Whole gut microbiome composition of damselfish and cardinalfish before and after reef settlement.

Darren J Parris,Danielle L Dixson,Rohan M Brooker,Michael A Morgan,Frank J Stewart

doi:10.7717/peerj.2412

Darren J Parris, Danielle L Dixson + Show 3 more

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https://doi.org/10.7717/peerj.2412

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Journal: PeerJ	Publication Date: Aug 31, 2016
Citations: 79	License type: CC BY 4.0

Affiliation: Georgia Institute of Technology, University of Delaware

Abstract

The Pomacentridae (damselfish) and Apogonidae (cardinalfish) are among the most common fish families on coral reefs and in the aquarium trade. Members of both families undergo a pelagic larvae phase prior to settlement on the reef, where adults play key roles in benthic habitat structuring and trophic interactions. Fish-associated microbial communities (microbiomes) significantly influence fish health and ecology, yet little is known of how microbiomes change with life stage. We quantified the taxonomic (16S rRNA gene) composition of whole gut microbiomes from ten species of damselfish and two species of cardinalfish from Lizard Island, Australia, focusing specifically on comparisons between pelagic larvae prior to settlement on the reef versus post-settlement juvenile and adult individuals. On average, microbiome phylogenetic diversity increased from pre- to post-settlement, and was unrelated to the microbial composition in the surrounding water column. However, this trend varied among species, suggesting stochasticity in fish microbiome assembly. Pre-settlement fish were enriched with bacteria of the Endozoicomonaceae, Shewanellaceae, and Fusobacteriaceae, whereas settled fish harbored higher abundances of Vibrionaceae and Pasteurellaceae. Several individual operational taxonomic units, including ones related to Vibrio harveyi, Shewanella sp., and uncultured Endozoicomonas bacteria, were shared between both pre and post-settlement stages and may be of central importance in the intestinal niche across development. Richness of the core microbiome shared among pre-settlement fish was comparable to that of settled individuals, suggesting that changes in diversity with adulthood are due to the acquisition or loss of host-specific microbes. These results identify a key transition in microbiome structure across host life stage, suggesting changes in the functional contribution of microbiomes over development in two ecologically dominant reef fish families.

Highlights

Animals harbor diverse microbial communities that influence key aspects of host health, development, and behavior
As observed in other fish species (Spanggaard et al, 2000; Al-Harbi & Naim Uddin, 2004; Martin-Antonio et al, 2007; Sullam et al, 2012; Xing et al, 2013), Pomacentrid and Apogonid gut microbiomes were dominated by Gammaproteobacteria of the Pseudoaltermonadaceae, Endozoicimonaceae, Vibrionaceae, and Shewanellaceae with these Families constituting 80% (±10.3 SD) and 67% (±6.7 SD) of all sequence reads in pre- and post-settlement fishes, respectively (Fig. S1), key differences in the relative abundance of microbial families were evident
Persistence over development may be an important indicator of commensal or mutualistic taxa ubiquitous to reef fish. These results describe a diverse gut microbiome in two abundant reef fish families and highlight the importance of life stage in structuring microbiome composition

Summary

Introduction

Animals harbor diverse microbial communities that influence key aspects of host health, development, and behavior. Studies of fish gut microbiomes have focused primarily on commercial or model species, with most targeting only a small number of host or microbial taxa (Roeselers et al, 2011; Clements et al, 2014; Llewellyn et al, 2014) These studies raise the possibility of a core set of fish gut microbes shared across diverse hosts, notably a dominance by bacteria of the Gammaproteobacteria and Firmicutes, including unique fish-associated strains of the Vibrionales and Clostridia (Spanggaard et al, 2000; Al-Harbi & Naim Uddin, 2004; Martin-Antonio et al, 2007; Sullam et al, 2012; Xing et al, 2013; Llewellyn et al, 2014) Significant variation in the fish gut microbiome has been reported with changes in taxonomic composition shown to affect host immunity, nutrient acquisition, and epithelial differentiation (Rawls, Samuel & Gordon, 2004; Bates et al, 2006; Bates et al, 2007; Cheesman & Guillemin, 2007; Cheesman et al, 2010; Kanther & Rawls, 2010; Ghanbari, Kneifel & Domig, 2015). Fish microbiome composition has been linked to diverse factors including host type (Ye et al, 2014; Givens et al, 2015; Hennersdorf et al, 2016), trophic ecology and diet (Bolnick et al, 2014a; Bolnick et al, 2014b; Miyake, Ngugi & Stingl, 2015; Sullam et al, 2015), and environmental conditions (e.g., salinity; Sullam et al, 2012; Schmidt et al, 2015)

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