Comprehensive Genomic Analysis Reveals Extensive Diversity of Type I and Type IV Secretion Systems in Klebsiella pneumoniae

Yang, Menglei; Zhou, Xinzhu; Bao, Yang‐Yang; Zhang, Yang; Liu, Boya; Lin, Ge; Wei, Tao; Tuo, Jiying; Gong, H.

doi:10.1007/s00284-023-03362-5

Cited by 5 publications

(4 citation statements)

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“…The type IV secretion system (T4SS) is evolutionarily related to the conjugation system of bacteria and it was speculated that the low GC content and the presence of T4SS may be linked with horizontal gene transfer (HGT), which helps bacteria adapt to environmental changes and acquire antibiotic resistance. In a recent study of 952 K. pneumoniae strains, the presence of one conserved T2SS, one conserved T5SS, and two conserved T6SS was detected in more than 90% of the strains, whereas T1SS and T4SS were enriched in the hypervirulent and classical multidrug resistance pathotypes of K. pneumoniae, respectively [19]. In ECC, T2SS genes were absent in the E. kobei, E. hormaechei, and E. ludwigii, type strains previously studied, but there is a lack of experimental data to link the absence of T2SS with the pathogenicity of these strains.…”

Section: Discussionmentioning

confidence: 99%

“…In silico characterisation and comparative genomics were performed for the gene clusters encoding the major virulence components of the cell surface of Gram-negative bacteria, such as the enterobacterial common antigen (ECA), colanic acid (CA), and O-antigen lipopolysaccharide (LPS), pili, flagella and fimbriae [7,8]. Additionally, we have explored the presence of genomic islands, which carried acquired plasmids, antimicrobial resistance and virulence genes, including secretion systems and toxin-antitoxin systems [18][19][20].…”

Section: Introductionmentioning

confidence: 99%

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Comprehensive Analysis of Virulence Determinants and Genomic Islands of blaNDM-1-Producing Enterobacter hormaechei Clinical Isolates from Greece

Mavroidi,

Gartzonika,

Spanakis

et al. 2023

Antibiotics

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Nosocomial outbreaks of multidrug-resistant (MDR) Enterobacter cloacae complex (ECC) are often reported worldwide, mostly associated with a small number of multilocus-sequence types of E. hormaechei and E. cloacae strains. In Europe, the largest clonal outbreak of blaNDM-1-producing ECC has been recently reported, involving an ST182 E. hormaechei strain in a Greek teaching hospital. In the current study, we aimed to further investigate the genetic make-up of two representative outbreak isolates. Comparative genomics of whole genome sequences (WGS) was performed, including whole genome-based taxonomic analysis and in silico prediction of virulence determinants of the bacterial cell surface, plasmids, antibiotic resistance genes and virulence factors present on genomic islands. The enterobacterial common antigen and the colanic antigen of the cell surface were identified in both isolates, being similar to the gene clusters of the E. hormaechei ATCC 49162 and E. cloacae ATCC 13047 type strains, whereas the two strains possessed different gene clusters encoding lipopolysaccharide O-antigens. Other virulence factors of the bacterial cell surface, such as flagella, fimbriae and pili, were also predicted to be encoded by gene clusters similar to those found in Enterobacter spp. and other Enterobacterales. Secretion systems and toxin–antitoxin systems, which also contribute to pathogenicity, were identified. Both isolates harboured resistance genes to multiple antimicrobial classes, including β-lactams, aminoglycosides, quinolones, chloramphenicol, trimethoprim, sulfonamides and fosfomycin; they carried blaTEM-1, blaOXA-1, blaNDM-1, and one of them also carried blaCTXM-14, blaCTXM-15 and blaLAP-2 plasmidic alleles. Our comprehensive analysis of the WGS assemblies revealed that blaNDM-1-producing outbreak isolates possess components of the bacterial cell surface as well as genomic islands, harbouring resistance genes to several antimicrobial classes and various virulence factors. Differences in the plasmids carrying β-lactamase genes between the two strains have also shown diverse modes of acquisition and an ongoing evolution of these mobile elements.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Comprehensive Analysis of Virulence Determinants and Genomic Islands of blaNDM-1-Producing Enterobacter hormaechei Clinical Isolates from Greece

Mavroidi,

Gartzonika,

Spanakis

et al. 2023

Antibiotics

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“…Aside from being in S. maltophilia , T4SSs are known to function in both environmental bacteria, including species of Agrobacterium, Bradyrhizobium, Lysinibacillus, Lysobacter, Mesorhizobium, Piscirickettsia, Dinoroseobacter, Sinorhizobium, Vampirovibrio, Vibrio, Wolbachia, and Xanthomonas ( 45 , 56 , 114 – 127 ), and pathogens of humans/mammals, including species of Actinobacillus, Anaplasma , Bartonella , Bordetella, Brucella, Burkholderia, Coxiella, Ehrlichia, Escherichia, Helicobacter, Klebsiella, Legionella, Neisseria, Orientia, and Rickettsia ( 48 , 128 – 153 ). Thus, studies on the T4SS of S. maltophilia and its bactericidal role should have broad implications in environmental, agricultural, and medical arenas.…”

Section: Discussionmentioning

confidence: 99%

Bactericidal effectors of the Stenotrophomonas maltophilia type IV secretion system: functional definition of the nuclease TfdA and structural determination of TfcB

Cobe,

Dey,

Minasov

et al. 2024

mBio

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Stenotrophomonas maltophilia expresses a type IV protein secretion system (T4SS) that promotes contact-dependent killing of other bacteria and does so partly by secreting the effector TfcB. Here, we report the structure of TfcB, comprising an N-terminal domain similar to the catalytic domain of glycosyl hydrolase (GH-19) chitinases and a C-terminal domain for recognition and translocation by the T4SS. Utilizing a two-hybrid assay to measure effector interactions with the T4SS coupling protein VirD4, we documented the existence of five more T4SS substrates. One of these was protein 20845, an annotated nuclease. A S. maltophilia mutant lacking the gene for 20845 was impaired for killing Escherichia coli , Klebsiella pneumoniae , and Pseudomonas aeruginosa . Moreover, the cloned 20845 gene conferred robust toxicity, with the recombinant E. coli being rescued when 20845 was co-expressed with its cognate immunity protein. The 20845 effector was an 899 amino-acid protein, comprised of a GHH-nuclease domain in its N-terminus, a large central region of indeterminant function, and a C-terminus for secretion. Engineered variants of the 20845 gene that had mutations in the predicted catalytic site did not impede E. coli , indicating that the antibacterial effect of 20845 involves its nuclease activity. Using flow cytometry with DNA staining, we determined that 20845, but not its mutant variants, confers a loss in DNA content of target bacteria. Database searches revealed that uncharacterized homologs of 20845 occur within a range of bacteria. These data indicate that the S. maltophilia T4SS promotes interbacterial competition through the action of multiple toxic effectors, including a potent, novel DNase. IMPORTANCE Stenotrophomonas maltophilia is a multi-drug-resistant, Gram-negative bacterium that is an emerging pathogen of humans. Patients with cystic fibrosis are particularly susceptible to S. maltophilia infection. In hospital water systems and various types of infections, S. maltophilia co-exists with other bacteria, including other pathogens such as Pseudomonas aeruginosa . We previously demonstrated that S. maltophilia has a functional VirB/D4 type VI protein secretion system (T4SS) that promotes contact-dependent killing of other bacteria. Since most work on antibacterial systems involves the type VI secretion system, this observation remains noteworthy. Moreover, S. maltophilia currently stands alone as a model for a human pathogen expressing an antibacterial T4SS. Using biochemical, genetic, and cell biological approaches, we now report both the discovery of a novel antibacterial nuclease (TfdA) and the first structural determination of a bactericidal T4SS effector (TfcB).

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“…The T9SS, on the other hand, is a recently discovered secretion system that has only been found in Bacteroides bacteria. 3 First identified in V. cholerae by Pukatzki et al in 2006, the Type VI Secretion System (T6SS) is involved in the secretion of hemolysin co-regulatory protein (Hcp) and valine-glycine repeat protein G (VgrG). 4 These secretions are associated with cytotoxic effects and require a cluster of intracellular multiplication protein F-related homologous genes.…”

Section: Introductionmentioning

confidence: 99%

The Biological and Regulatory Role of Type VI Secretion System of Klebsiella pneumoniae

Liu,

Li,

Cao

et al. 2023

IDR

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Bacteria communicate with their surroundings through diverse secretory systems, and the recently discovered Type VI Secretion System (T6SS) has gained significant attention. Klebsiella pneumoniae (K. pneumoniae), an opportunistic pathogen known for causing severe infections in both hospital and animal settings, possesses this intriguing T6SS. This system equips K. pneumoniae with a formidable armory of protein-based weaponry, enabling the delivery of toxins into neighboring cells, thus granting a substantial competitive advantage. Remarkably, the T6SS has also been associated with K. pneumoniae's ability to form biofilms and acquire resistance against antibiotics. However, the precise effects of the T6SS on K. pneumoniae's functions remain inadequately studied, despite research efforts to understand the intricacies of these mechanisms. This comprehensive review aims to provide an overview of the current knowledge regarding the biological functions and regulatory mechanisms of the T6SS in K. pneumoniae.

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Comprehensive Genomic Analysis Reveals Extensive Diversity of Type I and Type IV Secretion Systems in Klebsiella pneumoniae

Cited by 5 publications

References 50 publications

Comprehensive Analysis of Virulence Determinants and Genomic Islands of blaNDM-1-Producing Enterobacter hormaechei Clinical Isolates from Greece

Comprehensive Analysis of Virulence Determinants and Genomic Islands of blaNDM-1-Producing Enterobacter hormaechei Clinical Isolates from Greece

Bactericidal effectors of the Stenotrophomonas maltophilia type IV secretion system: functional definition of the nuclease TfdA and structural determination of TfcB

The Biological and Regulatory Role of Type VI Secretion System of Klebsiella pneumoniae

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