Intestinal melatonin levels and gut microbiota homeostasis are independent of the pineal gland in pigs

IntroductionMelatonin (MEL) is a crucial neuroendocrine hormone primarily produced by the pineal gland. Pinealectomy (PINX) has been performed on an endogenous MEL deficiency model to investigate the functions of pineal MEL and its relationship with various diseases. However, the effect of PINX on t...

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Main Authors: Jiaming Zheng, Yewen Zhou, Di Zhang, Kezhe Ma, Yuneng Gong, Xuan Luo, Jiali Liu, Sheng Cui
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-03-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1352586/full
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author Jiaming Zheng
Jiaming Zheng
Yewen Zhou
Yewen Zhou
Di Zhang
Di Zhang
Kezhe Ma
Kezhe Ma
Yuneng Gong
Yuneng Gong
Xuan Luo
Jiali Liu
Sheng Cui
Sheng Cui
Sheng Cui
author_facet Jiaming Zheng
Jiaming Zheng
Yewen Zhou
Yewen Zhou
Di Zhang
Di Zhang
Kezhe Ma
Kezhe Ma
Yuneng Gong
Yuneng Gong
Xuan Luo
Jiali Liu
Sheng Cui
Sheng Cui
Sheng Cui
author_sort Jiaming Zheng
collection DOAJ
description IntroductionMelatonin (MEL) is a crucial neuroendocrine hormone primarily produced by the pineal gland. Pinealectomy (PINX) has been performed on an endogenous MEL deficiency model to investigate the functions of pineal MEL and its relationship with various diseases. However, the effect of PINX on the gastrointestinal tract (GIT) MEL levels and gut microbiome in pigs has not been previously reported.MethodsBy using a newly established pig PINX model, we detected the levels of MEL in the GIT by liquid chromatography–tandem mass spectrometry. In addition, we examined the effects of PINX on the expression of MEL synthesis enzymes, intestinal histomorphology, and the intestinal barrier. Furthermore, 16S rRNA sequencing was performed to analyze the colonic microbiome.ResultsPINX reduced serum MEL levels but did not affect GIT MEL levels. Conversely, MEL supplementation increased MEL levels in the GIT and intestinal contents. Neither PINX nor MEL supplementation had any effect on weight gain, organ coefficient, serum biochemical indexes, or MEL synthetase arylalkylamine N-acetyltransferase (AANAT) expression in the duodenum, ileum, and colon. Furthermore, no significant differences were observed in the intestinal morphology or intestinal mucosal barrier function due to the treatments. Additionally, 16S rRNA sequencing revealed that PINX had no significant impact on the composition of the intestinal microbiota. Nevertheless, MEL supplementation decreased the abundance of Fibrobacterota and increased the abundance of Actinobacteriota, Desulfobacterota, and Chloroflexi.ConclusionWe demonstrated that synthesis of MEL in the GIT is independent of the pineal gland. PINX had no influence on intestinal MEL level and microbiota composition in pigs, while exogenous MEL alters the structure of the gut microbiota.
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spelling doaj.art-0b377baa17d242548ebaef940017551f2024-03-26T15:28:54ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-03-011510.3389/fmicb.2024.13525861352586Intestinal melatonin levels and gut microbiota homeostasis are independent of the pineal gland in pigsJiaming Zheng0Jiaming Zheng1Yewen Zhou2Yewen Zhou3Di Zhang4Di Zhang5Kezhe Ma6Kezhe Ma7Yuneng Gong8Yuneng Gong9Xuan Luo10Jiali Liu11Sheng Cui12Sheng Cui13Sheng Cui14College of Veterinary Medicine, Yangzhou University, Yangzhou, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, ChinaState Key Laboratory of Animal Biotech Breeding, College of Biological Sciences, China Agricultural University, Beijing, ChinaState Key Laboratory of Animal Biotech Breeding, College of Biological Sciences, China Agricultural University, Beijing, ChinaCollege of Veterinary Medicine, Yangzhou University, Yangzhou, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, ChinaInstitute of Reproduction and Metabolism, Yangzhou University, Yangzhou, ChinaIntroductionMelatonin (MEL) is a crucial neuroendocrine hormone primarily produced by the pineal gland. Pinealectomy (PINX) has been performed on an endogenous MEL deficiency model to investigate the functions of pineal MEL and its relationship with various diseases. However, the effect of PINX on the gastrointestinal tract (GIT) MEL levels and gut microbiome in pigs has not been previously reported.MethodsBy using a newly established pig PINX model, we detected the levels of MEL in the GIT by liquid chromatography–tandem mass spectrometry. In addition, we examined the effects of PINX on the expression of MEL synthesis enzymes, intestinal histomorphology, and the intestinal barrier. Furthermore, 16S rRNA sequencing was performed to analyze the colonic microbiome.ResultsPINX reduced serum MEL levels but did not affect GIT MEL levels. Conversely, MEL supplementation increased MEL levels in the GIT and intestinal contents. Neither PINX nor MEL supplementation had any effect on weight gain, organ coefficient, serum biochemical indexes, or MEL synthetase arylalkylamine N-acetyltransferase (AANAT) expression in the duodenum, ileum, and colon. Furthermore, no significant differences were observed in the intestinal morphology or intestinal mucosal barrier function due to the treatments. Additionally, 16S rRNA sequencing revealed that PINX had no significant impact on the composition of the intestinal microbiota. Nevertheless, MEL supplementation decreased the abundance of Fibrobacterota and increased the abundance of Actinobacteriota, Desulfobacterota, and Chloroflexi.ConclusionWe demonstrated that synthesis of MEL in the GIT is independent of the pineal gland. PINX had no influence on intestinal MEL level and microbiota composition in pigs, while exogenous MEL alters the structure of the gut microbiota.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1352586/fullpigpinealectomymelatoninintestinegut microbiota
spellingShingle Jiaming Zheng
Jiaming Zheng
Yewen Zhou
Yewen Zhou
Di Zhang
Di Zhang
Kezhe Ma
Kezhe Ma
Yuneng Gong
Yuneng Gong
Xuan Luo
Jiali Liu
Sheng Cui
Sheng Cui
Sheng Cui
Intestinal melatonin levels and gut microbiota homeostasis are independent of the pineal gland in pigs
Frontiers in Microbiology
pig
pinealectomy
melatonin
intestine
gut microbiota
title Intestinal melatonin levels and gut microbiota homeostasis are independent of the pineal gland in pigs
title_full Intestinal melatonin levels and gut microbiota homeostasis are independent of the pineal gland in pigs
title_fullStr Intestinal melatonin levels and gut microbiota homeostasis are independent of the pineal gland in pigs
title_full_unstemmed Intestinal melatonin levels and gut microbiota homeostasis are independent of the pineal gland in pigs
title_short Intestinal melatonin levels and gut microbiota homeostasis are independent of the pineal gland in pigs
title_sort intestinal melatonin levels and gut microbiota homeostasis are independent of the pineal gland in pigs
topic pig
pinealectomy
melatonin
intestine
gut microbiota
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1352586/full
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