon farmed in a marine environment. While the disease is currently managed using freshwater or hydrogen peroxide baths, there is a need to develop other treatments. The aims of this study were to examine the effect of salinity (0 ppt and 35 ppt) and temperature (3 °C and 15 °C) on attachment and survival of Neoparamoeba perurans in vitro over short exposure times (15 min and 2 h) and to assess the efficacy of reduced temperature (3 °C) as treatment for Atlantic salmon affected by AGD. In vitro freshwater 3 °C was at least as effective as freshwater 15 °C and the attachment was significantly lower after 2 h in freshwater 3 °C than freshwater 15 °C. In vivo there was no difference between the fish treated with freshwater 15 °C for 2 h or freshwater 3 °C. This study showed that despite exposure to low temperature reducing attachment of N. perurans to their substrate in vitro, 15 min cold-water bath treatment was not more effective at reducing AGD in Atlantic salmon than current commercial 2 h freshwater bath. Full article

(This article belongs to the Special Issue Amoebic Gill Disease)

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14 pages, 1327 KiB

Open AccessArticle

Differential Exoproteome and Biochemical Characterisation of Neoparamoeba perurans

by Kerrie Ní Dhufaigh, Natasha Botwright, Eugene Dillon, Ian O’Connor, Eugene MacCarthy and Orla Slattery

Microorganisms 2021, 9(6), 1258; https://doi.org/10.3390/microorganisms9061258 - 09 Jun 2021

Cited by 2 | Viewed by 2300

Abstract

Infection with the protozoan ectoparasite Neoparamoeba perurans, the causative agent of AGD, remains a global threat to salmonid farming. This study aimed to analyse the exoproteome of both an attenuated and virulent N. perurans isolate using proteomics and cytotoxicity testing. A disproportionate [...] Read more.

Infection with the protozoan ectoparasite Neoparamoeba perurans, the causative agent of AGD, remains a global threat to salmonid farming. This study aimed to analyse the exoproteome of both an attenuated and virulent N. perurans isolate using proteomics and cytotoxicity testing. A disproportionate presence of proteins from the co-cultured microbiota of N. perurans was revealed on searching an amalgamated database of bacterial, N. perurans and Amoebozoa proteins. LC-MS/MS identified 33 differentially expressed proteins, the majority of which were upregulated in the attenuated exoproteome. Proteins of putative interest found in both exoproteomes were maltoporin, ferrichrome-iron receptor, and putative ferric enterobactin receptor. Protease activity remained significantly elevated in the attenuated exoproteome compared with the virulent exoproteome. Similarly, the attenuated exoproteome had a significantly higher cytotoxic effect on rainbow trout gill cell line (RTgill W1) cells compared with the virulent exoproteome. The presence of a phosphatase and serine protease in the virulent exoproteome may facilitate AGD infection but do not appear to be key players in causing cytotoxicity. Altogether, this study reveals prolonged culture of N. perurans affects the exoproteome composition in favour of nutritional acquisition, and that the current culturing protocol for virulent N. perurans does not facilitate the secretion of virulence factors. Full article

(This article belongs to the Special Issue Amoebic Gill Disease)

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15 pages, 3528 KiB

Open AccessArticle

Host Response of Atlantic Salmon (Salmo salar) Re-Inoculated with Paramoeba perurans

by Michelle McCormack, Anita Talbot, Eugene Dillon, Ian O’Connor and Eugene MacCarthy

Microorganisms 2021, 9(5), 993; https://doi.org/10.3390/microorganisms9050993 - 05 May 2021

Cited by 1 | Viewed by 1929

Abstract

In aquaculture, recurrence rates of amoebic gill disease (AGD) caused by the ectoparasite Paramoeba perurans are high and no prophylactic strategies exist for disease prevention. In this study, Atlantic salmon (Salmo salar) were initially inoculated with P. perurans and following the [...] Read more.

In aquaculture, recurrence rates of amoebic gill disease (AGD) caused by the ectoparasite Paramoeba perurans are high and no prophylactic strategies exist for disease prevention. In this study, Atlantic salmon (Salmo salar) were initially inoculated with P. perurans and following the development of amoebic gill disease were treated with freshwater immersion on day 21 and day 35 post inoculation. Fish were re-inoculated following a negative qPCR analysis for the presence of P. perurans. The gill host immune response was investigated at 7, 14, and 18 days post re-inoculation. Differential proteome expression of immune related proteins was assessed by comparison of each time point against naïve controls. In the gill, some proteins of the innate immune system were expressed in response to gill re-colonization by P. perurans, while no features of adaptive immunity were found to be differentially expressed. Many of the proteins identified are novel in the context of AGD and their expression profiles suggest that their roles in the response to disease development and progression in single or multiple infections warrant further investigation. Full article

(This article belongs to the Special Issue Amoebic Gill Disease)

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21 pages, 1893 KiB

Open AccessArticle

The Effect of Antimicrobial Treatment upon the Gill Bacteriome of Atlantic Salmon (Salmo salar L.) and Progression of Amoebic Gill Disease (AGD) In Vivo

by Joel Slinger, Mark B. Adams, Chris N. Stratford, Megan Rigby and James W. Wynne

Microorganisms 2021, 9(5), 987; https://doi.org/10.3390/microorganisms9050987 - 02 May 2021

Cited by 11 | Viewed by 3264

Abstract

Branchial surfaces of finfish species contain a microbial layer rich in commensal bacteria which can provide protection through competitive colonization and production of antimicrobial products. Upon disturbance or compromise, pathogenic microbiota may opportunistically infiltrate this protective barrier and initiate disease. Amoebic gill disease [...] Read more.

Branchial surfaces of finfish species contain a microbial layer rich in commensal bacteria which can provide protection through competitive colonization and production of antimicrobial products. Upon disturbance or compromise, pathogenic microbiota may opportunistically infiltrate this protective barrier and initiate disease. Amoebic gill disease (AGD) is a globally significant health condition affecting salmonid mariculture. The current study examined whether altering the diversity and/or abundance of branchial bacteria could influence the development of experimentally induced AGD. Here, we challenged Atlantic salmon (Salmo salar) with Neoparamoeba perurans in a number of scenarios where the bacterial community on the gill was altered or in a state of instability. Administration of oxytetracycline (in-feed) and chloramine-T (immersion bath) significantly altered the bacterial load and diversity of bacterial taxa upon the gill surface, and shifted the community profile appreciably. AGD severity was marginally higher in fish previously subjected to chloramine-T treatment following 21 days post-challenge. This research suggests that AGD progression and severity was not clearly linked to specific bacterial taxa present in these systems. However, we identified AGD associated taxa including known pathogenic genus (Aliivibrio, Tenacibaculum and Pseudomonas) which increased in abundance as AGD progressed. Elucidation of a potential role for these bacterial taxa in AGD development is warranted. Full article

(This article belongs to the Special Issue Amoebic Gill Disease)

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17 pages, 4760 KiB

Open AccessArticle

Evaluation of the Infectious Potential of Neoparamoeba perurans Following Freshwater Bathing Treatments

by Richard S. Taylor, Joel Slinger, Chris Stratford, Megan Rigby and James W. Wynne

Microorganisms 2021, 9(5), 967; https://doi.org/10.3390/microorganisms9050967 - 29 Apr 2021

Cited by 2 | Viewed by 3090

Abstract

Freshwater bathing for 2–3 h is the main treatment to control amoebic gill disease of marine-farmed Atlantic salmon. Recent in vitro studies have demonstrated that amoebae (Neoparamoeba perurans) detach when exposed to freshwater and that some eventually reattach to culture plates [...] Read more.

Freshwater bathing for 2–3 h is the main treatment to control amoebic gill disease of marine-farmed Atlantic salmon. Recent in vitro studies have demonstrated that amoebae (Neoparamoeba perurans) detach when exposed to freshwater and that some eventually reattach to culture plates when returned to seawater. Here, we evaluated the potential for gill-detached N. perurans to survive a commercially relevant treatment and infect AGD-naïve fish and whether holding used bathwater for up to 6 h post treatment would lower infectivity. AGD-affected fish were bathed in freshwater for 2 h. Naïve salmon were exposed to aliquots of the used bathwater after 2, 4, 6 and 8 h. The inoculation was performed at 30 ppt for 2 h, followed by gradual dilution with seawater. Sampling at 20 days post inoculation (dpi) and 40 dpi confirmed rapid AGD development in fish inoculated in 2 h used bathwater, but a slower AGD development following exposure to 4 h bathwater. AGD signs were variable and reduced following longer bathwater holding times. These results suggest that viable amoebae are likely returned to seawater following commercial freshwater treatments, but that the risk of infection can be reduced by retention of bathwater before release. Full article

(This article belongs to the Special Issue Amoebic Gill Disease)

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20 pages, 2565 KiB

Open AccessArticle

Investigation of the Initial Host Response of Naïve Atlantic Salmon (Salmo salar) Inoculated with Paramoeba perurans

by Michelle McCormack, Eugene Dillon, Ian O’Connor and Eugene MacCarthy

Microorganisms 2021, 9(4), 746; https://doi.org/10.3390/microorganisms9040746 - 02 Apr 2021

Cited by 2 | Viewed by 2174

Abstract

Amoebic Gill Disease (AGD), caused by the ectoparasite Paramoeba perurans is characterised by hyperplasia of the gill epithelium and lamellar fusion. In this study, the initial host response of naïve Atlantic salmon (Salmo salar) inoculated with P. perurans was investigated. Using [...] Read more.

Amoebic Gill Disease (AGD), caused by the ectoparasite Paramoeba perurans is characterised by hyperplasia of the gill epithelium and lamellar fusion. In this study, the initial host response of naïve Atlantic salmon (Salmo salar) inoculated with P. perurans was investigated. Using gel-free proteomic techniques and mass spectrometry gill and serum samples were analysed at 7 timepoints (2, 3, 4, 7, 9, 11 and 14 days) post-inoculation with P. perurans. Differential expression of immune related proteins was assessed by comparison of protein expression from each time point against naïve controls. Few host immune molecules associated with innate immunity showed increased expression in response to gill colonisation by amoebae. Furthermore, many proteins with roles in immune signalling, phagocytosis and T-cell proliferation were found to be inhibited upon disease progression. Initially, various immune factors demonstrated the anticipated increase in expression in response to infection in the serum while some immune inhibition became apparent at the later stages of disease progression. Taken together, the pro-immune trend observed in serum, the lack of a robust early immune response in the gill and the diversity of those proteins in the gill whose altered expression negatively impact the immune response, support the concept of a pathogen-derived suppression of the host response. Full article

(This article belongs to the Special Issue Amoebic Gill Disease)

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16 pages, 4017 KiB

Open AccessArticle

Gill Mucus and Gill Mucin O-glycosylation in Healthy and Amebic Gill Disease-Affected Atlantic Salmon

by John Benktander, János T. Padra, Ben Maynard, George Birchenough, Natasha A. Botwright, Russel McCulloch, James W. Wynne, Sinan Sharba, Kristina Sundell, Henrik Sundh and Sara K. Lindén

Microorganisms 2020, 8(12), 1871; https://doi.org/10.3390/microorganisms8121871 - 26 Nov 2020

Cited by 11 | Viewed by 3044

Abstract

Amoebic gill disease (AGD) causes poor performance and death in salmonids. Mucins are mainly comprised by carbohydrates and are main components of the mucus covering the gill. Since glycans regulate pathogen binding and growth, glycosylation changes may affect susceptibility to primary and secondary [...] Read more.

Amoebic gill disease (AGD) causes poor performance and death in salmonids. Mucins are mainly comprised by carbohydrates and are main components of the mucus covering the gill. Since glycans regulate pathogen binding and growth, glycosylation changes may affect susceptibility to primary and secondary infections. We investigated gill mucin O-glycosylation from Atlantic salmon with and without AGD using liquid chromatography–mass spectrometry. Gill mucin glycans were larger and more complex, diverse and fucosylated than skin mucins. Confocal microscopy revealed that fucosylated mucus coated sialylated mucus strands in ex vivo gill mucus. Terminal HexNAcs were more abundant among O-glycans from AGD-affected Atlantic salmon, whereas core 1 structures and structures with acidic moieties such as N-acetylneuraminic acid (NeuAc) and sulfate groups were less abundant compared to non-infected fish. The fucosylated and NeuAc-containing O-glycans were inversely proportional, with infected fish on the lower scale of NeuAc abundance and high on fucosylated structures. The fucosylated epitopes were of three types: Fuc-HexNAc-R, Gal-[Fuc-]HexNAc-R and HexNAc-[Fuc-]HexNAc-R. These blood group-like structures could be an avenue to diversify the glycan repertoire to limit infection in the exposed gills. Furthermore, care must be taken when using skin mucus as proxy for gill mucus, as gill mucins are distinctly different from skin mucins. Full article

(This article belongs to the Special Issue Amoebic Gill Disease)

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Review

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12 pages, 270 KiB

Open AccessReview

Experimental Challenge Models and In Vitro Models to Investigate Efficacy of Treatments and Vaccines against Amoebic Gill Disease

by Jemma Hudson and Barbara F. Nowak

Microorganisms 2021, 9(4), 710; https://doi.org/10.3390/microorganisms9040710 - 30 Mar 2021

Cited by 2 | Viewed by 1890

Abstract

Amoebic Gill Disease (AGD) severely affects salmonid mariculture due to fish losses and costs associated with management of the disease. Continued research into management solutions, including new treatments and vaccine development, is highly important for the future of salmonid production worldwide. This requires [...] Read more.

Amoebic Gill Disease (AGD) severely affects salmonid mariculture due to fish losses and costs associated with management of the disease. Continued research into management solutions, including new treatments and vaccine development, is highly important for the future of salmonid production worldwide. This requires both in vitro (both pathogen only and host-pathogen models) and in vivo (disease challenge) testing. Challenge models are still widely varied, in particular with regard to: infection methods (cohabitation or immersion), source of the pathogen (isolated from infected fish or cultured), infectious dose, environmental conditions (in particular temperature) and the endpoints across experimental treatment and vaccine studies which makes comparisons between studies difficult. This review summarises in vitro assays, the challenge methods and endpoints used in studies of experimental treatments and vaccines for AGD. Full article

(This article belongs to the Special Issue Amoebic Gill Disease)

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9 pages, 4013 KiB

Open AccessCase Report

Assessment of Marine Gill Disease in Farmed Atlantic Salmon (Salmo salar) in Chile Using a Novel Total Gross Gill Scoring System: A Case Study

by Sophie Fridman, Smaragda Tsairidou, Nilantha Jayasuriya, Halina Sobolewska, Alastair Hamilton, Carlos Lobos, Ross D. Houston, Hamish Rodger, James Bron and Tharangani Herath

Microorganisms 2021, 9(12), 2605; https://doi.org/10.3390/microorganisms9122605 - 16 Dec 2021

Cited by 4 | Viewed by 3995

Abstract

Gill disorders have become more prevalent and widespread in finfish aquaculture in recent years. Their aetiology is often considered to be multifactorial. Effective diagnosis, control and prevention are hindered by the lack of standardised methodologies to characterise the aetiological agents, which produce an [...] Read more.

Gill disorders have become more prevalent and widespread in finfish aquaculture in recent years. Their aetiology is often considered to be multifactorial. Effective diagnosis, control and prevention are hindered by the lack of standardised methodologies to characterise the aetiological agents, which produce an array of clinical and pathological presentations. The aim of this study was to define a novel gross pathological scoring system suitable for field-based macroscopic assessment of complex or multifactorial gill disease in farmed Atlantic salmon, using samples derived from a gill disease outbreak in Chile. Clinical assessment of gross gill morphology was performed, and gill samples were collected for qPCR and histology. A novel total gill scoring system was developed, which assesses gross pathological changes combining both the presumptive or healed amoebic gill disease (AGD) and the presence of other types of gill lesions. This scoring system offers a standardised approach to characterise the severe proliferative pathologies in affected gills. This total gill scoring system can substantially contribute to the development of robust mitigation strategies and could be used as an indicator trait for incorporating resistance to multifactorial gill disease into breeding goals. Full article

(This article belongs to the Special Issue Amoebic Gill Disease)

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