The Contribution of Eimeria Coinfection and Intestinal Inflammation to Cecal Colonization and Systemic Spread of Salmonella Typhimurium Deficient in Tetrathionate Reductase or Type III Secretion Systems Salmonella Pathogenicity Island 1 or 2

Abstract

Intestinal inflammation may provide a growth advantage for <i>Salmonella</i> and enhance its systemic spread in chickens. <i>Salmonella</i> triggers intestinal inflammation in the host by using type III secretion systems (T3SS) and produces the inflammatory end product tetrathionate. In mice, tetrathionate respiration confers a growth advantage for <i>Salmonella</i> Typhimurium over the competitive microbiome in the inflamed intestine. Coccidia also promote intestinal inflammation and enhance <i>Salmonella</i> intestinal growth and systemic spread in chickens. The objective of this study was to evaluate the contribution of inflammation, induced by <i>Eimeria</i> spp. or <i>Salmonella</i> Typhimurium, to <i>Salmonella</i> colonization and dissemination in chickens. In addition, the fitness costs associated with defects in tetrathionate reductase and T3SS associated with <i>Salmonella</i> Pathogenicity Island 1 or 2 (SPI-1 or SPI-2) were evaluated in <i>in vivo</i> competition experiments with wild-type <i>Salmonella</i> strain, with or without <i>Eimeria</i> coinfection. One-day-old specific-pathogen-free chickens were orally inoculated with a sham inoculum or with 4 × 10²<i>Eimeria</i> oocysts cocktail of <i>Eimeria tenella</i>, <i>Eimeria acervulina</i>, <i>Eimeria maxima</i>, and <i>Eimeria mitis</i>. At 6 days of age, birds were orally administered a 1:1 ratio of <i>Salmonella</i> Typhimurium wild-type and mutant deficient in tetrathionate reductase, SPI-1, or SPI-2 (10⁸ colony forming units/bird). Ceca, livers, and drumsticks were collected at 3, 7, 14, and 42 days after <i>Salmonella</i> infection, for bacteriology. Intestinal inflammation was scored by histology. Significantly higher intestinal inflammation was observed in challenge groups compared with the control. However, there were no significant differences in intestinal inflammation scores between groups coinfected with both <i>Eimeria</i> spp. and <i>Salmonella</i> Typhimurium and birds infected with <i>Salmonella</i> alone, and <i>Eimeria</i> coinfection did not increase <i>Salmonella</i> prevalence or abundance. Contrary to mouse studies, tetrathionate reductase did not enhance <i>Salmonella</i> Typhimurium cecal colonization or systemic spread in chickens. SPI-1 and SPI-2 played a significant role in <i>Salmonella</i> dissemination and cecal colonization in chickens, respectively.