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Pathogenic  Yersinia  have a pronounced tropism for lymphatic tissues and harbor a virulence plasmid that encodes a type III secretion system, pTTSS, that transports Yops into host cells. Yops are critical virulence factors that prevent phagocytosis by macrophages and neutrophils and  Yersinia  mutants lacking one or more Yops are defective for survival in lymphatic tissues, liver, and gastrointestinal tract. However, here we demonstrate that  Y. pseudotuberculosis (Yptb)  mutants lacking the pTTSS survived as well as or better than wild-type (WT)  Yptb  in the mesenteric lymph nodes (MLN). Infection with pTTSS mutants caused lymphadenitis with little necrosis, whereas infection with WT  Yptb  provoked lymphadenitis with multiple necrotic suppurative foci. Gentamicin protection assays and microscopic examination of the MLN revealed that pTTSS mutants resided extracellularly adjacent to B and T lymphocytes in the cortex and paracortex. WT  Yptb  was found extracellularly adjacent to neutrophils and macrophages in necrotic areas and adjacent to B and T lymphocytes in less-inflamed areas. To determine whether lymphocytes protected pTTSS mutants from phagocytic cells,  Rag1 −/−   mice were infected with pTTSS mutants or WT  Yptb . pTTSS mutants but not WT, were impaired for survival in MLN of  Rag1 −/−   mice, suggesting that lymphocyte-rich regions constitute a protective niche for pTTSS mutants. Finally, we show that invasin and the chromosomally encoded TTSS were not required for  Yptb  survival in MLN. In summary, chromosomally encoded factors are sufficient for  Yptb  replication in the cortex and paracortex of MLN; the pTTSS enables  Yersinia  to survive within phagocyte-rich areas of lymph nodes, and spread to other tissues.

Yersinia Has a Tropism for B and T Cell Zones of Lymph Nodes That Is Independent of the Type III Secretion System