Abstract

The external mucosal surfaces of the fish harbor complex microbial communities, which may play pivotal roles in the physiological, metabolic, and immunological status of the host. Currently, little is known about the composition and role of these communities, whether they are species and/or tissue specific and whether they reflect their surrounding environment. Co-culture of fish, a common practice in semi-intensive aquaculture, where different fish species cohabit in the same contained environment, is an easily accessible and informative model toward understanding such interactions. This study provides the first in-depth characterization of gill and skin microbiomes in co-cultured Nile tilapia (Oreochromis niloticus) and grey mullet (Mugil capito) in semi-intensive pond systems in Egypt using 16S rRNA gene-based amplicon sequencing. Results showed that the microbiome composition of the external surfaces of both species and pond water was dominated by the following bacterial phyla: Proteobacteria, Fusobacteriota, Firmicutes, Planctomycetota, Verrucomicrobiota, Bacteroidota, and Actinobacteriota. However, water microbial communities had the highest abundance and richness and significantly diverged from the external microbiome of both species; thus, the external autochthonous communities are not a passive reflection of their allochthonous communities. The autochthonous bacterial communities of the skin were distinct from those of the gill in both species, indicating that the external microbiome is likely organ specific. However, gill autochthonous communities were clearly species specific, whereas skin communities showed higher commonalities between both species. Core microbiome analysis identified the presence of shared core taxa between both species and pond water in addition to organ-specific taxa within and between the core community of each species. These core taxa included possibly beneficial genera such as Uncultured Pirellulaceae, Exiguobacterium, and Cetobacterium and opportunistic potential pathogens such as Aeromonas, Plesiomonas, and Vibrio. This study provides the first in-depth mapping of bacterial communities in this semi-intensive system that in turn provides a foundation for further studies toward enhancing the health and welfare of these cultured fish and ensuring sustainability.

Highlights

  • The external surfaces of fish are considered the first and foremost line of immunological defense, owing to their intimate contact with the external aquatic milieu

  • Bacterial community richness was measured by calculating Chao1, which is a non-parametric estimator of the number of species in a community that gives more weight to low-abundance species (Kim et al, 2017)

  • Alpha-diversity indices identify a significant difference in bacterial richness and evenness between the external surface microbiome of both species and the rearing pond water

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Summary

Introduction

The external surfaces of fish are considered the first and foremost line of immunological defense, owing to their intimate contact with the external aquatic milieu. Skin and gill surfaces are covered with mucus, which is continuously secreted by goblet cells This mucus layer is an active immunological barrier consisting of mucins, lysozyme, proteases, antimicrobial peptides, lectins, proteins, and immunoglobulins (Esteban, 2012). These mucosal surfaces are colonized by a highly diverse commensal microbial community, the microbiome (Merrifield and Rodiles, 2015). The microbiome is understood to play a fundamental role in maintaining overall fish health and is likely impacted through host-dependent regulatory pathways and environmental interaction These mucosal communities may protect the host against pathogenic bacteria through competitive exclusion and mucus homeostasis, facilitating waste product excretion and improving host mucosal immunity (Lee and Mazmanian, 2010; van Kessel et al, 2016). There appears to be an acceptance for a key role for these external surface microbial communities in finfish health, little is known about their composition and their relationship with their environment as opposed to the finfish gastrointestinal microbiome (Perry et al, 2020)

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