Lactic acid mediates Lactobacillus johnsonii protection against Ascaridia galli infection in chickens
Ascaridia galli remains highly prevalent in poultry production and is primarily controlled with chemical anthelmintics, raising concerns about drug resistance and residue contamination. Our previous study showed that A. galli infection markedly reduced the abundance of Lactobacillus johnsonii in the chicken gut, suggesting its potential as a probiotic-based strategy for parasite control. In this study, forty 1-day-old chicks were randomly assigned to four groups: control, A. galli + PBS, PBS + L. johnsonii, and A. galli + L. johnsonii. Chicks were orally infected with 1,000 A. galli eggs and/or supplemented daily with L. johnsonii for 14 days. A. galli infection significantly impaired growth performance, disrupted intestinal barrier integrity, induced oxidative stress-mediated apoptosis, and increased pro-inflammatory cytokine expression. These pathological alterations were markedly alleviated by L. johnsonii supplementation, which also partially restored body weight gain and feed efficiency. In addition, 16S rRNA sequencing showed that L. johnsonii reshaped the parasite-disturbed gut microbiota and significantly reduced intestinal worm burden. Mass spectrometry of the culture supernatant, combined with in vitro co-culture assays, identified DL-lactic acid as the principal anthelmintic effector of L. johnsonii. In vivo, lactic acid largely recapitulated the protective effects of L. johnsonii by improving intestinal metabolic function, reducing oxidative stress and inflammation, and preserving barrier integrity. Moreover, lactic acid significantly increased the intestinal abundance of L. johnsonii, indicating a positive feedback loop that synergistically enhances protection against A. galli infection. Collectively, these findings demonstrated that L. johnsonii exerted anti-parasitic effects primarily through lactic acid production. Lactic acid appeared to exert dual functions by directly killing parasites while maintaining intestinal homeostasis, thereby highlighting a promising and sustainable microbiota-based strategy for the control of A. galli infection in poultry.