Type II secretion in Yersinia—a secretion system for pathogenicity and environmental fitness

Abstract

In Yersinia species, type III secretion (T3S) is the most prominent and best studied secretion system and a hallmark for the infection process of pathogenic Yersinia species. Type II secretion (T2S), on the other hand, is less well-characterized, although all Yersinia species, pathogenic as well as non-pathogenic, possess one or even two T2S systems. The only Yersinia strain in which T2S has so far been studied is the human pathogenic strain Y. enterocolitica 1b. Mouse infection experiments showed that at least one of the two T2S systems of Y. enterocolitica 1b, termed Yts1, is involved in dissemination and colonization of deeper tissues like liver and spleen. Interestingly, in vitro studies revealed a complex regulation of the Yts1 system, which is mainly active at low temperatures and high Mg2+-levels. Furthermore, the functional characterization of the proteins secreted in vitro indicates a role of the Yts1 machinery in survival of the bacteria in an environmental habitat. In silico analyses identified Yts1 homologous systems in bacteria that are known as plant symbionts or plant pathogens. Thus, the recent studies point to a dual function of the Yts1 T2S systems, playing a role in virulence of humans and animals, as well as in the survival of the bacteria outside of the mammalian host. In contrast, the role of the second T2S system, Yts2, remains ill defined. Whereas the T3S system and its virulence-mediating role has been intensively studied, it might now be time to also focus on the T2S system and its role in the Yersinia lifestyle, especially considering that most of the Yersinia isolates are not found in infected humans but have been gathered from various environmental samples.

Txc, a New Type II Secretion System of Pseudomonas aeruginosa Strain PA7, Is Regulated by the TtsS/TtsR Two-Component System and Directs Specific Secretion of the CbpE Chitin-Binding Protein

“…In support of this assumption, homologs of PSPA7_1418 have been recovered in other T2SSs involved in chitin-binding secretion. This is the case for the two other Pseudomonas Txc systems, found in P. fluorescens (52) and P. putida (51), but also for the Yts1 T2SS of Y. enterocolitica (22). In conclusion, we propose that, when possible, compatible T2SS-secreted exoproteins are exported by using the same general machine.…”

“…Our data revealed that this Txc T2SS, its unorthodox sensor TtsS, and the secreted protein CbpE are all encoded by a region of genome plasticity unique to this strain. While the Txc T2SS is limited to PA7 among P. aeruginosa strains, similar txc-cbpE clusters have been recovered from other members of the Pseudomonas genus, such as P. putida strain ND6 (51) and P. fluorescens strain F113 (52). However, and in contrast to what was mentioned previously by Redondo-Nieto et al (52), the txc cluster of P. fluorescens strain F113 is not a "second xcp cluster" but a new T2SS cluster, as we demonstrate in this study.…”

Transcriptomic Analysis of Yersinia enterocolitica Biovar 1B Infecting Murine Macrophages Reveals New Mechanisms of Extracellular and Intracellular Survival

“…Strain GY4478 (JB580 pYVϪ) (27) was used as the parent strain for making insertion mutants of the Yts2 T2SS and Tad pilus in order to prevent the rapid killing of host cells by the Ysc T3SS. Plasmid pEP185.2 (24) was inserted into genes thought to be critical to the function of the Yts2 T2SS and Tad pilus (28)(29)(30), essentially as previously described (31). Briefly, 300-to 500-bp fragments of the genes yts2D (primer pair yts2D-F [5=-TCT AGA CCT ATA GTA GGA TAT GCG GAG AAC-3=] and yts2D-R [5=-TCT AGA CTG GCG TAG TAA CGG AGC-3=]) and tadA (primer pair tadA-F [5=-TCT AGA GCT CGC CAG TAT TGA TAT AGA TC-3=] and tadA-R [5=-TCT AGA CGT CCA ATG CAA TAG GGC-3=]) were PCR amplified and cloned into pCR-BluntII-TOPO (Life Technologies).…”

“…Three secreted effectors of the Yts1 system have been described, encoded by the genes chiY, engY, and YE3650 -each of which encodes a protein with the characteristic N-terminal signal sequence for T2S (29). Interestingly, the upstream regulator PclR (PypC-like regulator) appears to play a role in the expression of chiY but not of the genes directly downstream, which encode the structural apparatus of the Yts1 T2SS (29,30).…”

“…This system is common to all species of Yersinia pathogenic to humans; however, expression of the system has never been observed under any in vitro condition, and no secreted effectors have been found (29,30). Unlike the Yts1 system, the upstream regulator of the Yts2 system, PypC, directly regulates the downstream genes encoding the T2S apparatus (29).…”