A taxon-specific measurement of disruption in a multi-modal study of microbiomes and metabolomes reveals system-wide dysbiosis preceding HIV-1 infection

F. Fouladi, Y. Chen, S. Bera, A. K. Jarmusch, D. Van Tyne, F. J. Palella, J. B. Margolick, K. W. Chew, J. Sun, J. Martinson, C. R. Rinaldo and S. D. Peddada ()
Additional contact information
F. Fouladi: Research Triangle Park, Biostatistics and Computational Biology Branch, Division of Intramural Research, National Institute of Environmental Health Sciences, National Institutes of Health
Y. Chen: University of Pittsburgh School of Medicine, Division of Infectious Diseases, Department of Medicine
S. Bera: Research Triangle Park, Biostatistics and Computational Biology Branch, Division of Intramural Research, National Institute of Environmental Health Sciences, National Institutes of Health
A. K. Jarmusch: Research Triangle Park, Immunity, Inflammation, and Disease Laboratory, Division of Intramural Research, National Institute of Environmental Health Sciences, National Institutes of Health
D. Van Tyne: University of Pittsburgh School of Medicine, Division of Infectious Diseases, Department of Medicine
F. J. Palella: Northwestern University, Division of Infectious Diseases, Feinberg School of Medicine
J. B. Margolick: Johns Hopkins University, Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health
K. W. Chew: David Geffen School of Medicine at University of California, Los Angeles, Division of Infectious Diseases, Department of Medicine
J. Sun: Johns Hopkins University, Department of Epidemiology, Bloomberg School of Public Health
J. Martinson: University of Pittsburgh, Department of Infectious Diseases and Microbiology, School of Public Health
C. R. Rinaldo: University of Pittsburgh School of Medicine, Division of Infectious Diseases, Department of Medicine
S. D. Peddada: Research Triangle Park, Biostatistics and Computational Biology Branch, Division of Intramural Research, National Institute of Environmental Health Sciences, National Institutes of Health

Nature Communications, 2025, vol. 16, issue 1, 1-14

Abstract: Abstract The microbiome plays an important role in immune responses and inflammation in HIV-1 infection. Hence, a deeper understanding of the changes in the microbiome, its function and metabolites, and their interactions prior to HIV-1 infection is potentially important for HIV-1 prevention strategies. Using stool, oral washes, and plasma biospecimens obtained from men who have sex with men (MSM) and who were without HIV-1, we found several differences in microbial ecologies, gene functions, and metabolites between MSM who became HIV-1 infected (Pre-HIV) within six months and those who remained HIV-1 uninfected (Non-HIV). The Pre-HIV group had an enrichment of enzymes involved in purine metabolism, lower amino acid metabolism, and higher oxidative stress before the infection compared to the Non-HIV group. We also introduced a novel and broadly applicable taxon-specific measure of DISruption in COrrelations (DISCO) with other features, such as microbial taxa and metabolites in a given group (e.g., Pre-HIV group) relative to a reference group (e.g., Non-HIV group). Using DISCO, we identified several gut and oral species with disrupted correlations prior to HIV-1 infection. Application of DISCO to external datasets revealed that Prevotella spp. are consistently disrupted in their correlations across multiple cohorts prior to or following HIV-1 infection.

Date: 2025
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DOI: 10.1038/s41467-025-64822-z

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