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Serum metabolites link immune-microbiota interaction in children and young adults from Russian Karelia and Finnish Karelia with contrasting lifestyle and environment.

Piia Karisola,H. Sinkko,Anni I. Nieminen,T. Laatikainen,Ying Yang,L. Paalanen,Pekka Jousilahti,Erkki Vartiainen,M. J. Mäkelä,N. Fyhrquist,T. Haahtela,H. Alenius

Published 2025 in Environment International

ABSTRACT

BACKGROUND Environmental exposureregulates the immune, circulatory, and nervous systems, thereby affecting health. We investigated the associations between serum metabolite profiles, skin microbiota, and immune-related gene expression of peripheral blood mononuclear cells in children and young adults from Russian Karelia (RUS) and Finnish Karelia (FIN), two regions with contrasting environmental exposures and lifestyles. METHODS Serum metabolites (n = 278) from 15 to 20-year-old participants from RUS (n = 162) and FIN (n = 116) were profiled. Using integrative analysis, a subset of metabolomics was combined with skin microbiota (n = 143) and blood transcriptomics (n = 144) to characterize environment-linked metabolic and immune signatures. RESULTS Serum metabolite profiles differed significantly between the RUS and FIN subjects, reflecting divergent metabolic states. Citrulline and glutamate/glutamine metabolism were prominent in the RUS subjects while tryptophan catabolism was enhanced in the FIN subjects. Transcriptomic network analysis identified co-expression modules associated with metabolites, skin microbial taxa and key immune traits. A strongly RUS-associated module was dominated by epigenetic long non-coding RNAs and associated positively with anti-inflammatory metabolites such as circulating short-chain fatty acids (SCFAs) and betaine - both present at reduced levels in the FIN subjects. In contrast, FIN-associated modules were linked to inflammatory metabolites such as xanthurenic acid and L-cystine, as well as gene pathways involved in interferon (anti-viral) signaling and neutrophil responses. Across all omics layers, RUS subjects exhibited a more tightly integrated molecular network, with stronger correlations between circulating metabolites, microbial taxa and immune-related gene regulation. CONCLUSIONS Multi-omics integration revealed a more coordinated and responsive immune-metabolic network in RUS youth, potentially shaped by environmental exposures typical of their living context. In contrast, the FIN cohort exhibited metabolic patterns more closely linked to inflammatory gene expression.

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