The microbiome of the penis, semen and male reproductive tract

We are just starting to appreciate the influences of microbiota on the various areas of the human body, particularly the gut microbiome^​1,2​.

The gut microbiome impacts the immune system and neurobehaviour^​1​, for instance. The vaginal and penile microbiomes are now being studied in much more detail, providing clues as to the underlying health of the genital and reproductive tracts^​3–5​.

For once, most studies have focused on the vaginal microbiome and the impacts on fertility, pregnancy and infection. A protective vaginal microbiome consists of larger numbers of Lactobacillus species. The upper genital tract (uterus, fallopian tubes, ovaries) are also proving rich grounds for microbiome research^​3​.

Bacteria in sperm

The male genital tract microbiome has only been more recently studied, in a limited capacity, which is less that men have been ignored, rather an assumption that men don’t have microbiome problems and therefore it was not worth studying. The opposite is becoming apparently true.

There is evidence that many bacteria are shared in the vagina and penis of sexual partners^​6​, including those that cause bacterial vaginosis (BV). The male microbiome impacts fertility and the health of the male reproductive tract.^​7–12​

Bacteria in the male genital tract has traditionally been associated with infection, with the most common conditions being orchitis, epididymitis, prostatitis and urethritis.

The majority of epididymo-orchitis symptoms are caused by sexually transmitted infections (STIs) such as chlamydia and gonorrhoea^​13,14​, while acute and chronic prostatitis are usually caused by Escherichia coli, Klebsiella, Proteus, Pseudomonas aeruginosa, Enterococcus and Staphylococcus aureus^​14,15​.

Bacteria in sperm (bacteriospermia) has been linked with male genital tract infections, but initially only because the reproductive tracts were supposedly sterile (now known to absolutely not be true).

The bacteria most commonly isolated from human sperm are members of the Staphylococcus, Enterococcus, Escherichia and Ureaplasma families^​16​. New DNA testing methods show we’re covered in bacteria from top to toe, and the male genital tract is no exception^​17​.

Collection of male samples

Collecting microbiome samples from the inner male reproductive tract is invasive and difficult to perform. So far the most common sample types have been take from prostate cancer or infertility cases, skewing the sample group from what might be considered normal or healthy.

Microbiome of testes, epididymis and vas deferens

Research has demonstrated that the testes (with no signs of infection or inflammation) contain low abundant bacteria.

Alfano et al did a comparison between the bacteria of two different groups of men, with Firmicutes and Actinobacteria were the two groups in greatest abundance, with men with azoospermia (no sperm in ejaculate) showing a significant increased abundance of Actinobacteria and decreased Proteobacteria and Bacteriodetes.

Another study questioned the existence of a testicular microbiome, suggesting contamination^​18​. However, testicular microbiota found include Blautia, Cellulosibacter, Clostridium XIVa, Clostridium XIVb, Clostridium XVIII, Collinsella, Prevotella, Prolixibacter, Robinsoniella, and Wandonia. Prevotella was found to be one of the main components of the seminal microbiome^​19​.

Men undergoing vasectomy had the microbial composition of semen evaluated before and after the surgery, with vasectomy resulting in a decrease in α-diversity, but overall the samples were not vastly different^​20​.

Microbiome of the prostate, seminal vesicles and bulbourethral glands

Semen is comprised mainly of fluids from accessory glands – the prostate, seminal vesicles and bulbourethral glands. Interest in the microbiomes of these glands is increasing in terms of the relationship with prostate cancer^​20​.

Studies show the existence of a prostatic microbiome.^​21,22​

Samples taken from men with aggressive prostate cancer showed the Enterobacteteriaceae family was highly prevalent – 37-81%. Escherichia spp. were found in all samples, at around 30% of all results. Other bacterial families included Actinobacteria, Pseudomonas and Streptococcus, though at very low abundance.^​23​

In another study into the bacterial patterns of prostate biopsies found Actinobacteria dominated, followed by Firmicutes and Proteobacteria. Major species included Proionibacterium, Corynebacterium, and Staphylococcus. Prevotella was, interestingly, not detected, despite being found in high abundance in other studies.^​24​

In men with benign prostatic hyperplasia (BPH), Proteobacteria were dominant (around 50%)^​25​. The bacterial patterns did not match those found by Next Generation Sequencing (NGS) testing, as they were tested using older culturing methods which are not as specific. A similar study found Firmicutes dominated in BPH^​26​.

The urinary microbiome and prostate microbiome were significantly different, indicating a unique local colony.

The seminal vesicle and bulbourethral gland microbiomes remain unknown due to sampling challenges. In one study of the seminal vesicles Firmicutes were dominant (52%), followed by Bacteroidetes (22%), Proteobacteria (13%), Actinobacteria (10%) and Fusobacteria (2%). Specific genera included Bacteroides (9%), Lactobacillus (5%), Bifidobacterium (5%) and Faecalibacterium (5%).^​27​

Patients with and without signs of infection didn’t differ significantly, but importantly, samples from seminal vesicles didn’t differ greatly from urine samples obtained prior to the operation, highlighting possible contamination.

Urethral microbiome

Studies have examined the microbial content of first void urine samples^{​28–30​} of men, and urethral samples^​29​ with both samples showing similar bacterial profiles. Recurring themes include Lactobacillus, Streptococcus, Sneathia, Veillonella, Corynebacterium and Prevotella. The most common STI was gonorrhoea.

However, other studies found that the sampling types revealed different microbiome patterns^​28​, implying a specific urethral microbiome^​31​, with first-catch and mid-stream urine samples showing significantly different alpha diversity.

In first-catch urine samples, Prevotella, Streptococcus and Campylobacter were abundant.

The urethral microbiome was influenced in men with and without urethritis and depended on the sex of their partner. Haemophilus influenzae was significantly increased in men with male partners, while Corynebacterium spp. was significantly increased in men with female partners.

Microbiome of the penis and glans

Penile skin has been examined for its microbiota composition multiple times^{​32–34​}, with results showing colonisation patterns dominated by Corynebacterium and Staphylococcus, which are typical skin commensals^​5,35​.

The sexual entry sites for STIs are the foreskin mucosa and penis glans, with dysbiosis with anaerobic bacteria increasing the risk of HIV infection^​7–9​. Anaerobic-dominant microbiomes influence local production of inflammatory cytokines which impact the immune system, with Peptostreptococcus, Prevotella and Dialister increasing cytokine production, attracting HIV-susceptible CD4+ T cells to the inner foreskin^​36​.

Circumcision is seen to drastically impact the penile microbiome, with increased access to oxygen reducing anaerobic species such as Prevotella, Anaerococcus, Finegoldia and Peptoniphilus.

Circumcision was also associated with lower bacterial load and diversity, increasing Corynebacterium spp. and Staphylococcus spp.

Circumcision is also associated with a reduction in bacterial vaginosis in female partners^​37​. If the penile microbiome is largely anaerobic, this may trigger immune system activation and an increase in STIs^​38​.

Microbiome of semen

The most abundant genera found in the seminal microbiome were Ralstonia, Lactobacillus, Corynebacterium, Streptococcus and Staphylococcus. Anaerococcus was associated with poorer sperm quality.^​39​

Three seminal bacterial community types have been identified:

1. G1 (Pseudomonas-predominant group)
2. G2 (Lactobacillus-predominant group)
   Associated with better sperm quality
3. G3 (Prevotella-predominant group)
   Associated with poorer sperm quality

Gardnerella vaginalis – associated with BV – was positively correlated with sperm quality^​40​.

Low motility and abnormal spermiograms were associated with Prevotella-predominant microbiota. Increased abundance of Lactobacillus spp. was correlated with normal semen morphology. Staphylococcus was linked to normal spermiogram and high total motility. Overall, low abundance was confirmed.^{​41–43​}

All studies, however, do not agree, which may be due to geographical or testing differences affecting the microbiome.

In other research, pathogenic bacteria (Neisseria spp., Klebsiella spp., and Pseudomonas spp.) were associated with seminal thickness (hyperviscosity) and low sperm count.

A high prevalence of Enterococcus spp. was found. In infertile men, Aerococcus, Rhodocytophaga and Gemella were increased, and in normal sperm, Colinsella spp.^​44​

References

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