Chimeric systems composed of swapped Tra subunits between distantly-related F plasmids reveal striking plasticity among type IV secretion machines

Bacterial type IV secretion systems (T4SSs) are a versatile family of macromolecular translocators, collectively able to recruit diverse DNA and protein substrates and deliver them to a wide range of cell types. Presently, there is little understanding of how T4SSs recognize substrate repertoires an...

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Published in:PLoS genetics 2024-03, Vol.20 (3), p.e1011088-e1011088
Main Authors: Kishida, Kouhei, Li, Yang Grace, Ogawa-Kishida, Natsumi, Khara, Pratick, Al Mamun, Abu Amar M, Bosserman, Rachel E, Christie, Peter J
Format: Article
Language:English
Subjects:
Bacterial Proteins - metabolism
Biology and Life Sciences
Chimeras
Conjugation
Deoxyribonucleic acid
DNA
DNA, Bacterial
F Factor
Fimbriae Proteins - genetics
Gene deletion
Genetic aspects
Gram-negative bacteria
Medicine and Health Sciences
Mutation
Nucleotide sequence
Plasmids
Plasmids - genetics
Proteins
Research and Analysis Methods
Secretion
Translocation (Genetics)
Type IV Secretion Systems - chemistry
Type IV Secretion Systems - genetics
Type IV Secretion Systems - metabolism
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Summary:Bacterial type IV secretion systems (T4SSs) are a versatile family of macromolecular translocators, collectively able to recruit diverse DNA and protein substrates and deliver them to a wide range of cell types. Presently, there is little understanding of how T4SSs recognize substrate repertoires and form productive contacts with specific target cells. Although T4SSs are composed of a number of conserved subunits and adopt certain conserved structural features, they also display considerable compositional and structural diversity. Here, we explored the structural bases underlying the functional versatility of T4SSs through systematic deletion and subunit swapping between two conjugation systems encoded by the distantly-related IncF plasmids, pED208 and F. We identified several regions of intrinsic flexibility among the encoded T4SSs, as evidenced by partial or complete functionality of chimeric machines. Swapping of VirD4-like TraD type IV coupling proteins (T4CPs) yielded functional chimeras, indicative of relaxed specificity at the substrate-TraD and TraD-T4SS interfaces. Through mutational analyses, we further delineated domains of the TraD T4CPs contributing to recruitment of cognate vs heterologous DNA substrates. Remarkably, swaps of components comprising the outer membrane core complexes, a few F-specific subunits, or the TraA pilins supported DNA transfer in the absence of detectable pilus production. Among sequenced enterobacterial species in the NCBI database, we identified many strains that harbor two or more F-like plasmids and many F plasmids lacking one or more T4SS components required for self-transfer. We confirmed that host cells carrying co-resident, non-selftransmissible variants of pED208 and F elaborate chimeric T4SSs, as evidenced by transmission of both plasmids. We propose that T4SS plasticity enables the facile assembly of functional chimeras, and this intrinsic flexibility at the structural level can account for functional diversification of this superfamily over evolutionary time and, on a more immediate time-scale, to proliferation of transfer-defective MGEs in nature.
ISSN:1553-7404
1553-7390
1553-7404
DOI:10.1371/journal.pgen.1011088