Differential Cellular Response to Translocated Toxic Effectors and Physical Penetration by the Type VI Secretion System

Kamal, Fatima; Liang, Xiaoye; Manera, Kevin; Pei, Tong‐Tong; Kim, Haeun; Lam, Linh; Pun, Alexander; Hersch, Steven J.; Dong, Tao

doi:10.1016/j.celrep.2020.107766

Cited by 57 publications

(82 citation statements)

References 60 publications

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“…Most recently, an elegant study by Kamal et al (55) showed that a single effector of V. cholerae (TseL) was necessary and sufficient for generating activation of the H1-T6SS of P. aeruginosa through the classical tit-for-tat interaction with T6SS + V. cholerae. Ectopic expression of tseL in the periplasm of P. aeruginosa (but not in the cytosol) could also trigger T6SS assembly in a TagQRST-dependent fashion (55). Given that TseL is a lipase and that lipases are very common effectors of T6SSs (8,94,95), it is possible that a signal generated by phospholipid hydrolysis within the periplasm is recognized by part of the P. aeruginosa TagQRST sensory transduction system.…”

Section: Discussionmentioning

confidence: 99%

“…Chemical substances that interact with gram-negative lipopolysaccharides (LPSs), including polymyxin B (43), DNA, and chelators (54), can also activate the H1-T6SS of P. aeruginosa (again dependent on the TagQRST-PpkA-FhA1-PppA system) and these outer membrane perturbants can trigger rapid (i.e., under 1 min) assembly and firing of the H1-T6SS apparatus. Finally, the V. cholerae lipase TseL (47) has been reported to be necessary and sufficient to induce the tit-for-tat response by P. aeruginosa (55), suggesting that enzymic attack of membrane phospholipids may also trigger the TagQRST-PpkA-FhA1-PppA pathway of H1-T6SS assembly and firing.…”

Section: Significancementioning

confidence: 99%

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Endogenous membrane stress induces T6SS activity in Pseudomonas aeruginosa

Stolle

Meader

Toska

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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The type 6 secretion system (T6SS) is a dynamic organelle encoded by many gram-negative bacteria that can be used to kill competing bacterial prey species in densely occupied niches. Some predatory species, such asVibrio cholerae, use their T6SS in an untargeted fashion while in contrast,Pseudomonas aeruginosaassembles and fires its T6SS apparatus only after detecting initial attacks by other bacterial prey cells; this targeted attack strategy has been termed the T6SS tit-for-tat response. Molecules that interact with theP. aeruginosaouter membrane such as polymyxin B can also trigger assembly of T6SS organelles via a signal transduction pathway that involves protein phosphorylation. Recent work suggests that a phospholipase T6SS effector (TseL) ofV. choleraecan induce T6SS dynamic activity inP. aeruginosawhen delivered to or expressed in the periplasmic space of this organism. Here, we report that inhibiting expression of essential genes involved in outer membrane biogenesis can also trigger T6SS activation inP. aeruginosa. Specifically, we developed a CRISPR interference (CRISPRi) system to knock down expression ofbamA,tolB, andlptDand found that these knockdowns activated T6SS activity. This increase in T6SS activity was dependent on the same signal transduction pathway that was previously shown to be required for the tit-for-tat response. We conclude that outer membrane perturbation can be sensed byP. aeruginosato activate the T6SS even when the disruption is generated by aberrant cell envelope biogenesis.

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Section: Discussionmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

Endogenous membrane stress induces T6SS activity in Pseudomonas aeruginosa

Stolle

Meader

Toska

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…Although the molecular regulation of retaliatory T6SS firing has received attention 27 , 28 , 30 , 34 , its evolution has not—leaving open the question of why such a complex strategy has evolved in bacteria, and only in some species. At a broader level, while the evolution of reciprocation has a long history of study in evolutionary biology 35 – 38 , past efforts have focused largely on the evolution of reciprocal cooperation, rather than competition.…”

Section: Introductionmentioning

confidence: 99%

“…So far, it has been shown that various stimuli can trigger counterattacks in P. aeruginosa strain PAO1, including incoming T6SS attacks from multiple bacterial species 23,27,28 , conjugative T4SS pili 29 , and membrane-disrupting antibiotics like polymyxin B 29 . There is also evidence that retaliation can be toxin-specific-not all T6SS effectors trigger counterattacks, and in V. cholerae, only the lipase effector TseL triggers retaliation 30 . Across stimuli, P. aeruginosa appears to be responding to membrane perturbation, and a putative model is that this response is mediated post-transcriptionally via the TagQRST pathway.…”

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confidence: 99%

The evolution of tit-for-tat in bacteria via the type VI secretion system

et al. 2020

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Tit-for-tat is a familiar principle from animal behavior: individuals respond in kind to being helped or harmed by others. Remarkably some bacteria appear to display tit-for-tat behavior, but how this evolved is not understood. Here we combine evolutionary game theory with agent-based modelling of bacterial tit-for-tat, whereby cells stab rivals with poisoned needles (the type VI secretion system) after being stabbed themselves. Our modelling shows tit-for-tat retaliation is a surprisingly poor evolutionary strategy, because tit-for-tat cells lack the first-strike advantage of preemptive attackers. However, if cells retaliate strongly and fire back multiple times, we find that reciprocation is highly effective. We test our predictions by competing Pseudomonas aeruginosa (a tit-for-tat species) with Vibrio cholerae (random-firing), revealing that P. aeruginosa does indeed fire multiple times per incoming attack. Our work suggests bacterial competition has led to a particular form of reciprocation, where the principle is that of strong retaliation, or ‘tits-for-tat’.

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“…Membrane damage from an incoming conjugative pilus or polymyxin B can likewise trigger this response [7]. A specific toxin effector from a competitor T6SS has also been shown to activate the T6SS [8] in a manner reminiscent of colicin activation by the SOS response following colicin-mediated DNA damage (Fig 1). Additional signals from quorum sensing and nutrient availability are also integrated into these control mechanisms [9].…”

mentioning

confidence: 99%