Heat stress and avian pathogenic Escherichia coli infection differentially alter bacterial colonization dynamics, mucosal and systemic immunity, and cecal microbiome homeostasis in late-production laying hens in cage-free housing.

Abstract

Heat stress (HS) and avian pathogenic E. coli (APEC) infection are major challenges to the health and productivity of commercial laying hens, yet their combined effects remain poorly understood. This study evaluated the effects of continuous HS and oral APEC O78 infection on production performance, bacterial colonization, immune responses, and the cecal microbiome of 70-week-old Hy-Line W-36 cage-free laying hens. Four treatments, thermoneutral control (TNC), thermoneutral APEC-inoculated (TNI), heat stress control (HSC), and heat stress APEC-inoculated (HSI), were assigned to a total of 112 hens. The indoor thermal environmental conditions were set at either 22°C or 35°C, and half the birds in each infected group received 1 × 10⁹ CFU of APEC O78 by oral gavage and were co-housed with non-inoculated contact birds. Heat stress negatively affected egg production and egg weight, whereas APEC infection alone did not further impair production performance. APEC rapidly established persistent gastrointestinal colonization regardless of thermal environment, while HS uniquely exacerbated pulmonary colonization at 7 days post-inoculation. Compared with the control and single-challenge groups, the combined HS and APEC challenge induced greater upregulation of splenic IL-6, TNF-α, and Hsp70, and altered mucosal immunity by attenuating APEC-induced conventional TCRαβ⁺ intraepithelial lymphocyte responses while expanding non-conventional innate lymphoid populations. Cecal microbiome analysis identified HS as the primary driver of microbial dysbiosis, with the combined challenge producing the greatest reduction in microbial richness and the highest number of differentially abundant genera. Predicted functional profiling further indicated disruption of microbial metabolic pathways involved in purine degradation and arginine biosynthesis under the combined HS and APEC challenge. These findings demonstrate that HS exacerbates APEC-associated immune dysregulation and microbiome disruption, highlighting the importance of integrated thermal management and infection control strategies to improve hen health and productivity in commercial egg production.

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