Phage lysis‐lysogeny switches and programmed cell death: Danse macabre

Benler, Sean; Koonin, Eugene V.

doi:10.1002/bies.202000114

Cited by 26 publications

(12 citation statements)

References 127 publications

(182 reference statements)

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“…For example, Ribbon-Helix-Helix (RHH) domains are common in MetJ/Arc-family transcription factors as well as in TAs, suggesting that the bacterial transcription factors of this family were originally derived from antitoxins ( Aravind et al, 2005 ). Given that TAs and other MGEs are activated by various signals, such as DNA damage ( Knowles et al, 2017 ) or the presence of other MGE ( McKitterick and Seed, 2018 ; LeGault et al, 2021 ), recruitment of MGE-encoded transcription factors could be favorable for the host, enabling it to respond to the same stressors ( Benler and Koonin, 2020 ).…”

Section: Mainmentioning

confidence: 99%

Recruitment of Mobile Genetic Elements for Diverse Cellular Functions in Prokaryotes

Benler

Koonin

2022

Front. Mol. Biosci.

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Prokaryotic genomes are replete with mobile genetic elements (MGE) that span a continuum of replication autonomy. On numerous occasions during microbial evolution, diverse MGE lose their autonomy altogether but, rather than being quickly purged from the host genome, assume a new function that benefits the host, rendering the immobilized MGE subject to purifying selection, and resulting in its vertical inheritance. This mini-review highlights the diversity of the repurposed (exapted) MGE as well as the plethora of cellular functions that they perform. The principal contribution of the exaptation of MGE and their components is to the prokaryotic functional systems involved in biological conflicts, and in particular, defense against viruses and other MGE. This evolutionary entanglement between MGE and defense systems appears to stem both from mechanistic similarities and from similar evolutionary predicaments whereby both MGEs and defense systems tend to incur fitness costs to the hosts and thereby evolve mechanisms for survival including horizontal mobility, causing host addiction, and exaptation for functions beneficial to the host. The examples discussed demonstrate that the identity of an MGE, overall mobility and relationship with the host cell (mutualistic, symbiotic, commensal, or parasitic) are all factors that affect exaptation.

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Section: Mainmentioning

confidence: 99%

Recruitment of Mobile Genetic Elements for Diverse Cellular Functions in Prokaryotes

Benler

Koonin

2022

Front. Mol. Biosci.

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“…These population-level phage-defense systems are often grouped together under the umbrella term “abortive infection” (Abi) ( Labrie et al., 2010 ; Lopatina et al., 2020 ) but actually represent diverse mechanisms to prevent phage replication and induce cell death ( Bingham et al., 2000 ; Cohen et al., 2019 ; Fineran et al., 2009 ; Meeske et al., 2019 ; Pecota and Wood, 1996 ; Watson et al., 2019 ). Such mechanistic diversity and the high prevalence of abortive infection systems in nature emphasizes the selective advantage the Abi strategy imparts in the battle against phages ( Benler and Koonin, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Prophages encode phage-defense systems with cognate self-immunity

Owen

Wenner

Dulberger

et al. 2021

Cell Host & Microbe

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Summary Temperate phages are pervasive in bacterial genomes, existing as vertically inherited islands termed prophages. Prophages are vulnerable to predation of their host bacterium by exogenous phages. Here, we identify BstA, a family of prophage-encoded phage-defense proteins in diverse Gram-negative bacteria. BstA localizes to sites of exogenous phage DNA replication and mediates abortive infection, suppressing the competing phage epidemic. During lytic replication, the BstA-encoding prophage is not itself inhibited by BstA due to self-immunity conferred by the anti-BstA ( aba ) element, a short stretch of DNA within the bstA locus. Inhibition of phage replication by distinct BstA proteins from Salmonella , Klebsiella , and Escherichia prophages is generally interchangeable, but each possesses a cognate aba element. The specificity of the aba element ensures that immunity is exclusive to the replicating prophage, preventing exploitation by variant BstA-encoding phages. The BstA protein allows prophages to defend host cells against exogenous phage attack without sacrificing the ability to replicate lytically.

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“…Here, we identify a pair of transcriptional regulators, termed CapH and CapP, that are associated with hundreds of CBASS systems and upregulate CBASS expression in response to DNA damage. DNA damage is a universal stress signal in bacterial cells (Benler & Koonin, 2020), and we show that CapH and CapP are structurally and functionally similar to regulators that mobilize prophages and integrative and conjugative elements (ICE elements), and to activators of the DNA damage response in radiation-resistant Deinococcus species. We also identify CapH and CapP-like regulators associated with a variety of known or putative bacterial immune systems, revealing that these proteins represent a conserved signaling module that regulates defense-system expression in response to DNA damage across bacteria.…”

Section: Introductionmentioning

confidence: 90%

A conserved signaling pathway activates bacterial CBASS immune signaling in response to DNA damage

Lau

Enüstün

et al. 2022

Preprint

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To protect themselves from the constant threat of bacteriophage (phage) infection, bacteria have evolved diverse immune systems including restriction/modification, CRISPR/Cas, and many others. Here we describe the discovery of a two-protein transcriptional regulator module associated with hundreds of CBASS (Cyclic oligonucleotide Based Anti-phage Signaling System) immune systems, and demonstrate that this module drives expression of its associated CBASS system in response to DNA damage. We show that the helix-turn-helix transcriptional repressor CapH binds the promoter region of its associated CBASS system to repress transcription until it is cleaved by the metallopeptidase CapP. CapP is inactive except in the presence of single-stranded DNA, and CapP activity in cells is stimulated by DNA-damaging drugs. Together, CapH and CapP drive increased expression of their associated CBASS system in response to DNA damage. In both their structures and mechanisms, CapH and CapP resemble regulators that drive increased expression of DNA damage response genes in radiation-resistant Deinococcus, and control the mobilization of prophages and mobile elements in response to DNA damage. We also identify CapH and CapP-related proteins associated with diverse known and putative bacterial immune systems, including DISARM and two uncharacterized operons encoding proteins related to eukaryotic ubiquitin signaling pathways. Overall, our data highlight a mechanism by which bacterial immune systems can sense and respond to a universal stress signal, potentially enabling multiple immune systems to mount a coordinated defensive effort against an invading pathogen.

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Phage lysis‐lysogeny switches and programmed cell death: Danse macabre

Cited by 26 publications

References 127 publications

Recruitment of Mobile Genetic Elements for Diverse Cellular Functions in Prokaryotes

Recruitment of Mobile Genetic Elements for Diverse Cellular Functions in Prokaryotes

Prophages encode phage-defense systems with cognate self-immunity

A conserved signaling pathway activates bacterial CBASS immune signaling in response to DNA damage

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