TY - JOUR
T1 - Effect of the gut microbiota-derived tryptophan metabolite indole-3-acetic acid in pneumonia
AU - Kullberg, Robert F J
AU - van Linge, Christine C A
AU - Haak, Bastiaan W
AU - Paul, Prasanjit S
AU - Butler, Joe M
AU - Wolff, Nora
AU - van Engelen, Tjitske S R
AU - Sikkens, Jonne J
AU - Bomers, Marije K
AU - Lefèvre, Antoine
AU - Cremer, Olaf L
AU - Roelofs, Joris J T H
AU - Sovran, Bruno
AU - van den Wijngaard, René
AU - de Vos, Alex F
AU - de Jonge, Wouter J
AU - van der Poll, Tom
AU - Wiersinga, W Joost
N1 - Publisher Copyright:
© The Author(s) 2025.
PY - 2025/9/29
Y1 - 2025/9/29
N2 - Gut microbiota influence the severity of pneumonia by producing metabolites that enhance systemic and pulmonary immune responses. Preclinical studies suggested that gut microbiota-derived indoles have protective effects against numerous diseases, including influenza and abdominal infections. However, the precise role of tryptophan metabolites during pneumonia is unknown. Here, we perform translational analyses in a large general-population cohort (n = 13,464), critically ill patients with severe community-acquired pneumonia (CAP; n = 158; NCT01905033), a randomized human intervention trial on antibiotic-mediated microbiota modulation (NCT03051698), and mice to investigate the effects of tryptophan metabolites, specifically indole-3-acetic acid (IAA), on pneumonia. In the population-based cohort, baseline IAA is associated with a higher risk of future hospital admission for pneumonia (cause-specific hazard ratio 1.15, 95% confidence interval 1.09-1.22 p < 0.0001). In patients with severe CAP higher levels of IAA are associated with increased mortality, independent from potential confounders (hazard ratio 1.30 per log2 increase, 95% confidence interval 1.02-1.68, p = 0.037). In a mouse model of bacterial pneumonia, IAA supplementation aggravates pulmonary damage while reducing systemic dissemination, which is mediated by the aryl hydrocarbon receptor (AhR) and increased release of reactive oxygen species from neutrophils. In summary, these findings from general population and severe pneumonia cohorts, and murine pneumonia experiments, show that the gut microbiota-derived tryptophan metabolite IAA affects pneumonia, suggesting that various indoles may have diverging, context-dependent effects.
AB - Gut microbiota influence the severity of pneumonia by producing metabolites that enhance systemic and pulmonary immune responses. Preclinical studies suggested that gut microbiota-derived indoles have protective effects against numerous diseases, including influenza and abdominal infections. However, the precise role of tryptophan metabolites during pneumonia is unknown. Here, we perform translational analyses in a large general-population cohort (n = 13,464), critically ill patients with severe community-acquired pneumonia (CAP; n = 158; NCT01905033), a randomized human intervention trial on antibiotic-mediated microbiota modulation (NCT03051698), and mice to investigate the effects of tryptophan metabolites, specifically indole-3-acetic acid (IAA), on pneumonia. In the population-based cohort, baseline IAA is associated with a higher risk of future hospital admission for pneumonia (cause-specific hazard ratio 1.15, 95% confidence interval 1.09-1.22 p < 0.0001). In patients with severe CAP higher levels of IAA are associated with increased mortality, independent from potential confounders (hazard ratio 1.30 per log2 increase, 95% confidence interval 1.02-1.68, p = 0.037). In a mouse model of bacterial pneumonia, IAA supplementation aggravates pulmonary damage while reducing systemic dissemination, which is mediated by the aryl hydrocarbon receptor (AhR) and increased release of reactive oxygen species from neutrophils. In summary, these findings from general population and severe pneumonia cohorts, and murine pneumonia experiments, show that the gut microbiota-derived tryptophan metabolite IAA affects pneumonia, suggesting that various indoles may have diverging, context-dependent effects.
KW - Aged
KW - Animals
KW - Anti-Bacterial Agents/therapeutic use
KW - Disease Models, Animal
KW - Female
KW - Gastrointestinal Microbiome/physiology
KW - Hospitalization
KW - Humans
KW - Indoleacetic Acids/metabolism
KW - Male
KW - Mice
KW - Mice, Inbred C57BL
KW - Middle Aged
KW - Pneumonia, Bacterial/microbiology
KW - Pneumonia/metabolism
KW - Tryptophan/metabolism
U2 - 10.1038/s41467-025-63611-y
DO - 10.1038/s41467-025-63611-y
M3 - Article
C2 - 41022731
SN - 2041-1723
VL - 16
JO - Nature Communications
JF - Nature Communications
IS - 1
M1 - 8565
ER -