Dynamic interactions of fish skin microbiomes with their aquatic environments and the impacts of antibiotic exposures in aquaculture
McMurtrie, J
Date: 4 March 2024
Thesis or dissertation
Publisher
University of Exeter
Degree Title
PhD in Biological Sciences
Abstract
Aquaculture is a crucial food sector to meet food demands for the growing human population. Finfish culture in earthen aquaculture ponds is the most dominant form of production globally, largely occurring in Asian countries. Antibiotics are widely used in an attempt to combat disease, which is one of the greatest threats to the production ...
Aquaculture is a crucial food sector to meet food demands for the growing human population. Finfish culture in earthen aquaculture ponds is the most dominant form of production globally, largely occurring in Asian countries. Antibiotics are widely used in an attempt to combat disease, which is one of the greatest threats to the production and expansion of aquaculture. This antibiotic (mis)use brings human and environmental concerns, but often with little regulatory monitoring. Limited research has been conducted to understand the complex microbial interactions within earthen aquaculture ponds, particularly the microbes harboured at the fish skin mucosal surface which are critical for the support of fish health and disease resilience. This work focuses on the widely farmed finfish tilapia and utilises high-throughput sequencing approaches to reveal the dynamic interface between fish skin microbiomes and their aquatic environment; knowledge which is then applied to assess the impact of antibiotic exposures in aquaculture.
Field assessments of aquaculture ponds in Malawi highlight the inherent variability of tilapia skin microbiomes, with the aquatic environment shown to be an integral determinant by explaining 50% of divergence in microbial community compositions. The majority of microbial taxa are shared between the microbiomes of pond water and tilapia skin, but they are assembled in different compositions and conserved taxa of the tilapia skin are evident. These conserved taxa were studied to assess their response to an antibiotic exposure of Nile tilapia (Oreochromis niloticus) in an experimental outdoor earthen aquaculture pond system in Bangladesh. Here, important commensals, such as Cetobacterium, and putative pathobionts, such as Aeromonas, were transiently depleted and enriched, respectively, in the tilapia skin microbiome in response to antibiotic exposure. Alpha diversity was also reduced, suggesting antibiotics allow a subset of taxa to become more dominant in this community. However, a more general disruption to tilapia skin microbiome compositions was not apparent. Instead, microbiome plasticity in response to temporally fluctuating environmental conditions was a more influential determinant. The functionality of the tilapia skin and pond water microbial communities were also impacted by antibiotic exposure through the transient selection of antimicrobial resistance genes, specifically tetA, tetE, tetA(58) and tetB(P), conferring resistance to the target antibiotic oxytetracycline. There was no evidence to suggest this experimental antibiotic exposure impacted the mobilisation of antimicrobial resistance genes, however, the aquaculture pond environment was found to harbour a diverse resistome, highlighting the potential risks posed by sustained antibiotic misusage. Overall, this work suggests a short-term therapeutic dose of oxytetracycline presents limited risks to fish health and for the development and dissemination of antimicrobial resistance.
Collectively, the work presented in this thesis identifies the intricate and dynamic relationship of the fish skin microbiome with the pond environment for tilapia grown in earthen ponds. The variations identified in microbiome responses to stressors, such as antibiotics, highlight the impact of environmental conditions and host factors as key determinants of these microbiomes. A deeper comprehension of these microbial systems and their interplay with the aquatic environment will be critical to optimise aquaculture conditions and mitigate the impacts of disease, paving the way for a sustainable expansion of aquaculture production.
Doctoral Theses
Doctoral College
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