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

ABSTRACT: Recent studies have highlighted connections between bacterial microbiome (BM) of the gut and seminal fluid and male reproductive health. However, knowledge regarding the BM within the testis—the site of spermatogenesis—remains notably limited. Here, we employed INVADEseq, an improved single-cell RNA sequencing technology, to explore the testicular BM in terms of its composition, distribution, age-related changes, host-microbiome interactions and impact on reproductive capacity. Our analyses unveiled a widespread yet sparse distribution of BM across diverse testicular cell types. Notably, we identified significant spatial heterogeneity in BM load, with somatic cells and early-stage germ cells located outside the blood-testis barrier (BTB) exhibiting relatively higher BM abundance. Additionally, we observed an age-dependent increase in BM load, potentially attributable to compromised BTB integrity in aged testes. Functionally, the presence of BM induced distinct transcriptional responses across testicular cell types. Specifically, it enhanced testosterone production in Leydig cells, promoted endocytosis and autophagy functions in M2 macrophages, and reshaped the ligand-receptor interaction network. Collectively, our study presents the first single-cell resolution atlas of host-microbiome interactions in the testis. 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:Akt1 plays a protective role in the postnatal C57BL6 mouse testis following lactational exposure to the neonatal goitrogen, propylthiouracil (PTU). To elucidate the transcriptional profile mediating this phenotypic effect, we monitored changes in testicular gene expression at postnatal days (PNDs) 15 and 25 in Akt1+/+, Akt1+/-, and Akt1-/- testes following exposure to 0.01% PTU allowing us to determine changes in gene expression due to 1.) genotype effects; 2.) exposure effects; and 3.) genotype-by-exposure interactions. Early PTU-dependent gene changes included genes involved in lipid metabolism, spermatid differentiation, meiosis and adhesion. Early Akt1-dependent effects were associated with germ cell development, spermatid development and differentiation, and sperm motility. By PND25, the Akt1 gene-environment interaction had pronounced effects on genes associated with Sertoli cell (SC) differentiation and claudin-associated junctional formation suggesting delayed formation of the blood-testis barrier (BTB). To confirm these observations, biotin tracer experiments demonstrated a permeable blood-testis barrier in PTU-exposed PKB/Akt1-/- tubules as late as PND25 compared to PTU-exposed Akt1+/+ seminiferous tubules. Transmission electron microscopy demonstrated altered SC morphology, aberrant SC localization, and disorganized actin bundle formation. Taken together, loss of Akt1 coupled with postnatal exposure to the neonatal goitrogen, PTU, in the testis contributes to a transcriptional profile associated with impaired integrity of the blood-testis barrier. In summary, the Akt1-/- mouse represents a potentially important model to study BTB formation and reassembly in response to male reproductive toxicants and the various signaling networks which mediate these responses. The microarray analysis employed a balanced factorial design, with one chip created for each of three mice under each experimental condition: mouse genotype (Akt1+/+, Akt1+/-, and Akt1-/-), exposure (PTU and Control), and age (sacrificed at PND15 and 25), with a total of 36 mice and 36 chips. MoGene 1.0 st v1 arrays were used for the samples from PND 15 and Mouse Genome 430 2.0 arrays were used for the samples from PND 25. One chip, PTU-exposed, Akt1-/-, PND25, was determined to not be of high quality and was not included in the analysis or provided here.

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

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