Dual Targeting Factors Are Required for LXG Toxin Export by the Bacterial Type VIIb Secretion System

Klein, Timothy A.; Grebenc, Dirk W.; Shah, Prakhar Y.; McArthur, Owen D.; Dickson, Brandon H.; Surette, Michael G.; Kim, Youngchang; Whitney, John C.

doi:10.1128/mbio.02137-22

Title: Dual Targeting Factors Are Required for LXG Toxin Export by the Bacterial Type VIIb Secretion System

Journal Article · 28 August 2022 · mBio (Online)

DOI: https://doi.org/10.1128/mbio.02137-22 · OSTI ID:2404409

^[1];

^[1]; McArthur, Owen D. ^[1]; Dickson, Brandon H. ^[1];

^[1]; Kim, Youngchang ^[2];

^[1]

McMaster Univ., Hamilton, ON (Canada)
Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Bacterial type VIIb secretion systems (T7SSb) are multisubunit integral membrane protein complexes found in Firmicutes that play a role in both bacterial competition and virulence by secreting toxic effector proteins. The majority of characterized T7SSb effectors adopt a polymorphic domain architecture consisting of a conserved N-terminal Leu-X-Gly (LXG) domain and a variable C-terminal toxin domain. Recent work has started to reveal the diversity of toxic activities exhibited by LXG effectors; however, little is known about how these proteins are recruited to the T7SSb apparatus. In this work, we sought to characterize genes encoding domains of unknown function (DUFs) 3130 and 3958, which frequently cooccur with LXG effector-encoding genes. Using coimmunoprecipitation-mass spectrometry analyses, in vitro copurification experiments, and T7SSb secretion assays, we found that representative members of these protein families form heteromeric complexes with their cognate LXG domain and in doing so, function as targeting factors that promote effector export. Additionally, an X-ray crystal structure of a representative DUF3958 protein, combined with predictive modeling of DUF3130 using AlphaFold2, revealed structural similarity between these protein families and the ubiquitous WXG100 family of T7SS effectors. Interestingly, we identified a conserved FxxxD motif within DUF3130 that is reminiscent of the YxxxD/E “export arm” found in mycobacterial T7SSa substrates and mutation of this motif abrogates LXG effector secretion. Overall, our data experimentally link previously uncharacterized bacterial DUFs to type VIIb secretion and reveal a molecular signature required for LXG effector export.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: Canadian Institutes of Health Research (CIHR); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 2404409

Journal Information:: mBio (Online), Journal Name: mBio (Online) Journal Issue: 5 Vol. 13; ISSN 2150-7511

Publisher:: American Society for Microbiology (ASM)Copyright Statement

Country of Publication:: United States

Language:: English

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Title: Dual Targeting Factors Are Required for LXG Toxin Export by the Bacterial Type VIIb Secretion System

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