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Spatial variation in the gastrointestinal microbiome, diet, and nutritional condition of a juvenile flatfish among coastal habitats

Spatial variation in the gastrointestinal microbiome, diet, and nutritional condition of a juvenile flatfish among coastal habitats
Spatial variation in the gastrointestinal microbiome, diet, and nutritional condition of a juvenile flatfish among coastal habitats

Gut microbiota are important for the health, fitness and development of animal hosts, but little is known about these assemblages in wild populations of fish. Such knowledge is particularly important for juvenile life stages where nutritional intake critically determines early development, growth, and ultimately recruitment. We characterise the microbiome inhabiting the gut of young-of-the-year European plaice (‘YOY plaice’) on sandy beaches, their key juvenile habitat, and examine how these microbial communities vary spatially in relation to diet and nutritional condition of their plaice hosts. Body size, diet (stomach fullness and eukaryotic 18S ribosomal sequencing), nutritional condition (RNA:DNA) and gut microbiota (16S prokaryotic ribosomal sequencing) were compared in fish at two spatial scales: between beaches separated by 10s of kilometres and between sites at different depths on the same beach, separated by 10s of metres. The main microbial phyla in YOY plaice guts were Proteobacteria, Spirochaetes, Tenericutes and Verrucomicrobiae. Within the Proteobacteria there was an unusual dominance of Alphaproteobacteria. Differences in body size, diet and nutritional condition of YOY plaice between beaches were accompanied by differences in gut microbial assemblage structure. Notably, substantially reduced nutritional condition and size at one of the beaches was associated with lower stomach fullness, reduced consumption of annelids and differences in the abundance and presence of specific microbial taxa. Differences were also detected in microbial assemblages, body size, and diet between depths within the same nursery beach, although stomach fullness and nutritional condition did not vary significantly. The functional links between the environment, gut microbiota, and their hosts are potentially important mediators of the development of young fish through critical life stages. Our study indicates that these links need to be addressed at 10 km and even 10 m scales to capture the variability observed in wild populations of juvenile fish.

Essential fish habitat, Gastrointestinal microbiota, Gut microbiome, Juvenile fish, Nursery habitats, Pleuronectes platessa, Sandy beach
0141-1136
105413
Morris, Marc T.
4f80ea70-1c41-42b7-b817-905c8fed8aa6
Hauton, Chris
7706f6ba-4497-42b2-8c6d-00df81676331
Baylay, Alison J.
08ea69f8-9910-4c8b-86a9-602e45b8a44e
Peruzza, Luca
c01f028c-1fb4-44a4-83b9-f24698a9c9e5
Targett, Timothy E.
97f9fce4-ce29-4156-b466-0df128381a55
Ciotti, Benjamin J.
034551e4-d770-4cd2-80cc-b95c677938d2
Morris, Marc T.
4f80ea70-1c41-42b7-b817-905c8fed8aa6
Hauton, Chris
7706f6ba-4497-42b2-8c6d-00df81676331
Baylay, Alison J.
08ea69f8-9910-4c8b-86a9-602e45b8a44e
Peruzza, Luca
c01f028c-1fb4-44a4-83b9-f24698a9c9e5
Targett, Timothy E.
97f9fce4-ce29-4156-b466-0df128381a55
Ciotti, Benjamin J.
034551e4-d770-4cd2-80cc-b95c677938d2

Morris, Marc T., Hauton, Chris, Baylay, Alison J., Peruzza, Luca, Targett, Timothy E. and Ciotti, Benjamin J. (2021) Spatial variation in the gastrointestinal microbiome, diet, and nutritional condition of a juvenile flatfish among coastal habitats. Marine Environmental Research, 170, 105413, [105413]. (doi:10.1016/j.marenvres.2021.105413).

Record type: Article

Abstract

Gut microbiota are important for the health, fitness and development of animal hosts, but little is known about these assemblages in wild populations of fish. Such knowledge is particularly important for juvenile life stages where nutritional intake critically determines early development, growth, and ultimately recruitment. We characterise the microbiome inhabiting the gut of young-of-the-year European plaice (‘YOY plaice’) on sandy beaches, their key juvenile habitat, and examine how these microbial communities vary spatially in relation to diet and nutritional condition of their plaice hosts. Body size, diet (stomach fullness and eukaryotic 18S ribosomal sequencing), nutritional condition (RNA:DNA) and gut microbiota (16S prokaryotic ribosomal sequencing) were compared in fish at two spatial scales: between beaches separated by 10s of kilometres and between sites at different depths on the same beach, separated by 10s of metres. The main microbial phyla in YOY plaice guts were Proteobacteria, Spirochaetes, Tenericutes and Verrucomicrobiae. Within the Proteobacteria there was an unusual dominance of Alphaproteobacteria. Differences in body size, diet and nutritional condition of YOY plaice between beaches were accompanied by differences in gut microbial assemblage structure. Notably, substantially reduced nutritional condition and size at one of the beaches was associated with lower stomach fullness, reduced consumption of annelids and differences in the abundance and presence of specific microbial taxa. Differences were also detected in microbial assemblages, body size, and diet between depths within the same nursery beach, although stomach fullness and nutritional condition did not vary significantly. The functional links between the environment, gut microbiota, and their hosts are potentially important mediators of the development of young fish through critical life stages. Our study indicates that these links need to be addressed at 10 km and even 10 m scales to capture the variability observed in wild populations of juvenile fish.

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Spatial variation in the gastrointestinal microbiome, diet, and nutritional condition ...
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Accepted/In Press date: 9 July 2021
e-pub ahead of print date: 14 July 2021
Published date: 1 August 2021
Additional Information: Funding Information: The authors thank Michael Burrows from the Scottish Association for Marine Science for assistance with field collections and two anonymous reviewers for constructive comments on an earlier draft of the manuscript. Funding was provided by a Teaching and Learning award from the University of Plymouth and UK BBSRC grant BB/N005058/1. Funding Information: The authors thank Michael Burrows from the Scottish Association for Marine Science for assistance with field collections and two anonymous reviewers for constructive comments on an earlier draft of the manuscript. Funding was provided by a Teaching and Learning award from the University of Plymouth and UK BBSRC grant BB/N005058/1 . Publisher Copyright: © 2021 Elsevier Ltd Copyright: Copyright 2021 Elsevier B.V., All rights reserved.
Keywords: Essential fish habitat, Gastrointestinal microbiota, Gut microbiome, Juvenile fish, Nursery habitats, Pleuronectes platessa, Sandy beach

Identifiers

Local EPrints ID: 453458
URI: http://eprints.soton.ac.uk/id/eprint/453458
ISSN: 0141-1136
PURE UUID: 868adb6b-5fab-422f-8433-9ba32e63938e
ORCID for Chris Hauton: ORCID iD orcid.org/0000-0002-2313-4226
ORCID for Alison J. Baylay: ORCID iD orcid.org/0000-0002-0814-0740

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Date deposited: 18 Jan 2022 17:32
Last modified: 28 Apr 2022 02:12

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Contributors

Author: Marc T. Morris
Author: Chris Hauton ORCID iD
Author: Luca Peruzza
Author: Timothy E. Targett
Author: Benjamin J. Ciotti

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