Relationship Between Quorum Sensing and Secretion Systems

Abstract

Quorum sensing (QS) is a communication mechanism between bacteria that allows specific processes to be controlled, such as biofilm formation, virulence factor expression, production of secondary metabolites and stress adaptation mechanisms such as bacterial competition systems including secretion systems (SS). These SS have an important role in bacterial communication. SS are ubiquitous; they are present in both Gram-negative and Gram-positive bacteria and in Mycobacterium sp. To date, 8 types of SS have been described (T1SS, T2SS, T3SS, T4SS, T5SS, T6SS, T7SS, and T9SS). They have global functions such as the transport of proteases, lipases, adhesins, heme-binding proteins, and amidases, and specific functions such as the synthesis of proteins in host cells, adaptation to the environment, the secretion of effectors to establish an infectious niche, transfer, absorption and release of DNA, translocation of effector proteins or DNA and autotransporter secretion. All of these functions can contribute to virulence and pathogenesis. In this review, we describe the known types of SS and discuss the ones that have been shown to be regulated by QS. Due to the large amount of information about this topic in some pathogens, we focus mainly on Pseudomonas aeruginosa and Vibrio spp.

Keywords: competence; motility; quorum; secretion; virulence.

FIGURE 1

Structure of secretion systems. Schematic representation of secretory systems: type I (T1SS), type II (T2SS), type V (T5SS), type IX (T9SS), type III (T3SS), type IV (T4SS), type VI (T6SS), and type VII (T7SS). The type I pathway is exemplified by hemolysin A (HlyA) secretion in E. coli where TolC, HlyD, and HlyB are the three components which constitute the channel to transport HlyA to extracellular space. Sec (general secretion route) and Tat (twin-arginine translocation pathway) transfer the substrates of T2SS and T5SS across the inner membrane. Sec also participates in the transport of T9SS substrates across de inner membrane. T9SS is also called Por Secretion System (PoSS). T4SS is represented by VirB/D system of Agrobacterium tumefaciens. The T7SS is based on a system in Mycobacteria. Red squares represent the ATPases. HM, host membrane; EM, extracellular medium; OM, outer membrane; IM, inner membrane; MM, mycomembrane. Substrates secreted by each secretory system are included in a circle in the top of the figure. Adapted from Tseng et al. (2009).

FIGURE 2

Secretion systems and QS network elements. The figure shows the relationship between QS networks and expression of secretion systems (blue squares). The genes regulated by QS are in purple boxes. Each QS network is represented by a different color. Starting at the top right of the figure: The swr QS system of S. liquefaciens controls the lipB genes of the T1SS (orange); Ax21 (QS effector) and QS system Rax regulate RaxABC TOSS (T1SS) in gram negative bacteria (ochre); QS (RhlIR and LasIR) regulates expression of T2SS, T3SS, and T6SS in P. aeruginosa (brown); VqsM (an AraC family transcription factor) interacts with the LasIR and ExsA promoters (a master regulator of T3SS) in P. aeruginosa (dark orange); T2SS is regulated by LuxS/LuxI/AI-2 QS in E. coli and indole production by TnA (tryptophanase) regulates esp genes expression (T2SS) in this bacterium (blue); in Yersinia sp. the Hfq chaperone is connected with QS (AI-2) and regulates the Yop-Ysc type III secretion system (T3SS) (green); in Xanthomonas sp. T2SS and T3SS are regulated by DSF (diffusible signal factor) which is a quorum sensing signal (yellow); T4SS (virB operon) is regulated by VjbR (LuxR like protein) and LuxI in Brucella (turquoise) and Roseobacter (pink), respectively; a connection between Acinetobacter baumanii QS (AbaI/AbaR, controlled by bile salts) and T6SS has been established (maroon); in Vibrio sp. there is a complex network which relates QS (LuxO/HapR/TfoX) with T6SS (aquamarine); AhyRI (a QS network) in Aeromonas sp. and P. atrosepticum is involved in Hcp and VgrG secretion (sky blue) and finally, iron is transported across the cell membrane accompanied by PQS, a quorum sensing signal in P. aeruginosa, and this process depend on Tse a substrate of T6SS, which binds to OMVs (outer membrane vesicles) containing PQS- Fe³⁺.