Homologous recombination between tandem paralogues drives evolution of Type VII secretion system immunity genes in firmicute bacteria

2022 ◽  
Author(s):  
Stephen Garrett ◽  
Giuseppina Mariano ◽  
Tracy Palmer
Keyword(s):  
Homologous Recombination ◽  
Sequence Homology ◽  
Secretion System ◽  
Immunity Protein ◽  
Conserved Sequence ◽  
Type Vii Secretion ◽  
Lipid Ii ◽  
Immunity Genes ◽  
Type Vii Secretion System ◽  
High Sequence Homology

The Type VII secretion system (T7SS) is found in many Gram-positive firmicutes and secretes protein toxins that mediate bacterial antagonism. Two T7SS toxins have been identified in Staphylococcus aureus, EsaD a nuclease toxin that is counteracted by the EsaG immunity protein, and TspA, which has membrane depolarising activity and is neutralised by TsaI. Both toxins are polymorphic, and strings of non-identical esaG and tsaI immunity genes are encoded in all S. aureus strains. During genome sequence analysis of closely related S. aureus strains we noted that there had been a deletion of six consecutive esaG copies in one lineage. To investigate this further, we analysed the sequences of the tandem esaG genes and their encoded proteins. We identified three blocks of high sequence homology shared by all esaG genes, and identified evidence of extensive recombination events between esaG paralogues facilitated through these conserved sequence blocks. Recombination between these blocks accounts for loss of esaG genes from S. aureus genomes. TipC, an immunity protein for the TelC lipid II phosphatase toxin secreted by the streptococcal T7SS, is also encoded by multiple gene paralogues. Two blocks of high sequence homology locate to the 5-prime and 3-prime end of tipC genes, and we found strong evidence for recombination between tipC paralogues encoded by Streptococcus mitis BCC08. By contrast, we found only a single block of homology across tsaI genes, and little evidence for intergenic recombination within this gene family. We conclude that homologous recombination is one of the drivers for the evolution of T7SS immunity gene clusters.

The Type VII Secretion System of Staphylococcus

2021 ◽  
Vol 75 (1) ◽  
Author(s):  
Lisa Bowman ◽  
Tracy Palmer
Keyword(s):  
Protein Transport ◽  
Secretion System ◽  
Genomic Islands ◽  
Annual Review ◽  
Publication Date ◽  
Bacterial Antagonism ◽  
Type Vii Secretion ◽  
Immunity Genes ◽  
Protein Secretion System ◽  
Type Vii Secretion System

The type VII protein secretion system (T7SS) of Staphylococcus aureus is encoded at the ess locus. T7 substrate recognition and protein transport are mediated by EssC, a membrane-bound multidomain ATPase. Four EssC sequence variants have been identified across S. aureus strains, each accompanied by a specific suite of substrate proteins. The ess genes are upregulated during persistent infection, and the secretion system contributes to virulence in disease models. It also plays a key role in intraspecies competition, secreting nuclease and membrane-depolarizing toxins that inhibit the growth of strains lacking neutralizing immunity proteins. A genomic survey indicates that the T7SS is widely conserved across staphylococci and is encoded in clusters that contain diverse arrays of toxin and immunity genes. The presence of genomic islands encoding multiple immunity proteins in species such as Staphylococcus warneri that lack the T7SS points to a major role for the secretion system in bacterial antagonism. Expected final online publication date for the Annual Review of Microbiology, Volume 75 is October 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

scholarly journals Molecular Basis for Immunity Protein Recognition of a Type VII Secretion System Exported Antibacterial Toxin

2018 ◽  
Vol 430 (21) ◽  
pp. 4344-4358 ◽  
Author(s):  
Timothy A. Klein ◽  
Manuel Pazos ◽  
Michael G. Surette ◽  
Waldemar Vollmer ◽  
John C. Whitney
Keyword(s):  
Molecular Basis ◽  
Secretion System ◽  
Protein Recognition ◽  
Immunity Protein ◽  
Type Vii Secretion ◽  
Type Vii Secretion System

scholarly journals Structure of EspB from the ESX-1 Type VII Secretion System and Insights into its Export Mechanism

Structure ◽  
2015 ◽  
Vol 23 (3) ◽  
pp. 571-583 ◽  
Author(s):  
Matthew Solomonson ◽  
Dheva Setiaputra ◽  
Karl A.T. Makepeace ◽  
Emilie Lameignere ◽  
Evgeniy V. Petrotchenko ◽  
...  
Keyword(s):  
Secretion System ◽  
Type Vii Secretion ◽  
Type Vii Secretion System

A Chimeric EccB-MycP Fusion Protein is Functional and a Stable Component of the ESX-5 Type VII Secretion System Membrane Complex

2020 ◽  
Vol 432 (4) ◽  
pp. 1265-1278 ◽  
Author(s):  
Vincent J.C. van Winden ◽  
Catalin M. Bunduc ◽  
Roy Ummels ◽  
Wilbert Bitter ◽  
Edith N.G. Houben
Keyword(s):  
Fusion Protein ◽  
Secretion System ◽  
Stable Component ◽  
Type Vii Secretion ◽  
Membrane Complex ◽  
Type Vii Secretion System

scholarly journals The Ess/Type VII secretion system of Staphylococcus aureus shows unexpected genetic diversity

BMC Genomics ◽  
2016 ◽  
Vol 17 (1) ◽  
Author(s):  
Ben Warne ◽  
Catriona P. Harkins ◽  
Simon R. Harris ◽  
Alexandra Vatsiou ◽  
Nicola Stanley-Wall ◽  
...  
Keyword(s):  
Genetic Diversity ◽  
Staphylococcus Aureus ◽  
Secretion System ◽  
Type Vii Secretion ◽  
Type Vii Secretion System

scholarly journals A Duplicated ESAT-6 Region of ESX-5 Is Involved in Protein Export and Virulence of Mycobacteria

2015 ◽  
Vol 83 (11) ◽  
pp. 4349-4361 ◽  
Author(s):  
Swati Shah ◽  
Joe R. Cannon ◽  
Catherine Fenselau ◽  
Volker Briken
Keyword(s):  
Secretion System ◽  
Bacterial Virulence ◽  
Inflammasome Activation ◽  
Zebrafish Model ◽  
Content Type ◽  
Type Vii Secretion ◽  
Specific Subset ◽  
Host Cell Death ◽  
Type Vii Secretion System

ABSTRACTThe ESX-5 secretion system ofMycobacterium tuberculosisis important for bacterial virulence and for the secretion of the large PE/PPE protein family, whose genes constitute 10% of theM. tuberculosisgenome. A four-gene region of the ESX-5 system is duplicated three times in theM. tuberculosisgenome, but the functions of these duplicates are unknown. Here we investigated one of these duplicates: the region carrying theesxI,esxJ,ppe15, andpe8genes (ESX-5a). An ESX-5a deletion mutant in the model systemM. marinumbackground was deficient in the secretion of some members of the PE/PPE family of proteins. Surprisingly, we also identified other proteins that are not members of this family, thus expanding the range of ESX-5 secretion substrates. In addition, we demonstrated that ESX-5a is important for the virulence ofM. marinumin the zebrafish model. Furthermore, we showed the role of theM. tuberculosisESX-5a region in inflammasome activation but not host cell death induction, which is different from the case for theM. tuberculosisESX-5 system. In conclusion, the ESX-5a region is nonredundant with its ESX-5 paralog and is necessary for secretion of a specific subset of proteins inM. tuberculosisandM. marinumthat are important for bacterial virulence ofM. marinum. Our findings point to a role for the three ESX-5 duplicate regions in the selection of substrates for secretion via ESX-5, and hence, they provide the basis for a refined model of the molecular mechanism of this type VII secretion system.

scholarly journals Crosstalk between the ancestral type VII secretion system ESX-4 and other T7SS in Mycobacterium marinum

iScience ◽  
2021 ◽  
pp. 103585
Author(s):  
Yuchen Wang ◽  
Yuting Tang ◽  
Chen Lin ◽  
Junli Zhang ◽  
Juntao Mai ◽  
...  
Keyword(s):  
Secretion System ◽  
Mycobacterium Marinum ◽  
Type Vii Secretion ◽  
Type Vii Secretion System ◽  
Ancestral Type

scholarly journals A type VII secretion system of Streptococcus gallolyticus subsp. gallolyticus contributes to gut colonization and the development of colon tumors

2021 ◽  
Vol 17 (1) ◽  
pp. e1009182
Author(s):  
John Culver Taylor ◽  
Xinsheng Gao ◽  
Juan Xu ◽  
Michael Holder ◽  
Joseph Petrosino ◽  
...  
Keyword(s):  
Bacterial Culture ◽  
Secretion System ◽  
Host Cells ◽  
Secretion Systems ◽  
Colon Tumors ◽  
Type Vii Secretion ◽  
Streptococcus Gallolyticus ◽  
Gut Colonization ◽  
Type Vii Secretion System

Streptococcus gallolyticus subspecies gallolyticus (Sgg) has a strong clinical association with colorectal cancer (CRC) and actively promotes the development of colon tumors. However, the molecular determinants involved in Sgg pathogenicity in the gut are unknown. Bacterial type VII secretion systems (T7SS) mediate pathogen interactions with their host and are important for virulence in pathogenic mycobacteria and Staphylococcus aureus. Through genome analysis, we identified a locus in Sgg strain TX20005 that encodes a putative type VII secretion system (designated as SggT7SST05). We showed that core genes within the SggT7SST05 locus are expressed in vitro and in the colon of mice. Western blot analysis showed that SggEsxA, a protein predicted to be a T7SS secretion substrate, is detected in the bacterial culture supernatant, indicating that this SggT7SST05 is functional. Deletion of SggT7SST05 (TX20005Δesx) resulted in impaired bacterial adherence to HT29 cells and abolished the ability of Sgg to stimulate HT29 cell proliferation. Analysis of bacterial culture supernatants suggest that SggT7SST05-secreted factors are responsible for the pro-proliferative activity of Sgg, whereas Sgg adherence to host cells requires both SggT7SST05-secreted and bacterial surface-associated factors. In a murine gut colonization model, TX20005Δesx showed significantly reduced colonization compared to the parent strain. Furthermore, in a mouse model of CRC, mice exposed to TX20005 had a significantly higher tumor burden compared to saline-treated mice, whereas those exposed to TX20005Δesx did not. Examination of the Sgg load in the colon in the CRC model suggests that SggT7SST05-mediated activities are directly involved in the promotion of colon tumors. Taken together, these results reveal SggT7SST05 as a previously unrecognized pathogenicity determinant for Sgg colonization of the colon and promotion of colon tumors.

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