Investigating Both Mucosal Immunity and Microbiota in Response to Gut Enteritis in Yellowtail Kingfish

The mucosal surfaces of fish play numerous roles including, but not limited to, protection against pathogens, nutrient digestion and absorption, excretion of nitrogenous wastes and osmotic regulation. During infection or disease, these surfaces act as the first line of defense, where the mucosal imm...

Full description

Bibliographic Details
Main Authors: Thibault P. R. A. Legrand, James W. Wynne, Laura S. Weyrich, Andrew P. A. Oxley
Format: Article
Language:English
Published: MDPI AG 2020-08-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/8/9/1267
_version_ 1827708546282684416
author Thibault P. R. A. Legrand
James W. Wynne
Laura S. Weyrich
Andrew P. A. Oxley
author_facet Thibault P. R. A. Legrand
James W. Wynne
Laura S. Weyrich
Andrew P. A. Oxley
author_sort Thibault P. R. A. Legrand
collection DOAJ
description The mucosal surfaces of fish play numerous roles including, but not limited to, protection against pathogens, nutrient digestion and absorption, excretion of nitrogenous wastes and osmotic regulation. During infection or disease, these surfaces act as the first line of defense, where the mucosal immune system interacts closely with the associated microbiota to maintain homeostasis. This study evaluated microbial changes across the gut and skin mucosal surfaces in yellowtail kingfish displaying signs of gut inflammation, as well as explored the host gene expression in these tissues in order to improve our understanding of the underlying mechanisms that contribute to the emergence of these conditions. For this, we obtained and analyzed 16S rDNA and transcriptomic (RNA-Seq) sequence data from the gut and skin mucosa of fish exhibiting different health states (i.e., healthy fish and fish at the early and late stages of enteritis). Both the gut and skin microbiota were perturbed by the disease. More specifically, the gastrointestinal microbiota of diseased fish was dominated by an uncultured <i>Mycoplasmataceae</i> sp., and fish at the early stage of the disease showed a significant loss of diversity in the skin. Using transcriptomics, we found that only a few genes were significantly differentially expressed in the gut. In contrast, gene expression in the skin differed widely between health states, in particular in the fish at the late stage of the disease. These changes were associated with several metabolic pathways that were differentially expressed and reflected a weakened host. Altogether, this study highlights the sensitivity of the skin mucosal surface in response to gut inflammation.
first_indexed 2024-03-10T17:06:07Z
format Article
id doaj.art-a565d4fd50344c5fa54067972484478c
institution Directory Open Access Journal
issn 2076-2607
language English
last_indexed 2024-03-10T17:06:07Z
publishDate 2020-08-01
publisher MDPI AG
record_format Article
series Microorganisms
spelling doaj.art-a565d4fd50344c5fa54067972484478c2023-11-20T10:48:08ZengMDPI AGMicroorganisms2076-26072020-08-0189126710.3390/microorganisms8091267Investigating Both Mucosal Immunity and Microbiota in Response to Gut Enteritis in Yellowtail KingfishThibault P. R. A. Legrand0James W. Wynne1Laura S. Weyrich2Andrew P. A. Oxley3Department of Ecology and Evolution, School of Biological Sciences, The University of Adelaide, Adelaide, SA 5005, AustraliaCSIRO, Agriculture and Food, Hobart, TAS 7004, AustraliaDepartment of Ecology and Evolution, School of Biological Sciences, The University of Adelaide, Adelaide, SA 5005, AustraliaSchool of Life and Environmental Sciences, Faculty of Sciences Engineering and Built Environment, Deakin University, Waurn Ponds, VIC 3216, AustraliaThe mucosal surfaces of fish play numerous roles including, but not limited to, protection against pathogens, nutrient digestion and absorption, excretion of nitrogenous wastes and osmotic regulation. During infection or disease, these surfaces act as the first line of defense, where the mucosal immune system interacts closely with the associated microbiota to maintain homeostasis. This study evaluated microbial changes across the gut and skin mucosal surfaces in yellowtail kingfish displaying signs of gut inflammation, as well as explored the host gene expression in these tissues in order to improve our understanding of the underlying mechanisms that contribute to the emergence of these conditions. For this, we obtained and analyzed 16S rDNA and transcriptomic (RNA-Seq) sequence data from the gut and skin mucosa of fish exhibiting different health states (i.e., healthy fish and fish at the early and late stages of enteritis). Both the gut and skin microbiota were perturbed by the disease. More specifically, the gastrointestinal microbiota of diseased fish was dominated by an uncultured <i>Mycoplasmataceae</i> sp., and fish at the early stage of the disease showed a significant loss of diversity in the skin. Using transcriptomics, we found that only a few genes were significantly differentially expressed in the gut. In contrast, gene expression in the skin differed widely between health states, in particular in the fish at the late stage of the disease. These changes were associated with several metabolic pathways that were differentially expressed and reflected a weakened host. Altogether, this study highlights the sensitivity of the skin mucosal surface in response to gut inflammation.https://www.mdpi.com/2076-2607/8/9/1267microbiotaimmunityfishgutskinhealth
spellingShingle Thibault P. R. A. Legrand
James W. Wynne
Laura S. Weyrich
Andrew P. A. Oxley
Investigating Both Mucosal Immunity and Microbiota in Response to Gut Enteritis in Yellowtail Kingfish
Microorganisms
microbiota
immunity
fish
gut
skin
health
title Investigating Both Mucosal Immunity and Microbiota in Response to Gut Enteritis in Yellowtail Kingfish
title_full Investigating Both Mucosal Immunity and Microbiota in Response to Gut Enteritis in Yellowtail Kingfish
title_fullStr Investigating Both Mucosal Immunity and Microbiota in Response to Gut Enteritis in Yellowtail Kingfish
title_full_unstemmed Investigating Both Mucosal Immunity and Microbiota in Response to Gut Enteritis in Yellowtail Kingfish
title_short Investigating Both Mucosal Immunity and Microbiota in Response to Gut Enteritis in Yellowtail Kingfish
title_sort investigating both mucosal immunity and microbiota in response to gut enteritis in yellowtail kingfish
topic microbiota
immunity
fish
gut
skin
health
url https://www.mdpi.com/2076-2607/8/9/1267
work_keys_str_mv AT thibaultpralegrand investigatingbothmucosalimmunityandmicrobiotainresponsetogutenteritisinyellowtailkingfish
AT jameswwynne investigatingbothmucosalimmunityandmicrobiotainresponsetogutenteritisinyellowtailkingfish
AT laurasweyrich investigatingbothmucosalimmunityandmicrobiotainresponsetogutenteritisinyellowtailkingfish
AT andrewpaoxley investigatingbothmucosalimmunityandmicrobiotainresponsetogutenteritisinyellowtailkingfish