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Single-cell analysis of testicular bacterial microbiome changes during aging and effect on reproductive capacity in mice

ABSTRACT: The testis supports spermatogenesis through a tightly regulated microenvironment, and the bacterial microbiome (BM) may influence host cells through immune and metabolic pathways, thereby impacting reproductive capacity. Here, we applied invasion-adhesion-directed expression sequencing (INVADE-seq), a single-cell RNA sequencing approach that simultaneously captures host and bacterial transcripts, to examine how bacterial signals shape testicular cell states. We detected a sparse but widespread bacterial presence across multiple cell types, with somatic and early germ cells outside the blood-testis barrier (BTB) showing relatively higher bacterial abundance. Bacterial load increased with age, coinciding with transcriptional signatures of reduced BTB function. At the cellular level, bacterial-positive Leydig cells exhibited activation of steroidogenic genes, whereas macrophages upregulated pathways related to autophagy and immune modulation. These findings not only deepen our understanding of testicular microbiome biology but also hold promise for the discovery of novel diagnostic biomarkers and therapeutic targets for BM-related and age-associated male subfertility.

ORGANISM(S): Mus musculus

PROVIDER: GSE303193 | GEO | 2025/07/25

REPOSITORIES: GEO

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Project description:The specific role of polyamines in the testis physiology is not fully understood. Antizymes (OAZs) and antizyme inhibitors (AZINs) are modulators of ornithine decarboxylase (ODC), a key enzyme in polyamine biosynthesis and polyamine uptake. Although the three known OAZs are expressed in the testis, only OAZ3 is testis specific and has been proven to have an essential role in male fertility. Regarding the two existing AZINs, AZIN2 is the most abundantly expressed member in this gonad. Whereas previous studies suggested that AZIN2 might participate in mouse spermatogenesis, immunohistological analysis of human testicular sections revealed that AZIN2 is also detected in the steroidogenic Leydig cells but not in the germinal epithelium. In the present study, we found a close ontogenic similarity in the mRNA levels of OAZs and AZINs between mice and rats, but an opposite expression pattern of ODC activity. Further analysis of AZIN2 and OAZ3 in the testis of mice with different alterations in spermatogenesis and fertility, induced either genetically or pharmacologically, corroborated that both AZIN2 and OAZ3 are mainly expressed in the haploid germinal cells. Finally, by using transgenic mice with a truncated Azin2 gene fused to the bacterial lacZ gene, we studied the expression of Azin2 in testes, epididymides and spermatozoa. AZIN2 was detected in spermatids and spermatozoa, as well as in Leydig cells, and in epithelial epidydimal cells. Azin2 knock-out male mice were fertile; however, they showed marked decreases in testicular putrescine and plasma and testicular testosterone levels, and a dramatic reduction in the sperm motility. These results suggest an important role for AZIN2 in testicular cells by modulating polyamine concentrations, testosterone synthesis and sperm function. Overall, our data corroborate the relevance of polyamine regulation in spermatogenesis, where both AZIN2 and OAZ3 play fundamental roles. We used microarrays in order to detect how the disruption of Azin2 could affect overall gene expression in testis.

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Single-cell analysis of testicular bacterial microbiome changes during aging and effect on reproductive capacity in mice

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