Abstract
Ostertagia ostertagi is a highly prevalent nematode that affects grazing cattle and impacts performance and welfare by reducing appetite and hindering weight gain. Despite its economic significance, the influence of the abomasal parasite O. ostertagi on the rumen microbiome remains unexplored. We examined the effects of subclinical O. ostertagi infection and vaccination on the rumen microbiome at taxonomic and functional levels. In an experimental trial, calves treated with vaccine or adjuvant-only were orally challenged with O. ostertagi larvae daily for 25 days; 4 groups of animals (UNF: unvaccinated, unchallenged; VAC: vaccinated, challenged; CHE: unvaccinated, challenged, high cumulative faecal egg counts (cFEC), and CLE: unvaccinated, challenged, low cFEC) were selected for whole shotgun metagenomic sequencing. Using a rigorous permutation test based on partial least squares discriminant analyses, we identified 36 (91), 38 (31), 21 (57), 41 (64) and 29 (57) microbial genera (genes) that distinguished VAC, CHE and CLE from UNF, CHE from CLE, and CHE from VAC, respectively. The subclinical infection reshaped the rumen microbiome; enrichment of opportunistic pathogens such as Listeria, and depletion of Filifactor in infected animals were identified as potential biomarkers for host immune response, whereas Actinomyces and Microspora were potential biomarkers of resistance to infection. Microbial biochemical pathways like acetogenesis (e.g., Elusimicrobium, nrfA), pectin and hemicellulose degradation (e.g., Sphaerochaeta), and phosphorus and sulphur metabolism (e.g., Candidatus Accumulibacter and Desulfatibacillum) were also affected by parasitism. Both infection and vaccination altered methanogens, methanotrophs and the methane metabolism pathway, highlighted by distinct gene clustering patterns between infected and uninfected animals. Clustering patterns of infected and vaccinated animals exhibited some similarities, which may reflect immune system modulation of the ruminal microbiome as a result of an abomasal infection. This study unveils critical changes in the rumen microbiome due to the infection by and vaccination against the abomasal parasite O. ostertagi. Our results highlight the importance of monitoring microbial dynamics in the development of effective anthelmintic treatments and vaccines.