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Infection and Immunity, November 2007, p. 5191-5199, Vol. 75, No. 11
0019-9567/07/$08.00+0     doi:10.1128/IAI.00784-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Systemic Translocation of Salmonella enterica Serovar Dublin in Cattle Occurs Predominantly via Efferent Lymphatics in a Cell-Free Niche and Requires Type III Secretion System 1 (T3SS-1) but Not T3SS-2

Gillian D. Pullinger,¹ Susan M. Paulin,^1, Bryan Charleston,² Patricia R. Watson,^1, Alison J. Bowen,¹ Francis Dziva,¹ Eirwen Morgan,¹ Bernardo Villarreal-Ramos,² Timothy S. Wallis,^1, and Mark P. Stevens^1*

Divisions of Microbiology,¹ Immunology, Institute for Animal Health, Compton, Berkshire RG20 7NN, United Kingdom²

Received 8 June 2007/ Returned for modification 13 July 2007/ Accepted 14 August 2007

Salmonella enterica is an important diarrheal pathogen, and infections may involve severe systemic sequelae depending on serovar- and host-specific factors. The molecular mechanisms underlying translocation of host-restricted and -specific serovars of S. enterica from the intestines to distal organs are ill defined. By surgical cannulation of lymph and blood vessels draining the distal ileum in cattle, S. enterica serovar Dublin was observed to translocate predominantly via mesenteric lymph nodes to efferent lymphatics in a manner that correlates with systemic virulence, since the fowl typhoid-associated serovar Gallinarum translocated at a significantly lower level. While both S. enterica serovars Dublin and Gallinarum were intracellular while in the intestinal mucosa and associated with major histocompatibility complex class II-positive cells, the bacteria were predominantly extracellular within efferent lymph. Screening of a library of signature-tagged serovar Dublin mutants following oral inoculation of calves defined the role of 36 virulence-associated loci in enteric and systemic phases of infection. The number and proportion of tagged clones reaching the liver and spleen early after oral infection were identical to the values in efferent lymph, implying that this may be a relevant mode of dissemination. Coinfection studies confirmed that lymphatic translocation requires the function of type III secretion system 1 (T3SS-1) but, remarkably, not T3SS-2. This is the first description of the mode and genetics of systemic translocation of serovar Dublin in its natural host.

Published ahead of print on 27 August 2007.

Editor: J. B. Bliska

Present address: Institute of Environmental Science and Research Limited, Christchurch Science Centre, 27 Creyke Road, Ilam, P.O. Box 29 181, Christchurch, New Zealand.

Present address: Ridgeway Biologicals Ltd., c/o Institute for Animal Health, Compton, Berkshire RG20 7NN, United Kingdom.