Changes in seminal plasma microecological dynamics and the mechanistic impact of core metabolite hexadecanamide in asthenozoospermia patients

Author:

Han Baoquan12ORCID,Wang Yongyong3,Ge Wei4,Wang Junjie4,Yu Shuai2,Yan Jiamao4,Hua Lei1,Zhang Xiaoyuan4,Yan Zihui4,Wang Lu4,Zhao Jinxin4,Huang Cong5,Yang Bo2,Wang Yan6,Ma Qian2,Zhao Yong7,Jiang Hui2,Zhang Yunqi8,Liang Shaolin89,Zhao Jianjuan8,Sun Zhongyi1,Shen Wei4,Gui Yaoting2

Affiliation:

1. Department of Urology Shenzhen University General Hospital Shenzhen China

2. Shenzhen Key Laboratory of Male Reproductive Medicine and Genetics, Institute of Urology, Peking University Shenzhen Hospital Shenzhen‐Peking University‐The Hong Kong University of Science and Technology Medical Center Shenzhen China

3. Department of Reproductive Medicine, Qingdao Hospital University of Healthy and Rehabilitation Sciences (Qingdao Municipal Hospital) Qingdao China

4. College of Life Sciences Qingdao Agricultural University Qingdao China

5. Department of Dermatology, Skin Research Institute of Peking University Shenzhen Hospital, Peking University Shenzhen Hospital Shenzhen Peking University‐The Hong Kong University of Science and Technology Medical Center Shenzhen China

6. Department of Urology Peking University Shenzhen Hospital Shenzhen China

7. State Key Laboratory of Animal Nutrition, Institute of Animal Sciences Chinese Academy of Agricultural Sciences Beijing China

8. STI‐Zhilian Research Institute for Innovation and Digital Health Beijing China

9. Institute for Six‐sector Economy Fudan University Shanghai China

Abstract

AbstractAsthenozoospermia (AZS) is a prevalent contributor to male infertility, characterized by a substantial decline in sperm motility. In recent years, large‐scale studies have explored the interplay between the male reproductive system's microecology and its implications for reproductive health. Nevertheless, the direct association between seminal microecology and male infertility pathogenesis remains inconclusive. This study used 16S rDNA sequencing and multi‐omics analysis to conduct a comprehensive investigation of the seminal microbial community and metabolites in AZS patients. Patients were categorized into four distinct groups: Normal, mild AZS (AZS‐I), moderate AZS (AZS‐II), and severe AZS (AZS‐III). Microbiome differential abundance analysis revealed significant differences in microbial composition and metabolite profiles within the seminal plasma of these groups. Subsequently, patients were classified into a control group (Normal and AZS‐I) and an AZS group (AZS‐II and AZS‐III). Correlation and cross‐reference analyses identified distinct microbial genera and metabolites. Notably, the AZS group exhibited a reduced abundance of bacterial genera such as Pseudomonas, Serratia, and Methylobacterium‐Methylorubrum in seminal plasma, positively correlating with core differential metabolite (hexadecanamide). Conversely, the AZS group displayed an increased abundance of bacterial genera such as Uruburuella, Vibrio, and Pseudoalteromonas, with a negative correlation with core differential metabolite (hexadecanamide). In vitro and in vivo experiments validated that hexadecanamide significantly enhanced sperm motility. Using predictive metabolite‐targeting gene analysis and single‐cell transcriptome sequencing, we profiled the gene expression of candidate target genes PAOX and CA2. Protein immunoblotting techniques validated the upregulation protein levels of PAOX and CA2 in sperm samples after hexadecanamide treatment, enhancing sperm motility. In conclusion, this study uncovered a significant correlation between six microbial genera in seminal plasma and the content of the metabolite hexadecanamide, which is related to AZS. Hexadecanamide notably enhances sperm motility, suggesting its potential integration into clinical strategies for managing AZS, providing a foundational framework for diagnostic and therapeutic advancements.

Publisher

Wiley

Subject

Microbiology,Biotechnology

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