Recto-anal junction (RAJ) fecal microbiomes of cattle experimentally challenged with Escherichia coli O157:H7

Authors: MIR, RAIES - Orise Fellow; SCHAUT, ROBERT - Orise Fellow; Looft, Torey; Allen, Heather; Sharma, Vijay; Kudva, Indira

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/25/2020
Publication Date: 4/17/2020
Citation: Mir, R., Schaut, R.G., Looft, T.P., Allen, H.K., Sharma, V.K., Kudva, I.T. 2020. Recto-anal junction (RAJ) fecal microbiomes of cattle experimentally challenged with Escherichia coli O157:H7. Frontiers in Microbiology. 11:693. https://doi.org/10.3389/fmicb.2020.00693.
DOI: https://doi.org/10.3389/fmicb.2020.00693

Interpretive Summary: Cattle are the main ruminant reservoirs of Escherichia coli O157:H7 (O157), a food-borne human pathogen. In cattle, O157 preferentially colonizes the recto-anal junction (RAJ) found at the distal end of the intestinal tract but causes no disease in these animals. The diverse resident microbes (microbiota) normally found at the RAJ could impact or be impacted by O157, thus influencing colonization of the site. To get a better understanding of O157 interaction with the RAJ microbiota, we compared changes in the bovine RAJ and fecal microbiota in animals experimentally inoculated with O157. The presence of O157 caused subtle changes in the abundance of different bacteria comprising the RAJ microbiota suggesting that the RAJ microbial community could be transiently impacted by O157 colonization. These results provide insights into the colonization dynamics of this foodborne pathogen and may aid in development of better strategies to reduce O157 in cattle.

Technical Abstract: Cattle are the asymptomatic reservoirs of Escherichia coli O157:H7 (O157) that preferentially colonizes the bovine recto-anal junction (RAJ). Understanding O157 influences on the diversity of the RAJ microbiota could give insights into O157 persistence at RAJ in cattle. Hence, we compared changes in bovine fecal and RAJ microbiota due to O157 challenge under experimental conditions. Cattle were either orally challenged (n equals 4) with 10 to the power of 10 CFU of a streptomycin-resistant O157 strain 86-24, or mock-challenged (n equals 4). Feces and RAJ mucosal swab (RAMS) samples were collected at different time points for culture and microbiota analysis. Overall, alpha diversity measures (Chao1 species richness and Shannon diversity index) were significantly different between fecal and RAMS samples but were not influenced by O157 challenge. The Firmicutes to Bacteroidetes (F: B) ratio was higher in RAMS samples from O157 colonized animals that may have influenced consistent yet decreased O157 colonization at the RAJ. Specific bacterial genera in fecal and RAMS microbiota, with low relative abundance, were associated with O157 colonization but this association did not affect the overall microbial diversity. Differential abundance analysis of genera in samples collected from cattle shedding O157 indicated significantly higher relative abundance of Tyzzerella in fecal samples, and Paenibacillus and Fusobacterium in RAMS samples. Non-shedding cattle showed higher relative abundance of Succinivibriio, and Prevotella 1 in fecal samples, and Intestinimonas and Citrobacter in RAMS samples. These results suggested transient interactions between O157 and the intestinal microbial community that might permit or interfere with O157 colonization in a site-specific manner. Importance This study explored changes in fecal and bovine RAJ microbiota, over time, before and after experimental challenge of cattle with O157. Understanding reciprocal influences or lack-thereof between O157 and the gut microbiota composition in cattle might provide insights into colonization dynamics of this foodborne pathogen and facilitate development of strategies effective in reducing natural O157 colonization in cattle.