The bacterial defense system MADS interacts with CRISPR-Cas to limit phage infection and escape

Alice Maestri; Benoit J Pons; Elizabeth Pursey; Charlotte E Chong; Sylvain Gandon; Rafael Custodio; Anna Olina; Aleksei Agapov; Matthew A W Chisnall; Anita Grasso; Steve Paterson; Mark D Szczelkun; Kate S Baker; Stineke van Houte; Anne Chevallereau; Edze R Westra

doi:10.1016/j.chom.2024.07.005

The bacterial defense system MADS interacts with CRISPR-Cas to limit phage infection and escape

Alice Maestri, Benoit J Pons, Elizabeth Pursey, Charlotte E Chong, Sylvain Gandon, Rafael Custodio, Anna Olina, Aleksei Agapov, Matthew A W Chisnall, Anita Grasso, Steve Paterson, Mark D Szczelkun, Kate S Baker, Stineke van Houte, Anne Chevallereau^*, Edze R Westra^*

^*Corresponding author for this work

School of Biochemistry

Research output: Contribution to journal › Article (Academic Journal) › peer-review

Abstract

The constant arms race between bacteria and their parasites has resulted in a large diversity of bacterial defenses, with many bacteria carrying multiple systems. Here, we report the discovery of a phylogenetically widespread defense system, coined methylation-associated defense system (MADS), which is distributed across gram-positive and gram-negative bacteria. MADS interacts with a CRISPR-Cas system in its native host to provide robust and durable resistance against phages. While phages can acquire epigenetic-mediated resistance against MADS, co-existence of MADS and a CRISPR-Cas system limits escape emergence. MADS comprises eight genes with predicted nuclease, ATPase, kinase, and methyltransferase domains, most of which are essential for either self/non-self discrimination, DNA restriction, or both. The complex genetic architecture of MADS and MADS-like systems, relative to other prokaryotic defenses, points toward highly elaborate mechanisms of sensing infections, defense activation, and/or interference.

Original language	English
Pages (from-to)	1412-1426
Number of pages	15
Journal	Cell Host & Microbe
Volume	32
Issue number	8
Early online date	1 Aug 2024
DOIs	https://doi.org/10.1016/j.chom.2024.07.005
Publication status	Published - 14 Aug 2024

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© 2024 The Authors.

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Maestri, A., Pons, B. J., Pursey, E., Chong, C. E., Gandon, S., Custodio, R., Olina, A., Agapov, A., Chisnall, M. A. W., Grasso, A., Paterson, S., Szczelkun, M. D., Baker, K. S., van Houte, S., Chevallereau, A., & Westra, E. R. (2024). The bacterial defense system MADS interacts with CRISPR-Cas to limit phage infection and escape. Cell Host & Microbe, 32(8), 1412-1426. https://doi.org/10.1016/j.chom.2024.07.005

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title = "The bacterial defense system MADS interacts with CRISPR-Cas to limit phage infection and escape",

abstract = "The constant arms race between bacteria and their parasites has resulted in a large diversity of bacterial defenses, with many bacteria carrying multiple systems. Here, we report the discovery of a phylogenetically widespread defense system, coined methylation-associated defense system (MADS), which is distributed across gram-positive and gram-negative bacteria. MADS interacts with a CRISPR-Cas system in its native host to provide robust and durable resistance against phages. While phages can acquire epigenetic-mediated resistance against MADS, co-existence of MADS and a CRISPR-Cas system limits escape emergence. MADS comprises eight genes with predicted nuclease, ATPase, kinase, and methyltransferase domains, most of which are essential for either self/non-self discrimination, DNA restriction, or both. The complex genetic architecture of MADS and MADS-like systems, relative to other prokaryotic defenses, points toward highly elaborate mechanisms of sensing infections, defense activation, and/or interference.",

author = "Alice Maestri and Pons, {Benoit J} and Elizabeth Pursey and Chong, {Charlotte E} and Sylvain Gandon and Rafael Custodio and Anna Olina and Aleksei Agapov and Chisnall, {Matthew A W} and Anita Grasso and Steve Paterson and Szczelkun, {Mark D} and Baker, {Kate S} and {van Houte}, Stineke and Anne Chevallereau and Westra, {Edze R}",

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doi = "10.1016/j.chom.2024.07.005",

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Maestri, A, Pons, BJ, Pursey, E, Chong, CE, Gandon, S, Custodio, R, Olina, A, Agapov, A, Chisnall, MAW, Grasso, A, Paterson, S, Szczelkun, MD, Baker, KS, van Houte, S, Chevallereau, A & Westra, ER 2024, 'The bacterial defense system MADS interacts with CRISPR-Cas to limit phage infection and escape', Cell Host & Microbe, vol. 32, no. 8, pp. 1412-1426. https://doi.org/10.1016/j.chom.2024.07.005

TY - JOUR

T1 - The bacterial defense system MADS interacts with CRISPR-Cas to limit phage infection and escape

AU - Maestri, Alice

AU - Pons, Benoit J

AU - Pursey, Elizabeth

AU - Chong, Charlotte E

AU - Gandon, Sylvain

AU - Custodio, Rafael

AU - Olina, Anna

AU - Agapov, Aleksei

AU - Chisnall, Matthew A W

AU - Grasso, Anita

AU - Paterson, Steve

AU - Szczelkun, Mark D

AU - Baker, Kate S

AU - van Houte, Stineke

AU - Chevallereau, Anne

AU - Westra, Edze R

PY - 2024/8/14

Y1 - 2024/8/14

N2 - The constant arms race between bacteria and their parasites has resulted in a large diversity of bacterial defenses, with many bacteria carrying multiple systems. Here, we report the discovery of a phylogenetically widespread defense system, coined methylation-associated defense system (MADS), which is distributed across gram-positive and gram-negative bacteria. MADS interacts with a CRISPR-Cas system in its native host to provide robust and durable resistance against phages. While phages can acquire epigenetic-mediated resistance against MADS, co-existence of MADS and a CRISPR-Cas system limits escape emergence. MADS comprises eight genes with predicted nuclease, ATPase, kinase, and methyltransferase domains, most of which are essential for either self/non-self discrimination, DNA restriction, or both. The complex genetic architecture of MADS and MADS-like systems, relative to other prokaryotic defenses, points toward highly elaborate mechanisms of sensing infections, defense activation, and/or interference.

AB - The constant arms race between bacteria and their parasites has resulted in a large diversity of bacterial defenses, with many bacteria carrying multiple systems. Here, we report the discovery of a phylogenetically widespread defense system, coined methylation-associated defense system (MADS), which is distributed across gram-positive and gram-negative bacteria. MADS interacts with a CRISPR-Cas system in its native host to provide robust and durable resistance against phages. While phages can acquire epigenetic-mediated resistance against MADS, co-existence of MADS and a CRISPR-Cas system limits escape emergence. MADS comprises eight genes with predicted nuclease, ATPase, kinase, and methyltransferase domains, most of which are essential for either self/non-self discrimination, DNA restriction, or both. The complex genetic architecture of MADS and MADS-like systems, relative to other prokaryotic defenses, points toward highly elaborate mechanisms of sensing infections, defense activation, and/or interference.

U2 - 10.1016/j.chom.2024.07.005

DO - 10.1016/j.chom.2024.07.005

M3 - Article (Academic Journal)

C2 - 39094583

SN - 1931-3128

VL - 32

SP - 1412

EP - 1426

JO - Cell Host & Microbe

JF - Cell Host & Microbe

IS - 8

ER -

The bacterial defense system MADS interacts with CRISPR-Cas to limit phage infection and escape

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