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Bacterial defense systems exhibit synergistic anti-phage activity

Bacterial defense systems exhibit synergistic anti-phage activity
Bacterial defense systems exhibit synergistic anti-phage activity

Bacterial defense against phage predation involves diverse defense systems acting individually and concurrently, yet their interactions remain poorly understood. We investigated >100 defense systems in 42,925 bacterial genomes and identified numerous instances of their non-random co-occurrence and negative association. For several pairs of defense systems significantly co-occurring in Escherichia coli strains, we demonstrate synergistic anti-phage activity. Notably, Zorya II synergizes with Druantia III and ietAS defense systems, while tmn exhibits synergy with co-occurring systems Gabija, Septu I, and PrrC. For Gabija, tmn co-opts the sensory switch ATPase domain, enhancing anti-phage activity. Some defense system pairs that are negatively associated in E. coli show synergy and significantly co-occur in other taxa, demonstrating that bacterial immune repertoires are largely shaped by selection for resistance against host-specific phages rather than negative epistasis. Collectively, these findings demonstrate compatibility and synergy between defense systems, allowing bacteria to adopt flexible strategies for phage defense.

Druantia, Gabija, Kiwa, Septu, Zorya, co-occurrence, ietAS, phylogroups, prokaryotic immunity, tmn
1931-3128
557-572.e6
Wu, Yi
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Garushyants, Sofya K.
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van den Hurk, Anne
b75b61f2-e41b-43cf-98d1-b096c86ea993
Aparicio-Maldonado, Cristian
56c97975-9aec-4357-8946-427c1005c67e
Krishnakant Kushwaha, Simran
bc3db251-8aac-41e2-90fd-0269a6762cac
King, Claire M.
cceb07b6-6709-4c7c-a89d-78092dd1835b
Ou, Yaqing
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Todeschini, Thomas C.
882a8867-6cc5-4f5c-a8e3-16d92c7010b4
Clokie, Martha R.J.
60126061-db02-45e6-b455-5466bd7202d8
Millard, Andrew D.
a09e9669-01b5-47a9-a000-1ab227ed56c0
Gençay, Yilmaz Emre
cb911b99-a620-4d93-a49a-05392d9c65da
Koonin, Eugene V.
50994a87-40cf-4509-8f39-e2f5975e649b
Nobrega, Franklin L.
6532795d-88a4-4f05-9b26-6af5b8f21a0d
Wu, Yi
9ee1023a-7e89-4260-9030-5c8b9fb2e1d8
Garushyants, Sofya K.
de07b7b5-3368-4dcc-a64a-22dd974cac78
van den Hurk, Anne
b75b61f2-e41b-43cf-98d1-b096c86ea993
Aparicio-Maldonado, Cristian
56c97975-9aec-4357-8946-427c1005c67e
Krishnakant Kushwaha, Simran
bc3db251-8aac-41e2-90fd-0269a6762cac
King, Claire M.
cceb07b6-6709-4c7c-a89d-78092dd1835b
Ou, Yaqing
5672db61-7f5c-4bfc-b9aa-ee63ef19f3e3
Todeschini, Thomas C.
882a8867-6cc5-4f5c-a8e3-16d92c7010b4
Clokie, Martha R.J.
60126061-db02-45e6-b455-5466bd7202d8
Millard, Andrew D.
a09e9669-01b5-47a9-a000-1ab227ed56c0
Gençay, Yilmaz Emre
cb911b99-a620-4d93-a49a-05392d9c65da
Koonin, Eugene V.
50994a87-40cf-4509-8f39-e2f5975e649b
Nobrega, Franklin L.
6532795d-88a4-4f05-9b26-6af5b8f21a0d

Wu, Yi, Garushyants, Sofya K., van den Hurk, Anne, Aparicio-Maldonado, Cristian, Krishnakant Kushwaha, Simran, King, Claire M., Ou, Yaqing, Todeschini, Thomas C., Clokie, Martha R.J., Millard, Andrew D., Gençay, Yilmaz Emre, Koonin, Eugene V. and Nobrega, Franklin L. (2024) Bacterial defense systems exhibit synergistic anti-phage activity. Cell Host & Microbe, 32 (4), 557-572.e6. (doi:10.1016/j.chom.2024.01.015).

Record type: Article

Abstract

Bacterial defense against phage predation involves diverse defense systems acting individually and concurrently, yet their interactions remain poorly understood. We investigated >100 defense systems in 42,925 bacterial genomes and identified numerous instances of their non-random co-occurrence and negative association. For several pairs of defense systems significantly co-occurring in Escherichia coli strains, we demonstrate synergistic anti-phage activity. Notably, Zorya II synergizes with Druantia III and ietAS defense systems, while tmn exhibits synergy with co-occurring systems Gabija, Septu I, and PrrC. For Gabija, tmn co-opts the sensory switch ATPase domain, enhancing anti-phage activity. Some defense system pairs that are negatively associated in E. coli show synergy and significantly co-occur in other taxa, demonstrating that bacterial immune repertoires are largely shaped by selection for resistance against host-specific phages rather than negative epistasis. Collectively, these findings demonstrate compatibility and synergy between defense systems, allowing bacteria to adopt flexible strategies for phage defense.

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Accepted/In Press date: 30 January 2024
e-pub ahead of print date: 22 February 2024
Published date: 10 April 2024
Keywords: Druantia, Gabija, Kiwa, Septu, Zorya, co-occurrence, ietAS, phylogroups, prokaryotic immunity, tmn

Identifiers

Local EPrints ID: 491528
URI: http://eprints.soton.ac.uk/id/eprint/491528
ISSN: 1931-3128
PURE UUID: 6eeeb924-47dc-4c12-b51d-2ded944bb092
ORCID for Thomas C. Todeschini: ORCID iD orcid.org/0009-0000-1648-8029
ORCID for Franklin L. Nobrega: ORCID iD orcid.org/0000-0002-8238-1083

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Date deposited: 25 Jun 2024 17:03
Last modified: 26 Jun 2024 02:02

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Contributors

Author: Yi Wu
Author: Sofya K. Garushyants
Author: Anne van den Hurk
Author: Cristian Aparicio-Maldonado
Author: Simran Krishnakant Kushwaha
Author: Claire M. King
Author: Yaqing Ou
Author: Martha R.J. Clokie
Author: Andrew D. Millard
Author: Yilmaz Emre Gençay
Author: Eugene V. Koonin

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