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PreprintCited by 1Plant Pathogenic Bacteria StudiesBacterial Genetics and BiotechnologyEscherichia coli research studies

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The protective function of an immunity protein against the cis -toxic effects of a Xanthomonas Type IV Secretion System Effector

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Oka, Gabriel U., Souza, Diorge P., Sgro, Germán G., Guzzo, Cristiane R., Dunger, German, Farah, Chuck S.·2023·EMBO Reports
DOI 10.1101/2023.08.28.555164PMC PMC10933484

Preprint — published as 10.1038/s44319-024-00060-6

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Abstract

Many bacterial species use specialized secretion systems to translocate proteinaceous toxic effectors into target bacterial cells. In most cases, effectors are encoded in bicistronic operons with their cognate immunity proteins. The current model is that immunity proteins could, in principle, provide protection in two different ways: i) by avoiding self-intoxication (suicide or cis -intoxication) or ii) by inhibiting intoxication due to “friendly-fire” translocation from neighboring sister cells (fratricide or trans -intoxication). Here, we set out to distinguish between these two protection mechanisms in the case of the bactericidal Xanthomonas citri Type IV Secretion System (X-T4SS), where killing is due to the action of a cocktail of secreted effectors (X-Tfes) that are inhibited by their cognate immunity proteins (X-Tfis). We use a set of X. citri mutants lacking multiple X-Tfe/X-Tfi pairs to show that X-Tfis are not absolutely required to protect against trans -intoxication. Our investigation then focused on the in vivo function of the lysozyme-like effector X-Tfe XAC2609 and its cognate immunity protein X-Tfi XAC2610 . We observe the accumulation of damage in the X. citri cell envelope and inhibition of biofilm formation due to the action of X-Tfe XAC2609 in the absence of X-Tfi XAC2610 . We show that X-Tfe XAC2609 toxicity is independent of an active X-T4SS and that X-Tfi XAC2610 protects the cell colony against X-Tfe XAC2609 -induced cis -intoxication via autolysis. In vitro assays employing X-Tfi XAC2610 mutants were used to test and validate an AlphaFold2-derived model of the X-Tfe XAC2609 -X-Tfi XAC2610 complex which presents topological similarities with the distantly related Tse1/Tsi1 complex from P. aeruginosa and the the i-type lysozyme from Meretrix lusoria (MI-iLys) in complex with PliI-Ah from Aeromonas hydrophila . While immunity proteins in other systems have been shown to protect against attacks by sister cells ( trans -intoxication), this is the first description of an antibacterial secretion system in which the immunity proteins are dedicated to protecting cells against cis -intoxication.

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Metadata

Authors
Oka, G. U., Souza, D. P., Sgro, G. G., Guzzo, C. R., Dunger, G., & Farah, C. S.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • Universidade de São Paulo (BR)
Corresponding author
Farah, Chuck S.
ORCID
Venue
EMBO Reports
Publisher
openRxiv
Published
2023-08-29
Volume
25
Issue
3
Pages
1436-1452
ISSN
1469-221X (ISSN-L)
DOI
10.1101/2023.08.28.555164
PMC
PMC10933484
OpenAlex
W4391644948
Cited by
1
References
1
Citations by year
2026: 1
FWCI
0.24
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • EMBO Reports (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Conicet (submittedVersion, cc-by)
  • HAL (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Greater South Information System
Funders
  • Fundação de Amparo à Pesquisa do Estado de São Paulo (2014/04294-1, 21/10577-0, 2011/22571-4, 2014/, 17/17303-7, 2017/173037, 2011/50521-1, 2021/, 2018/09277-9)
  • Universidade de São Paulo
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Pathogenic Bacteria Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Immunology and Microbiology › Microbiology › Escherichia coli research studies
Keywords
Xanthomonas citri, type IV secretion system, immunity proteins, effector proteins, cell envelope damage, cell death, biofilm formation, bacterial competition
MeSH terms
Type IV Secretion Systems, Anti-Bacterial Agents, Bacterial Proteins, Humans, Xanthomonas

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