Pulmonary mucoid Pseudomonas aeruginosa infection and association with higher species richness and stronger inflammatory immune response

The mucoid phenotype of Pseudomonas aeruginosa (PA) is regarded as a comprehensive adaptive stress response to difficult environmental circumstances. However, there is little knowledge about the relationship between the prevalence of mucoid PA and species richness and immune inflammatory response. A case-control study was conducted in hospitalized patients with pulmonary infections caused by mucoid and non-mucoid PA. Sputum samples were subjected to 16S rDNA sequencing to characterize microbial diversity and taxonomic composition, while serum levels of TNF-α, IL-6, IL-8, IL-10, and IL-17 were measured using enzyme-linked immunosorbent assays. Subsequent statistical analysis using R 4.0 revealed significant correlations between differentially abundant microbial taxa and cytokine profiles. Compared to the non-mucoid PA group, the mucoid PA group demonstrated significantly higher α-diversity indices in terms of species richness, as indicated by the Chao1 (P = 0.0015) and Observed-species metrics (P = 0.0014). Furthermore, distinct β-diversity patterns were observed between the two groups (P Veillonella spp., Haemophilus spp., Porphyromonas spp., Prevotella spp., Actinomyces spp., Lactobacillus spp., and Rothia spp. in the mucoid PA group, while Stenotrophomonas spp., Acinetobacter spp., Parvimonas spp., and Serratia spp. dominated in the non-mucoid PA group. The mucoid PA infections showed marked elevation of IL-8 (P = 0.0137), TNF-α (P = 0.0048), IL-10 (P = 0.0042), IL-17 (P = 0.0220), and IL-6 (P = 0.0001). Spearman correlation revealed Veillonella spp./Rothia spp./Porphyromonas spp./Prevotella spp. positively correlated with IL-10/TNF-α/IL-17/IL-6, whereas Haemophilus spp. showed a negative relationship with IL-17. Stenotrophomonas spp. exhibited strong negative correlations with IL-10/IL-6, and Serratia spp. was inversely associated with TNF-α in non-mucoid PA infections. Clinically distinct microbial ecosystems in mucoid PA correlate with exacerbated inflammation. This phenotype-driven dichotomy provides actionable biomarkers for stratified antimicrobial/immunomodulatory therapies in chronic lung disease.IMPORTANCEThis study holds significant clinical and scientific importance, as it elucidates the critical differences between mucoid and non-mucoid Pseudomonas aeruginosa (PA) infections in pulmonary patients. By demonstrating that mucoid PA infections are associated with distinct microbial ecosystems (higher species richness and different taxonomic compositions) and more severe inflammatory responses (elevated TNF-α, IL-6, IL-8, IL-10, and IL-17), the research provides crucial insights into phenotype-specific pathogenesis. The identified correlations between specific bacterial species (e.g., Veillonella/Rothia with pro-inflammatory cytokines) offer potential biomarkers for clinical stratification. These findings are particularly valuable for developing targeted therapeutic strategies, as they suggest mucoid PA infections may require different antimicrobial/immunomodulatory approaches compared to non-mucoid variants. The study bridges an important knowledge gap in understanding how bacterial phenotypic adaptation influences host-microbiome interactions and disease outcomes in chronic lung infections.