Microbial community dynamics of farmed Atlantic salmon gill microbiomes during amoebic gill disease episodes
Birlanga, Victor B.
Birlanga, Victor B.
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Publication Date
2022-06-14
Type
Thesis
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Abstract
Gill pathologies, especially the Amoebic Gill Disease (AGD), present one of the main health concerns for marine aquaculture worldwide. In Ireland alone, Atlantic salmon (Salmo salarL.) production in fish farms was 12,000 tonnes worth €114.5 millionin 2018, but the mortality of the livestock in marine farms due to AGDreaches an average between 10-20% every year. As of yet, the most common means to reduce AGD is to control the abundance of its first aetiological agent, the free-living amoebaNeoparamoeba perurans, that typically produces white mucoid patches on infected gills. There are two main ways to diagnose AGD: i)by scoring gills based on the abundance of white patches onthem; ii)quantifying N. peruransabundance ongillsusing quantitative-PCR assays. However, these diagnosis toolsare only useful in confirming the amoeba colonisation on gills, being unable to determine the vulnerability to AGD prior to the colonisation.Indeed, our understanding of AGD is far fromcomplete; specifically, the role of the gill microbiome from seawater farmed salmon and how it responds to anAGDepisodeis limited. The present thesis mainly aimed to characterise the prokaryotic gill microbiome from farmed Atlantic salmon (Salmo salarL.) before and during an AGD episodeusing high-throughput sequencing approaches. Afirst sampling campaign was carried out in a single Irish fish farm, where gill and mucus from gills were sampled from Atlantic salmonfrom May to October in 2017. A novel DNA extraction procedure was optimised and used to get the microbiome DNA from entire gill arches, with the objective to avoid under-sampling and taxa under-representation that could happen as a result of characterising the gill microbiome from part of a gill arch. On the other hand, the microbiome DNA in mucus samples was extracted and isolated aiming to test the efficacy of mucus sampling as a suitable alternative source to gills for AGD microbiome analyses. A set of variables, such as AGD gill scores, N. peruransabundance on gills, fish condition factor, water temperature, salinity, oxygen,and turbidity,was monitoredto track the development of the AGD episode and environmental variations. After an AGDonset, the prokaryotic community on salmon gills shifted towardslower diversity and less balance. In addition, the possible correlation between the development of AGD and the prokaryotic microbiome from gill and mucus samples was suggestedafter an AGD episode. Bacterial communities from gill and mucus samples presented close similarities, establishing mucus scrapings as a suitable non-lethal substitute for gill sampling for partial characterisation of the whole-gill prokaryotic community. Average AGD-associated mortalities in certain fish farms have been punctually reported to reach a 60-80% loss in stocks, higher than the annual average between 10-20% every year in most of the farm locations. In addition, frequency of AGD outbreaks seemedto differ betweensalmon-producing regions. Asecond sampling campaign aimed to characterise the prokaryotic microbiome on gills from farmed Atlantic salmon at six disparate fish farms before and duringAGD. Thus, from June to December 2018, salmon gills were sampled from each of the six farms alongthe West coast of Irelandat various sampling points. The gill microbiome DNA was extracted and isolated from following the DNA extraction optimised in the previous sampling campaign. Additionally, a set of variables was monitored during the campaign to track the AGD development and environmental variations. AGD severity was similar between farms; but, the AGD development was still correlatedwith changes ingill microbiome from every fish farm. However, the strong influence of the different environmental factors made it difficult to discern patterns. During the hottest time of the year, we found a decreasing gradient in gill microbiome diversity from northern to southern fish farms. In addition, the location of each fish farm significantly influencedthe bacterial community, in combination with theAGD development.Variations in the environmental factors greatly impactedthe gill microbiome, but there were evidencesuggesting the connection between the gill microbiome and AGD. Hence, athird sampling campaignaimed to further investigate the possible connection between the gill microbiome and AGD by describing the impact of the disease on the bacterial community on gills, but in a controlledlaboratory challenge. Additionally, functional diets were also recently shown to have a positive impact on the survivaland physiological response to AGD on salmon. Therefore, we also tested the effect of various functional diets on AGD severity and the gill microbiome in AGD-affected Atlantic salmon.Atlantic salmon were separated and treated distinctly in four tanks, sampling gills at each timepoint.The gill microbiome DNA was extracted and isolated following the DNA extraction optimised in the first sampling campaign. In addition, water samples were taken from each experimental tank to compare the gill and water microbiome, and to determine the effect of the functional diets on the surrounding seawater microbiome. The fish condition factor, AGD gill scores,andN. perurans abundance on gills were tracked.Unexpectedly, the diversity and evenness of the prokaryotic gill microbiome increased in AGD-affected salmon. Additionally,a tested functional diet impacted thegill microbiome before AGD, while the various diets differentiate the water microbiome duringthe whole laboratory trial. Bacterial communities were distinct between gill and water samples. These results further evidenced the impact of the AGD on the gill microbiome of Atlantic salmon, and also provided some initial evidence of the influence of the diet on both, the gill and the water microbiome.Our knowledge about the AGD onset and development is still far from complete; however, results in the present thesis proved that the AGD impacted the gill microbiome from farmed Atlantic salmon along the Irish West coast, and in laboratory conditions.
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NUI Galway