Testicular microbiome in azoospermic men-first evidence of the impact of an altered microenvironment

Hum Reprod. 2018 Jul 1;33(7):1212-1217. doi: 10.1093/humrep/dey116.

Abstract

Study question: Given the relevant role of the extracellular microenvironment in regulating tissue homeostasis, is testicular bacterial microbiome (BM) associated with germ cell aplasia in idiopathic non-obstructive azoospermia (iNOA)?

Summary answer: A steady increase of dysbiosis was observed among testis with normal spermatogenesis vs. iNOA with positive sperm retrieval and iNOA with complete germ cell aplasia.

What is known already: Tissue-associated BM has been reported to be a biologically important extracellular microenvironment component for numerous body habitats, but not yet for the human testis.

Study design, size, duration: Cross-sectional study, investigating tissue-associated BM in the testis of (i) five men with iNOA and negative sperm retrieval at microdissection testicular sperm extraction (microTESE); (ii) five men with iNOA and positive sperm retrieval at microTESE; and (iii) five normozoospermic men upon orchiectomy. Every testicular specimen was histologically classified and analyzed in terms of bacterial community.

Participants/materials, setting, methods: Massive ultra-deep pyrosequencing was applied to investigate testis microbiome. Metagenome was analyzed using Quantitative Insights Into Microbial Ecology (QIIME). Tissue-associated bacterial load was quantified by digital droplet PCR.

Main results and the role of chance: Normozoospermic men showed small amounts of bacteria in the testis, with Actinobacteria, Bacteroidetes, Firmicutes Proteobacteria as the dominating phyla; iNOA individuals had increased amounts of bacterial DNA (P = 0.02), associated with decreased taxa richness due to the lack of Bacteroidetes and Proteobacteria (P = 2 × 10-5). Specimens with negative sperm retrieval at microTESE depicted complete germ cell aplasia and a further decrease in terms of Firmicutes and Clostridia (P < 0.05), a complete lack of Peptoniphilus asaccharolyticus, but increased amount of Actinobacteria.

Limitations, reasons for caution: The limited number of specimens analyzed in this preliminary study deserves external validation. The paraneoplastic microenvironment could have an impact on the residential bacterial flora.

Wider implication of the findings: Human testicular microenvironment is not microbiologically sterile, containing low amounts of Actinobacteria, Bacteroidetes, Firmicutes and Proteobacteria. A dysbiotic bacterial community was associated with iNOA and complete germ cell aplasia. Novel findings on testicular BM could support future translational therapies of male-factor infertility.

Study funding/competing interest(s): This work was supported by URI-Urological Research Institute free funds. Authors declared no conflict of interest.

Trial registration number: N/A.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Azoospermia / complications*
  • Azoospermia / microbiology
  • Azoospermia / pathology
  • Cross-Sectional Studies
  • Dysbiosis / complications*
  • Dysbiosis / microbiology
  • Dysbiosis / pathology
  • Humans
  • Male
  • Microbiota*
  • Spermatogenesis / physiology
  • Testis / microbiology*
  • Testis / pathology

Supplementary concepts

  • Azoospermia, Nonobstructive