Salmonella enterica Serovar Typhimurium Colonizing the Lumen of the Chicken Intestine Grows Slowly and Upregulates a Unique Set of Virulence and Metabolism Genes

Abstract

The pattern of global gene expression in Salmonella enterica serovar Typhimurium bacteria harvested from the chicken intestinal lumen (cecum) was compared with that of a late-log-phase LB broth culture using a whole-genome microarray. Levels of transcription, translation, and cell division in vivo were lower than those in vitro. S. Typhimurium appeared to be using carbon sources, such as propionate, 1,2-propanediol, and ethanolamine, in addition to melibiose and ascorbate, the latter possibly transformed to D-xylulose. Amino acid starvation appeared to be a factor during colonization. Bacteria in the lumen were non-or weakly motile and nonchemotactic but showed upregulation of a number of fimbrial and Salmonella pathogenicity island 3 (SPI-3) and 5 genes, suggesting a close physical association with the host during colonization. S. Typhimurium bacteria harvested from the cecal mucosa showed an expression profile similar to that of bacteria from the intestinal lumen, except that levels of transcription, translation, and cell division were higher and glucose may also have been used as a carbon source.

Bacterial chitinases and chitin-binding proteins as virulence factors

“…The above-described in vitro data are supported by in vivo findings for several pathogens, such as chitinase gene upregulation in Listeria monocytogenes infecting mice intestine (Toledo-Arana et al, 2009) and in S. Typhimurium infecting chicken intestines (Harvey et al, 2011). Similarly, the chitinase from Francisella tularensis, the agent causing tularaemia, has been shown by proteomics to be highly expressed during in vivo infection of mice spleens (Twine et al, 2006).…”

“…Chitin, LacNAc, LacdiNAc Eriksson et al, 2003;Harvey et al, 2011; Hautefort et al, 2008; Larsen et al, 2011 …”

From food to cell: nutrient exploitation strategies of enteropathogens

“…The eut genes of Salmonella enterica sv. Typhimurium are upregulated in the intestine of chicken (Harvey et al, 2011) and an eut mutant is attenuated in macrophages as well as in mice when administered per os, but not intraperitoneally (Stojiljkovic et al, 1995), pointing to the role of ethanolamine utilization during proliferation in the gut. Similar findings were made for L. monocytogenes, which upregulates the eut genes in the intestine of Salmonella enterica sv.…”

“…Recent publications provide indirect and direct experimental evidence for the assumption that the utilization of ethanolamine and/or 1,2-propanediol is linked closely to intestinal proliferation and thus to the virulence of L. monocytogenes, enteropathogenic E. coli (EPEC), Salmonella enterica and Enterococcus faecalis (Becker et al, 2006;Harvey et al, 2011;Kendall et al, 2012;Klumpp & Fuchs, 2007;Maadani et al, 2007;Thiennimitr et al, 2011;Toledo-Arana et al, 2009). Two virulence regulators of Salmonella, CsrA and Fis, are known to control eut and pdu genes, thus further linking these metabolic pathways with infection (Kelly et al, 2004;Lawhon et al, 2003).…”

“…The transverse colonic mucosa contains higher levels of acetate, glutamate, inositols and lactate. Interestingly, a transcriptome profile during infection indicates that bacteria encounter amino acid starvation at the mucosa wall (Harvey et al, 2011).…”