Gut-Testis Axis: Microbiota Prime Metabolome To Increase Sperm Quality in Young Type 2 Diabetes

ABSTRACT Young type 2 diabetes (T2D) affects 15% of the population, with a noted increase in cases, and T2D-related male infertility has become a serious issue in recent years. The current study aimed to explore the improvements of alginate oligosaccharide (AOS)-modified gut microbiota on semen qual...

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Main Authors: Xiaowei Yan, Yanni Feng, Yanan Hao, Ruqing Zhong, Yue Jiang, Xiangfang Tang, Dongxin Lu, Hanhan Fang, Manjree Agarwal, Liang Chen, Yong Zhao, Hongfu Zhang
Format: Article
Language:English
Published: American Society for Microbiology 2022-10-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.01423-22
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author Xiaowei Yan
Yanni Feng
Yanan Hao
Ruqing Zhong
Yue Jiang
Xiangfang Tang
Dongxin Lu
Hanhan Fang
Manjree Agarwal
Liang Chen
Yong Zhao
Hongfu Zhang
author_facet Xiaowei Yan
Yanni Feng
Yanan Hao
Ruqing Zhong
Yue Jiang
Xiangfang Tang
Dongxin Lu
Hanhan Fang
Manjree Agarwal
Liang Chen
Yong Zhao
Hongfu Zhang
author_sort Xiaowei Yan
collection DOAJ
description ABSTRACT Young type 2 diabetes (T2D) affects 15% of the population, with a noted increase in cases, and T2D-related male infertility has become a serious issue in recent years. The current study aimed to explore the improvements of alginate oligosaccharide (AOS)-modified gut microbiota on semen quality in T2D. The T2D was established in young mice of 5 weeks of age with a blood glucose level of 21.2 ± 2.2 mmol/L, while blood glucose was 8.7 ± 1.1 mM in control animals. We discovered that fecal microbiota transplantation (FMT) of AOS-improved microbiota (A10-FMT) significantly decreased blood glucose, while FMT of gut microbiota from control animals (Con-FMT) did not. Sperm concentration and motility were decreased in T2D to 10% to 20% of those in the control group, while A10-FMT brought about a recovery of around 5- to 10-fold. A10-FMT significantly increased small intestinal Allobaculum, while it elevated small intestinal and cecal Lactobacillus in some extent, blood butyric acid and derivatives and eicosapentaenoic acid (EPA), and testicular docosahexaenoic acid (DHA), EPA, and testosterone and its derivatives. Furthermore, A10-FMT improved liver functions and systemic antioxidant environments. Most importantly, A10-FMT promoted spermatogenesis through the improvement in the expression of proteins important for spermatogenesis to increase sperm concentration and motility. The underlying mechanisms may be that A10-FMT increased gut-beneficial microbes Lactobacillus and Allobaculum to elevate blood and/or testicular butyric acid, DHA, EPA, and testosterone to promote spermatogenesis and thus to ameliorate sperm concentration and motility. AOS-improved gut microbes could emerge as attractive candidates to treat T2D-diminished semen quality. IMPORTANCE A10-FMT benefits gut microbiota, liver function, and systemic environment via improvement in blood metabolome, consequently to favor the testicular microenvironment to improve spermatogenesis process and to boost T2D-diminished semen quality. We established that AOS-improved gut microbiota may be used to boost T2D-decreased semen quality and metabolic disease-related male subfertility.
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spelling doaj.art-24281396fc2645de9841ebb08f8d53012022-12-22T03:53:38ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-10-0110510.1128/spectrum.01423-22Gut-Testis Axis: Microbiota Prime Metabolome To Increase Sperm Quality in Young Type 2 DiabetesXiaowei Yan0Yanni Feng1Yanan Hao2Ruqing Zhong3Yue Jiang4Xiangfang Tang5Dongxin Lu6Hanhan Fang7Manjree Agarwal8Liang Chen9Yong Zhao10Hongfu Zhang11State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of ChinaCollege of Veterinary Medicine, Qingdao Agricultural University, Qingdao, People’s Republic of ChinaState Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of ChinaState Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of ChinaState Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of ChinaState Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of ChinaState Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of ChinaState Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of ChinaCollege of Science, Health, Engineering and Education, Murdoch University, Perth, AustraliaState Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of ChinaState Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of ChinaState Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of ChinaABSTRACT Young type 2 diabetes (T2D) affects 15% of the population, with a noted increase in cases, and T2D-related male infertility has become a serious issue in recent years. The current study aimed to explore the improvements of alginate oligosaccharide (AOS)-modified gut microbiota on semen quality in T2D. The T2D was established in young mice of 5 weeks of age with a blood glucose level of 21.2 ± 2.2 mmol/L, while blood glucose was 8.7 ± 1.1 mM in control animals. We discovered that fecal microbiota transplantation (FMT) of AOS-improved microbiota (A10-FMT) significantly decreased blood glucose, while FMT of gut microbiota from control animals (Con-FMT) did not. Sperm concentration and motility were decreased in T2D to 10% to 20% of those in the control group, while A10-FMT brought about a recovery of around 5- to 10-fold. A10-FMT significantly increased small intestinal Allobaculum, while it elevated small intestinal and cecal Lactobacillus in some extent, blood butyric acid and derivatives and eicosapentaenoic acid (EPA), and testicular docosahexaenoic acid (DHA), EPA, and testosterone and its derivatives. Furthermore, A10-FMT improved liver functions and systemic antioxidant environments. Most importantly, A10-FMT promoted spermatogenesis through the improvement in the expression of proteins important for spermatogenesis to increase sperm concentration and motility. The underlying mechanisms may be that A10-FMT increased gut-beneficial microbes Lactobacillus and Allobaculum to elevate blood and/or testicular butyric acid, DHA, EPA, and testosterone to promote spermatogenesis and thus to ameliorate sperm concentration and motility. AOS-improved gut microbes could emerge as attractive candidates to treat T2D-diminished semen quality. IMPORTANCE A10-FMT benefits gut microbiota, liver function, and systemic environment via improvement in blood metabolome, consequently to favor the testicular microenvironment to improve spermatogenesis process and to boost T2D-diminished semen quality. We established that AOS-improved gut microbiota may be used to boost T2D-decreased semen quality and metabolic disease-related male subfertility.https://journals.asm.org/doi/10.1128/spectrum.01423-22type 2 diabetes in youthsperm concentrationsperm motilityspermatogenesisgut microbiotaDHA
spellingShingle Xiaowei Yan
Yanni Feng
Yanan Hao
Ruqing Zhong
Yue Jiang
Xiangfang Tang
Dongxin Lu
Hanhan Fang
Manjree Agarwal
Liang Chen
Yong Zhao
Hongfu Zhang
Gut-Testis Axis: Microbiota Prime Metabolome To Increase Sperm Quality in Young Type 2 Diabetes
Microbiology Spectrum
type 2 diabetes in youth
sperm concentration
sperm motility
spermatogenesis
gut microbiota
DHA
title Gut-Testis Axis: Microbiota Prime Metabolome To Increase Sperm Quality in Young Type 2 Diabetes
title_full Gut-Testis Axis: Microbiota Prime Metabolome To Increase Sperm Quality in Young Type 2 Diabetes
title_fullStr Gut-Testis Axis: Microbiota Prime Metabolome To Increase Sperm Quality in Young Type 2 Diabetes
title_full_unstemmed Gut-Testis Axis: Microbiota Prime Metabolome To Increase Sperm Quality in Young Type 2 Diabetes
title_short Gut-Testis Axis: Microbiota Prime Metabolome To Increase Sperm Quality in Young Type 2 Diabetes
title_sort gut testis axis microbiota prime metabolome to increase sperm quality in young type 2 diabetes
topic type 2 diabetes in youth
sperm concentration
sperm motility
spermatogenesis
gut microbiota
DHA
url https://journals.asm.org/doi/10.1128/spectrum.01423-22
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