Eimeria maxima-induced transcriptional changes in the cecal mucosa of broiler chickens

Authors: Li, Charles; Yan, Xianghe; Lillehoj, Hyun; GU, CHANGQIN - Huazhong Agricultural University; SUN, ZHIFENG - US Department Of Agriculture (USDA); OH, SUNGTAEK - US Department Of Agriculture (USDA); LEE, YOUNGSUB - US Department Of Agriculture (USDA); XIANYU, ZHEZI - University Of Delaware; ZHAO, HONGYAN - Yangzhou University; LIU, LIHENG - Jiangxi Agricultural University

Submitted to: Parasites & Vectors
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/27/2019
Publication Date: 6/4/2019
Citation: Li, C.Z., Yan, X., Lillehoj, H.S., Gu, C., Sun, Z., Oh, S., Lee, Y., Xianyu, Z., Zhao, H., Liu, L. 2019. Eimeria maxima-induced transcriptional changes in the cecal mucosa of broiler chickens. Parasites & Vectors. https://doi.org/10.1186/s13071-019-3534-4.
DOI: https://doi.org/10.1186/s13071-019-3534-4

Interpretive Summary: The increasing cost in control of infectious diseases is one of the big challenges that the global poultry food industry is facing. One of the top priority enteric diseases in poultry is coccidiosis. It is caused by a mixture of intestinal parasites called Eimeria, which damages the bird's intestinal barrier, results in underperformance of poultry growth and impacts animal welfare, with estimated economic loss of $3 billion annually worldwide. These parasites also are the most important inducing factor for another critical enteric infectious disease called necrotic enteritis, which has increased significantly in parallel with the reduction/withdrawal of growth promoting antibiotics from feed in response to government regulation and public concern over appearance of the antibiotic resistant bacteria. Lack of a full understanding of molecular mechanisms on chicken host-parasite interaction limits the development of effective control measurement. In order to effectively control coccidiosis, the disease-causing mechanism of parasitic pathogens needs to be elucidated. Genetic material known as mRNA was extracted from the intestine mucosa of chickens with coccidiosis infections, sequenced using advanced RNA sequencing (RNA-seq) and analyzed to evaluate gene profiles after parasite infections. RNA-seq analysis revealed that 27 genes were significantly up-regulated while 43 genes were significantly down-regulated. These genes were associated with immune-related gene families. In addition, parasitic infection resulted in a significant increase of single nucleotide changes with different forms or appearances of small insertions and deletions in the chicken genes. Furthermore, 10 novel genes were also found. Broad gene categories represented by highly differentiated host genes suggest enrichments for immune responses and tissue healing functions. Analysis of data revealed several potential molecular regulations and suggests novel putative immune components. These findings will enhance our understanding of chicken-parasite interaction in parasitic diseases that will facilitate the development of logical strategies for improvement of chicken immunity and disease control.

Technical Abstract: Apicomplexan protozoans of Eimeria spp. cause coccidiosis, one of the most economically relevant parasitic diseases in chickens. The lack of a complete understanding of molecular mechanisms in host-parasite interaction limits the development of effective control measures. In the present study, RNA sequencing (RNA-seq) was applied to investigate the host mRNA profiles of the cecal mucosa and its contents collected at day 5 post Eimeria maxima (EM) infection. Total RNA from the cecal samples of uninfected naïve control and EM groups was used to make libraries, generating 329,513,738 and 293,188,542 usable reads, which were assembled into a total of 825,238 high-quality unigenes (transcripts) in Trinity software. RNA-seq analysis of cecal samples in the two groups revealed 643 up-regulated and 774 down-regulated genes (|fold change|> 1.0, p = 0.050), including several significant immune-related gene families, such as immunoglobulin C1-set, major histocompatibility complex (MHC) class I alpha chain, and immunoglobulin subtype genes. In addition, a total of 160 cluster of differentiation (CD) molecular genes and 10 novel genes were found. The broad gene categories represented by the highly differentiated host genes suggested enrichment in immune response and tissue healing functions. The completeness of the assembled transcriptome was further assessed using the Kyoto Encyclopedia of Genes and Genomes (KEGG) database, Gene Ontology, eggNOG and CAZy for gene annotation. Pathway analysis revealed regulation of several potential pathways and the involvement of novel putative immune components, such as the TGF-ß signaling pathway and cell adhesion molecules, in coccidiosis. These findings provide information on host-parasite interaction that enhances knowledge of avian coccidiosis and may facilitate the development of strategies to manipulate host genetic and immune potential. Keywords: Eimeria maxima, host, ceca, RNA-seq, Chicken, transcription.