Abstract
The mucosal surfaces and associated microbiota of fish are an important primary barrier and provide the first line of defense against potential pathogens. An understanding of the skin and gill microbial assemblages and the factors which drive their composition may provide useful insights into the broad dynamics of fish host–microbial relationships, and may reveal underlying changes in health status. This is particularly pertinent to cultivated systems whereby various stressors may led to conditions (like enteritis) which impinge on productivity. As an economically important species, we assessed whether the outer-surface bacterial communities reflect a change in gut health status of cultivated Yellowtail Kingfish (Seriola lalandi). Active bacterial assemblages were surveyed from RNA extracts from swabs of the skin and gills by constructing Illumina 16S rRNA gene amplicon libraries. Proteobacteria and Bacteroidetes were predominant in both the skin and gills, with enrichment of key β-proteobacteria in the gills (Nitrosomonadales and Ferrovales). Fish exhibiting early stage chronic lymphocytic enteritis comprised markedly different global bacterial assemblages compared to those deemed healthy and exhibiting late stages of the disease. This corresponded to an overall loss of diversity and enrichment of Proteobacteria and Actinobacteria, particularly in the gills. In contrast, bacterial assemblages of fish with late stage enteritis were generally similar to those of healthy individuals, though with some distinct taxa. In conclusion, gut health status is an important factor which defines the skin and gill bacterial assemblages of fish and likely reflects changes in immune states and barrier systems during the early onset of conditions like enteritis. This study represents the first to investigate the microbiota of the outer mucosal surfaces of fish in response to underlying chronic gut enteritis, revealing potential biomarkers for assessing fish health in commercial aquaculture systems.
Highlights
The outermost surfaces of animals represent an important primary barrier, in fish where they share an intimate relationship with their watery surroundings
A total of 36 fish were sampled under the auspices of a commercial aquaculture enterprise from temperate waters of southern Australia according to industry best practice veterinary care and included 12 from a control sea cage where no obvious signs of infection or a health problem were observed in the population prior to sampling (“healthy” group, sea cage A) and 24 from a sea cage containing mixed populations of individuals displaying early and late stages of enteritis (n = 12/group, sea cage B) (Table 1), as confirmed earlier by necropsy and histopathological assessment
Despite the same starting status, a general decline in the mean fork length and weight was observed across the groups from healthy to early to late stage enteritis, where the mean weights were 3.4, 3.0, and 1.4 kg, and the fork length was 61.4, 59.7, and 49.3 cm, respectively (Table 1 and Supplementary Figures S2A,B)
Summary
The outermost surfaces of animals represent an important primary barrier, in fish where they share an intimate relationship with their watery surroundings. As an added feature, the epithelia of the skin and gills are coated in a secretion of mucus that is continuously replaced, and comprises immunologically active molecules that arise from the underlying lymphoid tissues which parallel those of the gut, hindering opportunistic pathogens (Magnadottir, 2010; Esteban, 2012; Rakers et al, 2013; Xu et al, 2013; Peatman et al, 2015; Derome et al, 2016) This mucus layer is host to an array of indigenous microbiota in which bacteria are predominant (Esteban, 2012; Llewellyn et al, 2014; Merrifield and Rodiles, 2015; Lokesh and Kiron, 2016). Balanced and complex interplays within the mucus layer are key for disease resistance (Jani and Briggs, 2014; Lowrey et al, 2015) and are pivotal for supporting health and fitness (Gómez and Balcázar, 2008)
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