Mucosal architecture, microbiota resilience and metabolic disruption reveal holobiont dynamics during bovine respiratory disease
Abstract
The gut-airway axis is increasingly recognised as an important determinant of respiratory health in livestock. However, the interactions among respiratory infections, microbial communities, mucosal barrier function, and microbial metabolism that underpin this axis remain poorly understood. Here, we combined longitudinal immunological, mucosal, microbiological, and metabolic analyses to characterise host-microbiota interactions during antibiotic treatment and experimental bovine respiratory disease (BRD). We found that the bovine respiratory tract is organised as a hierarchically structured mucosal ecosystem, with compartment-specific mucin expression patterns associated with distinct microbial communities. Within this framework, increasing respiratory pathogen loads were associated with greater clinical severity, oxidative stress, acute inflammation, and targeted alterations in mucosal regulation and microbial composition, while serum amyloid A emerged as the host biomarker most closely reflecting infection intensity. Although infection altered host and microbial states, antimicrobial treatment represented the dominant ecological perturbation. Antibiotic exposure reshaped both respiratory and intestinal microbial communities, reducing diversity, increasing community drift, and driving coordinated ecological transitions across the gut-airway axis that exceeded the effects of infection alone. Importantly, these compositional changes were accompanied by profound reductions in acetate, propionate, butyrate, and valerate, identifying short-chain fatty acids as a major functional consequence of gut microbiota disruption. Integrative multi-omics analyses revealed that mucosal organisation, microbial diversity, microbial metabolism, and immune activity were embedded within a highly structured gut-airway 1 network. Together, these findings support a holobiont view of BRD in which disease outcomes emerge not only from pathogen-host interactions but also from ecological disturbances that propagate across interconnected mucosal compartments. Notably, antimicrobial treatment affected ecosystem structure and function more than infection itself, highlighting potential trade-offs between pathogen control and microbiota stability. Preserving microbial resilience and its metabolic functions may therefore represent an important component of future strategies to improve respiratory health and disease resilience in cattle.
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BibTeX
@misc{sergio2026mucosal,
title = {{Mucosal architecture, microbiota resilience and metabolic disruption reveal holobiont dynamics during bovine respiratory disease}},
author = {Méndez Sergio and Guenaelle Derolez and Florence Mompart and Monie--Ibanes Maverick and Thomas Peyret and Corbin Marie and Bars-Cortina David and Sikht Fatima-Zohra and Geffré Anne and Pot Gwendoline and Robert Hortensia and Yves Farizon and Christine Citti and Eric A. Richard and Laurent Xavier Nouvel and Jansen Christine and Dudek Katarzyna and Schnee Christiane and Baranowski Eric and Meyer Gilles and Mariette F. Ducatez and Mach Núria},
howpublished = {HAL},
year = {2026},
month = oct,
url = {https://hal.inrae.fr/hal-05774858v1},
note = {CC BY-NC-ND 4.0},
}
RIS
TY - UNPB
TI - Mucosal architecture, microbiota resilience and metabolic disruption reveal holobiont dynamics during bovine respiratory disease
AU - Méndez Sergio
AU - Guenaelle Derolez
AU - Florence Mompart
AU - Monie--Ibanes Maverick
AU - Thomas Peyret
AU - Corbin Marie
AU - Bars-Cortina David
AU - Sikht Fatima-Zohra
AU - Geffré Anne
AU - Pot Gwendoline
AU - Robert Hortensia
AU - Yves Farizon
AU - Christine Citti
AU - Eric A. Richard
AU - Laurent Xavier Nouvel
AU - Jansen Christine
AU - Dudek Katarzyna
AU - Schnee Christiane
AU - Baranowski Eric
AU - Meyer Gilles
AU - Mariette F. Ducatez
AU - Mach Núria
PY - 2026
DA - 2026/10/02
PB - HAL
UR - https://hal.inrae.fr/hal-05774858v1
AB - The gut-airway axis is increasingly recognised as an important determinant of respiratory health in livestock. However, the interactions among respiratory infections, microbial communities, mucosal barrier function, and microbial metabolism that underpin this axis remain poorly understood. Here, we combined longitudinal immunological, mucosal, microbiological, and metabolic analyses to characterise host-microbiota interactions during antibiotic treatment and experimental bovine respiratory disease (BRD). We found that the bovine respiratory tract is organised as a hierarchically structured mucosal ecosystem, with compartment-specific mucin expression patterns associated with distinct microbial communities. Within this framework, increasing respiratory pathogen loads were associated with greater clinical severity, oxidative stress, acute inflammation, and targeted alterations in mucosal regulation and microbial composition, while serum amyloid A emerged as the host biomarker most closely reflecting infection intensity. Although infection altered host and microbial states, antimicrobial treatment represented the dominant ecological perturbation. Antibiotic exposure reshaped both respiratory and intestinal microbial communities, reducing diversity, increasing community drift, and driving coordinated ecological transitions across the gut-airway axis that exceeded the effects of infection alone. Importantly, these compositional changes were accompanied by profound reductions in acetate, propionate, butyrate, and valerate, identifying short-chain fatty acids as a major functional consequence of gut microbiota disruption. Integrative multi-omics analyses revealed that mucosal organisation, microbial diversity, microbial metabolism, and immune activity were embedded within a highly structured gut-airway 1 network. Together, these findings support a holobiont view of BRD in which disease outcomes emerge not only from pathogen-host interactions but also from ecological disturbances that propagate across interconnected mucosal compartments. Notably, antimicrobial treatment affected ecosystem structure and function more than infection itself, highlighting potential trade-offs between pathogen control and microbiota stability. Preserving microbial resilience and its metabolic functions may therefore represent an important component of future strategies to improve respiratory health and disease resilience in cattle.
ER -