Epithelial, metabolic and innate immunity transcriptomic signatures differentiating the rumen from other sheep and mammalian gastrointestinal tract tissues

Author:

Xiang Ruidong1,Oddy Victor Hutton2,Archibald Alan L.3,Vercoe Phillip E.4,Dalrymple Brian P.1

Affiliation:

1. CSIRO Agriculture, St. Lucia, QLD, Australia

2. NSW Department of Primary Industries, Beef Industry Centre, University of New England, Armidale, NSW, Australia

3. The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush, UK

4. School of Animal Biology and Institute of Agriculture, The University of Western Australia, Perth, Western Australia, Australia

Abstract

Background.Ruminants are successful herbivorous mammals, in part due to their specialized forestomachs, the rumen complex, which facilitates the conversion of feed to soluble nutrients by micro-organisms. Is the rumen complex a modified stomach expressing new epithelial (cornification) and metabolic programs, or a specialised stratified epithelium that has acquired new metabolic activities, potentially similar to those of the colon? How has the presence of the rumen affected other sections of the gastrointestinal tract (GIT) of ruminants compared to non-ruminants?Methods.Transcriptome data from 11 tissues covering the sheep GIT, two stratified epithelial and two control tissues, was analysed using principal components to cluster tissues based on gene expression profile similarity. Expression profiles of genes along the sheep GIT were used to generate a network to identify genes enriched for expression in different compartments of the GIT. The data from sheep was compared to similar data sets from two non-ruminants, pigs (closely related) and humans (more distantly related).Results.The rumen transcriptome clustered with the skin and tonsil, but not the GIT transcriptomes, driven by genes from the epidermal differentiation complex, and genes encoding stratified epithelium keratins and innate immunity proteins. By analysing all of the gene expression profiles across tissues together 16 major clusters were identified. The strongest of these, and consistent with the high turnover rate of the GIT, showed a marked enrichment of cell cycle process genes (P= 1.4 E−46), across the whole GIT, relative to liver and muscle, with highest expression in the caecum followed by colon and rumen. The expression patterns of several membrane transporters (chloride, zinc, nucleosides, amino acids, fatty acids, cholesterol and bile acids) along the GIT was very similar in sheep, pig and humans. In contrast, short chain fatty acid uptake and metabolism appeared to be different between the species and different between the rumen and colon in sheep. The importance of nitrogen and iodine recycling in sheep was highlighted by the highly preferential expression ofSLC14A1-urea (rumen), RHBG-ammonia (intestines) andSLC5A5-iodine (abomasum). The gene encoding a poorly characterized member of the maltase-glucoamylase family (MGAM2), predicted to play a role in the degradation of starch or glycogen, was highly expressed in the small and large intestines.Discussion.The rumen appears to be a specialised stratified cornified epithelium, probably derived from the oesophagus, which has gained some liver-like and other specialized metabolic functions, but probably not by expression of pre-existing colon metabolic programs. Changes in gene transcription downstream of the rumen also appear have occurred as a consequence of the evolution of the rumen and its effect on nutrient composition flowing down the GIT.

Funder

Department of Agriculture, Filling the Research Gap “International Coordination of the Rumen Pangenome project”

BBSRC Institute Strategic Programme Grants

BBSRC

NERC

MRC

Publisher

PeerJ

Subject

General Agricultural and Biological Sciences,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

Reference101 articles.

1. Ammonia and urea transport across the rumen epithelium: a review;Abdoun;Animal Health Research Reviews,2006

2. Modulation of urea transport across sheep rumen epithelium in vitro by SCFA and CO2;Abdoun;American Journal of Physiology—Gastrointestinal and Liver Physiology,2010

3. Role of the gut in lipid homeostasis;Abumrad;Physiological Reviews,2012

4. HTSeq–a Python framework to work with high-throughput sequencing data;Anders;Bioinformatics,2015

5. Special Functions

同舟云学术

1.学者识别学者识别

2.学术分析学术分析

3.人才评估人才评估

"同舟云学术"是以全球学者为主线,采集、加工和组织学术论文而形成的新型学术文献查询和分析系统,可以对全球学者进行文献检索和人才价值评估。用户可以通过关注某些学科领域的顶尖人物而持续追踪该领域的学科进展和研究前沿。经过近期的数据扩容,当前同舟云学术共收录了国内外主流学术期刊6万余种,收集的期刊论文及会议论文总量共计约1.5亿篇,并以每天添加12000余篇中外论文的速度递增。我们也可以为用户提供个性化、定制化的学者数据。欢迎来电咨询!咨询电话:010-8811{复制后删除}0370

www.globalauthorid.com

TOP

Copyright © 2019-2024 北京同舟云网络信息技术有限公司
京公网安备11010802033243号  京ICP备18003416号-3