Microbiome of Co-cultured Fish Exhibits Host Selection and Niche Differentiation at the Organ Scale.

Zhimin Zhang,Rong Tang,Li Li,Dapeng Li,Weitong Xu

doi:10.3389/fmicb.2019.02576

Zhimin Zhang, Rong Tang + Show 3 more

Open Access

https://doi.org/10.3389/fmicb.2019.02576

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Abstract

Fish are the most widespread aquaculture species and maintain complex associations with microbial consortiums. However, the ecology of these associations present in multiple microhabitats in fish remains elusive, especially on the microbial assembly in fish external (skin and gill) and internal (stomach and intestine) niches, and the relationship with the rearing environment. To understand host dependence and niche differentiation of organ-specific microbiome signatures using a 16S rRNA gene-based sequencing technique, we systematically provided characterizations of a comparative framework relevant to the microbiome of stomach, regional intestine, skin, and gill in two important farmed fish species, herbivorous grass carp (Ctenopharyngodon idella) and carnivorous southern catfish (Silurus meridionalis), and of the rearing water. The different feeding habits of grass carp and southern catfish showed a significant separation of microbial community structure, with great compositional differences across body sites within each species. Site-driven divergences relied on host species: the same types of microhabitats between grass carp and southern catfish harbored differential microbiome. Additionally, body sites had remarkably distinct communities and displayed lower alpha diversity compared to rearing water. Unexpectedly, the stomach of southern catfish had the highest microbial diversity in the digestive tract of the two co-cultured fish species. For external sites within each species, a higher diversity occurred in gill of grass carp and in skin of southern catfish. Our results unveil different topographical microbiome signatures of the co-cultured species, indicating host selection in individual-level microbial assemblages and niche differentiation at the organ scale. This work represents a foundation for understanding the comprehensive microbial ecology of cohabiting farmed fish, suggesting potential applications associated with fish microbiome that urgently needs to be assessed in polycultured operations in aquaculture.

Highlights

Hosts naturally harbor complex microbial population resident in multiple body habitats
Recent studies have reported that dietary interventions alter gut microbiota, which tends to be stable within a week (Hao et al, 2017), and that 2 weeks of transfer experiments at different aquatic environments reveal changes in microbial community of host skin (Bletz et al, 2016)
No temporal differences were observed in the microbiome community of grass carp (PERMANOVA, P > 0.05) and southern catfish (PERMANOVA, P > 0.05) as well as their rearing water (PERMANOVA, P > 0.05) based on BrayCurtis distances, as shown by the clear overlaps within each host or the environment sample sources (Figure 2A)

Summary

Introduction

Hosts naturally harbor complex microbial population resident in multiple body habitats. Gut is the most extensively studied anatomical site for microbial ecology with the advance of high-throughput sequencing. It is an ideal reservoir for microbial colonization in humans (Lee and Mazmanian, 2010; Nicholson et al, 2012) and in numerous terrestrial and aquatic vertebrates (Pascoe et al, 2017). The effects of geographic habitats have been reported on the microbial community of specific hosts like humans, rodents, poultry, and fish (Bolnick et al, 2014; Zhang et al, 2015; Pascoe et al, 2017). A major challenge to our understanding of microbial ecology in animals is that it is rather difficult to unravel one effect from the other due to highly variable geographic environments and host complexity

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