Virulence potential of five major pathogenicity islands (SPI-1 to SPI-5) of Salmonella enterica serovar Enteritidis for chickens

Abstract

BackgroundSalmonella is a highly successful parasite of reptiles, birds and mammals. Its ability to infect and colonise such a broad range of hosts coincided with the introduction of new genetic determinants, among them 5 major pathogenicity islands (SPI1-5), into the Salmonella genome. However, only limited information is available on how each of these pathogenicity islands influences the ability of Salmonella to infect chickens. In this study, we therefore constructed Salmonella Enteritidis mutants with each SPI deleted separately, with single individual SPIs (i.e. with the remaining four deleted) and a mutant with all 5 SPIs deleted, and assessed their virulence in one-day-old chickens, together with the innate immune response of this host.ResultsThe mutant lacking all 5 major SPIs was still capable of colonising the caecum while colonisation of the liver and spleen was dependent on the presence of both SPI-1 and SPI-2. In contrast, the absence of SPI-3, SPI-4 or SPI-5 individually did not influence virulence of S. Enteritidis for chickens, but collectively they contributed to the colonisation of the spleen. Proinflammatory signalling and heterophil infiltration was dependent on intact SPI-1 only and not on other SPIs.ConclusionsSPI-1 and SPI-2 are the two most important pathogenicity islands of Salmonella Enteritidis required for the colonisation of systemic sites in chickens.

Salmonella enterica subspecies enterica serovar Enteritidis Salmonella pathogenicity island 2 type III secretion system: role in intestinal colonization of chickens and systemic spread

“…Their study indicates the importance of both SPI-1 and SPI-2 in colonization of the liver and spleen, but also shows that although at much lower levels than the wild-type, mutants lacking one or both of SPI-1 and SPI-2 can still be isolated from the liver and spleen, further confirming our results. They found no difference in caecal colonization by any of their strains, in accordance with our results (Rychlik et al, 2009).…”

“…However, very recent work by Rychlik and co-workers, published after completion of our animal trials, describes the complete knockout of all the SPI regions (together and separately), and their effect on colonization of 1-day-old chicks (Rychlik et al, 2009). Also, at least partial deletions of SPI-2 have been produced in S. Typhimurium, as well as full deletions of SPI-1 ( Colonization of the liver and spleen of challenged birds was often quite low; therefore, portions of the liver and spleen were enriched in selenite broth to increase detection sensitivity.…”

“…The recent study by Rychlik et al (2009) used S. Enteritidis strain 147 SPI mutants lacking one of the islands (SPI-1 to -5), lacking both SPI-1 and SPI-2, lacking all islands (SPI-1 to -5), retaining one of the islands only (SPI-1 to -5), or retaining SPI-1 and SPI-2 only. They tested the ability of these mutants (compared with the wild-type strain) to colonize the liver and spleen of 1-day-old chicks.…”

Cell invasion of poultry-associated Salmonella enterica serovar Enteritidis isolates is associated with pathogenicity, motility and proteins secreted by the type III secretion system

“…Previous studies have also revealed that genes encoded by SPI-1 TTSS are involved in intestinal invasion whereas genes encoded on SPI-2 are required for systemic infection and survival within macrophages (Desin et al, 2009;Dieye et al, 2009;Jones et al, 2007;Li et al, 2009;Rychlík et al, 2009;Wisner et al, 2010). Mutations in the genes encoding secretory effector proteins or genes that regulate their expression lead to virulence attenuation in S. Enteritidis (Amy et al, 2004;Fardini et al, 2007;Parker & GuardPetter, 2001).…”

Experimental infection of chickens by a flagellated motile strain of Salmonella enterica serovar Gallinarum biovar Gallinarum

“…Salmonella flagella activate Toll-like receptor (TLR)-5 on enterocyte surfaces (Iqbal et al, 2005;Subramanian and Qadri, 2006) triggering a cascade of cellular events, which lead to the secretion of cytokines and chemokines responsible for stimulating innate and adaptive immunity, mainly through activation of dendritic and T cells (McSorley et al, 2002;Iqbal et al, 2005;Salazar-Gonzalez and McSorley, 2005).…”