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Establishment of a non-Westernized gut microbiota in men who have sex with men is associated with sexual practices.

ABSTRACT: The human gut microbiota is influenced by various factors, including health status and environmental conditions, yet considerable inter-individual differences remain unexplained. Previous studies identified that the gut microbiota of men who have sex with men (MSM) is distinct from that of non-MSM. Here, we reveal through species-level microbiota analysis using shotgun metagenomics that the gut microbiota of many MSM with Western origin resembles gut microbial communities of non-Westernized populations. Specifically, MSM gut microbiomes are frequently dominated by members of the Prevotellaceae family, including co-colonization of species from the Segatella copri complex and unknown Prevotellaceae members. Questionnaire-based analysis exploring inter-individual differences in MSM links specific sexual practices to microbiota composition. Moreover, machine learning identifies microbial features associated with sexual activities in MSM. Together, this study shows associations of sexual activities with gut microbiome alterations in MSM, which may have a large impact on population-based microbiota studies.

SUBMITTER: Huang KD

PROVIDER: S-EPMC10982974 | biostudies-literature | 2024 Mar

REPOSITORIES: biostudies-literature

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Establishment of a non-Westernized gut microbiota in men who have sex with men is associated with sexual practices.

Huang Kun D KD Amend Lena L Gálvez Eric J C EJC Lesker Till-Robin TR de Oliveira Romulo R Bielecka Agata A Blanco-Míguez Aitor A Valles-Colomer Mireia M Ruf Isabel I Pasolli Edoardo E Buer Jan J Segata Nicola N Esser Stefan S Strowig Till T Kehrmann Jan J

Cell reports. Medicine 20240215 3

The human gut microbiota is influenced by various factors, including health status and environmental conditions, yet considerable inter-individual differences remain unexplained. Previous studies identified that the gut microbiota of men who have sex with men (MSM) is distinct from that of non-MSM. Here, we reveal through species-level microbiota analysis using shotgun metagenomics that the gut microbiota of many MSM with Western origin resembles gut microbial communities of non-Westernized popu ...[more]

PMID: 38366600

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Project description:Urbanization has changed life styles of the children in some towns and cities on Leyte island in the Philippines. To evaluate the impact of modernization in dietary habits on gut microbiota, we compared fecal microbiota of 7 to 9-year-old children from rural Baybay city (n = 24) and urban Ormoc city (n = 19), and assessed the correlation between bacterial composition and diet. A dietary survey indicated that Ormoc children consumed fast food frequently and more meat and confectionary than Baybay children, suggesting modernization/westernization of dietary habits. Fat intake accounted for 27.2% of the total energy intake in Ormoc children; this was remarkably higher than in their Baybay counterparts (18.1%) and close to the upper limit (30%) recommended by the World Health Organization. Their fecal microbiota were analyzed by high-throughput 16S rRNA gene sequencing in conjunction with a dataset from five other Asian countries. Their microbiota were classified into two enterotype-like clusters with the other countries' children, each defined by high abundance of either Prevotellaceae (P-type) or Bacteroidaceae (BB-type), respectively. Baybay and Ormoc children mainly harbored P-type and BB-type, respectively. Redundancy analysis showed that P-type favored carbohydrates whereas BB-type preferred fats. Fat intake correlated positively with the Firmicutes-to-Bacteroidetes (F/B) ratio and negatively with the relative abundance of the family Prevotellaceae/genus Prevotella. A species-level analysis suggested that dietary fat positively correlated with an Oscillibacter species as well as a series of Bacteroides/Parabacteroides species, whereas dietary carbohydrate positively correlated with Dialister succinatiphilus known as succinate-utilizing bacteria and some succinate-producing species of family Prevotellaceae, Veillonellaceae, and Erysipelotrichaceae. We also found that a Succinivibrio species was overrepresented in the P-type community, suggesting the syntroph via hydrogen and succinate. Predicted metagenomics suggests that BB-type microbiota is well nourished and metabolically more active with simple sugars, amino acids, and lipids, while P-type community is more involved in digestion of complex carbohydrates. Overweight and obese children living in Ormoc, who consumed a high-fat diet, harbored microbiota with higher F/B ratio and low abundance of Prevotella. The altered gut microbiota may be a sign of a modern diet-associated obesity among children in developing areas.

Project description:BackgroundThe association between gut microbial metabolites and immunologic non-response among people living with HIV (PLHIV) receiving antiretroviral therapy (ART) has not been well established. We aimed to characterize gut microbial metabolites among HIV-infected men who have sex with men (MSM) with different immunologic responses.MethodsWe recruited HIV-infected MSM from Guangzhou Eighth People's Hospital and HIV-uninfected MSM (healthy controls, HC) from a local MSM community-based organization in Guangzhou between June and October 2021. HIV-infected MSM were grouped into good immunological responders (GIR) (CD4 + T cell count ≥ 350 cells/μl) and poor immunological responders (PIR) (CD4 + T cell count < 350 cells/μl) after 24 months of ART treatment. Online questionnaires and stool samples were collected. Microbial metabolites in stool were obtained through ultra-performance liquid chromatography coupled to a tandem mass spectrometry (UPLC-MS/MS) system. Differential metabolites were identified and analyzed using the Kruskal-Wallis test, followed by pairwise comparisons with the Wilcoxon rank-sum test. The least absolute selection and shrinkage operator was used to select potential metabolites biomarkers.ResultsA total of 51 HC, 56 GIR, and 42 PIR were included. No statistically significant differences were observed in the median time since HIV diagnosis and ART duration between GIR and PIR. Among the 174 quantified metabolites, 81 significantly differed among HC, GIR, and PIR (P < 0.05). Among differential metabolites, indole-3-propionic acid significantly decreased from HC (11.39 nmol/g) and GIR (8.16 nmol/g) to PIR (6.50 nmol/g). The pathway analysis showed that tryptophan metabolism differed significantly between GIR and PIR (P < 0.05). Four potential metabolites biomarkers (dimethylglycine, cinnamic acid, 3-hydroxyisovaleric acid, and propionic acid) that distinguish GIR and PIR were identified, and the corresponding area under the curve based on potential biomarkers was 0.773 (95% CI: 0.675-0.871).ConclusionsThis study identified significant differences in gut microbial metabolites among HIV-infected MSM with different immunologic responses. These results indicate the potential of gut microbial metabolites as novel disease progression markers and therapeutic targets.

Project description:ObjectivesIn the United States, all men who have sex with men (MSM) were banned from donating blood from 1985 through 2015. In 2016, the guideline was amended such that men who had sexual contact with other men within the previous 12 months could not donate blood. We aimed to identify blood donation practices and their relationship with HIV risk and testing among young adult MSM (YMSM) at risk for having HIV.MethodsIn 2014, we recruited HIV-negative non-Hispanic black, Hispanic, and non-Hispanic white YMSM aged 18-24 from across the United States through social media platforms to complete an online survey. Among these YMSM who previously donated blood, we conducted a secondary analysis examining the relationship between having donated blood within the past 12 months and sexual risk behavior from recent condomless anal intercourse (CAI), HIV testing, and self-perceived risk of having an undiagnosed HIV infection.ResultsOf the 2261 YMSM surveyed, 1104 (48.8%) had ever previously donated blood and 305 (13.5%) had donated blood within the past 12 months. Of the 305 blood donors, 50 (16.4%) had ever had CAI before their most recent blood donation. Among YMSM who donated blood, past-12-month blood donation was more likely among YMSM who never had CAI (adjusted odds ratio [aOR] = 1.84; 95% confidence interval [CI], 1.24-2.73) than among YMSM who had CAI and more likely among YMSM who believed it was not possible at all that they had an undiagnosed HIV infection (aOR = 1.57; 95% CI, 1.14-2.16) than among YMSM who believed there was any possibility of having an undiagnosed HIV infection; it was not related to past-12-month HIV testing.ConclusionsYMSM donated blood frequently, suggesting that the deferral process in place did not prevent YMSM from donating blood. The current donor screening process should be reconsidered if it is to prevent YMSM from donating blood. Future research could identify screening questions that permit YMSM with a low risk of HIV infection to donate blood while maintaining the safety of the blood supply.

Dataset Information

Establishment of a non-Westernized gut microbiota in men who have sex with men is associated with sexual practices.

Publications

Establishment of a non-Westernized gut microbiota in men who have sex with men is associated with sexual practices.

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