Microbiome

Microbial Community Restructuring Underlies Thermotolerance in Heat-Stressed Lactating Sows: An Integrated Multi-Omics Analysis

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Abstract

Heat stress compromises lactational performance in swine, causing substantial economic losses as climate change intensifies thermal challenges. While gut microbiome alterations during heat stress are recognized, the mechanistic basis of genetic variation in thermotolerance through host-microbiome interactions remains incompletely understood. We conducted an integrated multi-omics investigation to characterize metabolic and microbial adaptive responses in genetically divergent lines during lactation under heat stress.Two genetic lines divergent for thermotolerance genomic estimated breeding values (TOL, n=12; SEN, n=13) were subjected to cyclic heat stress (12h on/12h off) from day 4 to day 18 of lactation. Fecal samples were collected for metabolomic profiling (days 0, 14, 18; n=12,714 metabolites across 136 guilds), metagenomic analysis (days 4, 8, 14; 21 functional guilds), and metatranscriptomic sequencing (days 0, 18; 22 functional guilds). Guild-based analytical frameworks organized metabolites by chemical classification and microbial functions by metabolic pathways. Linear mixed-effects models evaluated temporal dynamics, genetic line effects, and their interactions, with post-hoc comparisons using false discovery rate correction and Cohen's d effect sizes.Temporal dynamics dominated across all omics platforms, with timepoint effects explaining substantially more variance than genetic line effects. Metabolomically, sphingolipids exhibited the strongest temporal depletion (p< 0.001), with 32 guilds showing significant temporal changes. Group à— timepoint interactions in sphingomyelins (p=0.036) indicated differential sphingolipid management between lines. Metagenomically, a three-phase pattern emerged: early divergence (day 4), transitional convergence (day 8), and pronounced late divergence (day 14). Enhanced methanogenic capacity specifically in TOL animals represented the largest effect (d=-0.920), coupled with increased fermentation and short-chain fatty acid production capacity. Metatranscriptomically, 68% of guilds showed temporal changes, predominantly downregulation, with carbohydrate metabolism exhibiting significant group à— timepoint interaction (p=0.015).A pattern of discordance emerged: TOL animals exhibited increased metagenomic functional capacity but decreased transcriptional activity across multiple guilds (fermentation, stress response, protein degradation, mucin degradation), suggesting adaptive community restructuring toward functional redundancy rather than sustained transcriptional investment. This strategy may be energetically advantageous during lactation's metabolic demands. In contrast, SEN animals maintained transcriptional activity without adaptive community restructuring, suggesting reduced metabolic flexibility. Baseline differences between lines were minimal, suggesting that thermotolerance manifests primarily as differential temporal response capacity rather than constitutive phenotypic differences.These findings suggest that thermotolerance in lactating sows may involve coordinated microbial community restructuring that achieves metabolic homeostasis through functional redundancy while minimizing energetic costs. Enhanced methanogenesis, increased fermentative capacity, and efficient transcriptional resource allocation appear to distinguish thermotolerant phenotypes. These mechanistic insights may inform genetic selection strategies and suggest potential intervention approaches-including dietary fiber supplementation and methanogen modulation-to enhance lactational thermotolerance under climate change scenarios.This research was supported by the USDA National Institute of Food and Agriculture (NIFA) under grants 2020-67015-3157 and 2022-67015-38319.

Keywords: 2026

How to Cite:

Maltecca, C., Gini, C., Wen, W., Byrd, M., van Vliet, S., Brito, L., Johnson, J., Jiang, J. & Tiezzi, F., (2026) “Microbial Community Restructuring Underlies Thermotolerance in Heat-Stressed Lactating Sows: An Integrated Multi-Omics Analysis”, World Congress on Genetics Applied to Livestock Production Digital Archive 2026(1): 2284552. doi: https://doi.org/10.31274/wcgalp.23588

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