scholarly journals Modular evolution of secretion systems and virulence plasmids in a bacterial species complex

BMC Biology ◽  
2022 ◽  
Vol 20 (1) ◽  
Author(s):  
Lin Chou ◽  
Yu-Chen Lin ◽  
Mindia Haryono ◽  
Mary Nia M. Santos ◽  
Shu-Ting Cho ◽  
...  
Keyword(s):  
Species Complex ◽  
Bacterial Species ◽  
Secretion System ◽  
Type Vi Secretion System ◽  
Secretion Systems ◽  
Bacterial Taxonomy ◽  
Plant Host ◽  
Modular Evolution ◽  
Species Complexes ◽  
Genes Encoding

Abstract Background Many named species as defined in current bacterial taxonomy correspond to species complexes. Uncertainties regarding the organization of their genetic diversity challenge research efforts. We utilized the Agrobacterium tumefaciens species complex (a.k.a. Agrobacterium biovar 1), a taxon known for its phytopathogenicity and applications in transformation, as a study system and devised strategies for investigating genome diversity and evolution of species complexes. Results We utilized 35 genome assemblies, including 14 newly generated ones, to achieve a phylogenetically balanced sampling of A. tumefaciens. Our genomic analysis suggested that the 10 genomospecies described previously are distinct biological species and supported a quantitative guideline for species delineation. Furthermore, our inference of gene content and core-genome phylogeny allowed for investigations of genes critical in fitness and ecology. For the type VI secretion system (T6SS) involved in interbacterial competition and thought to be conserved, we detected multiple losses and one horizontal gene transfer. For the tumor-inducing plasmids (pTi) and pTi-encoded type IV secretion system (T4SS) that are essential for agrobacterial phytopathogenicity, we uncovered novel diversity and hypothesized their involvement in shaping this species complex. Intriguingly, for both T6SS and T4SS, genes encoding structural components are highly conserved, whereas extensive diversity exists for genes encoding effectors and other proteins. Conclusions We demonstrate that the combination of a phylogeny-guided sampling scheme and an emphasis on high-quality assemblies provides a cost-effective approach for robust analysis in evolutionary genomics. We show that the T6SS VgrG proteins involved in specific effector binding and delivery can be classified into distinct types based on domain organization. The co-occurrence patterns of VgrG-associated domains and the neighboring genes that encode different chaperones/effectors can be used to infer possible interacting partners. Similarly, the associations between plant host preference and the pTi type among these strains can be used to infer phenotype-genotype correspondence. Our strategies for multi-level investigations at scales that range from whole genomes to intragenic domains and phylogenetic depths from between- to within-species are applicable to other bacteria. Furthermore, modularity observed in the molecular evolution of genes and domains is useful for inferring functional constraints and informing experimental works.

scholarly journals The Francisella Pathogenicity Island Protein PdpD Is Required for Full Virulence and Associates with Homologues of the Type VI Secretion System

2008 ◽  
Vol 190 (13) ◽  
pp. 4584-4595 ◽  
Author(s):  
Jagjit S. Ludu ◽  
Olle M. de Bruin ◽  
Barry N. Duplantis ◽  
Crystal L. Schmerk ◽  
Alicia Y. Chou ◽  
...  
Keyword(s):  
North America ◽  
Outer Membrane ◽  
Bacterial Pathogen ◽  
Pathogenicity Island ◽  
Secretion System ◽  
Type Vi Secretion System ◽  
Secretion Systems ◽  
Intracellular Growth ◽  
Type Vi Secretion ◽  
Genes Encoding

ABSTRACT Francisella tularensis is a highly infectious, facultative intracellular bacterial pathogen that is the causative agent of tularemia. Nearly a century ago, researchers observed that tularemia was often fatal in North America but almost never fatal in Europe and Asia. The chromosomes of F. tularensis strains carry two identical copies of the Francisella pathogenicity island (FPI), and the FPIs of North America-specific biotypes contain two genes, anmK and pdpD, that are not found in biotypes that are distributed over the entire Northern Hemisphere. In this work, we studied the contribution of anmK and pdpD to virulence by using F. novicida, which is very closely related to F. tularensis but which carries only one copy of the FPI. We showed that anmK and pdpD are necessary for full virulence but not for intracellular growth. This is in sharp contrast to most other FPI genes that have been studied to date, which are required for intracellular growth. We also showed that PdpD is localized to the outer membrane. Further, overexpression of PdpD affects the cellular distribution of FPI-encoded proteins IglA, IglB, and IglC. Finally, deletions of FPI genes encoding proteins that are homologues of known components of type VI secretion systems abolished the altered distribution of IglC and the outer membrane localization of PdpD.

scholarly journals Species boundaries in the Agrobacterium tumefaciens complex and multi-level modular evolution of their antibacterial type VI secretion system and tumor-inducing plasmids

2021 ◽  
Author(s):  
Lin Chou ◽  
Yu-Chen Lin ◽  
Mindia Haryono ◽  
Mary Nia M. Santos ◽  
Shu-Ting Cho ◽  
...  
Keyword(s):  
Agrobacterium Tumefaciens ◽  
Pathogenic Bacteria ◽  
Secretion System ◽  
Species Boundaries ◽  
Type Vi Secretion System ◽  
Type Iv ◽  
Type Vi Secretion ◽  
Modular Evolution ◽  
Species Complexes ◽  
Genome Phylogeny

Many pathogenic bacteria are recognized as species complexes and uncertainties regarding the organization of their genetic diversity are challenges for research efforts. Within Agrobacterium tumefaciens, multiple genomospecies have been identified; however, the exact species boundaries are unclear, which causes chaos in nomenclature and hampers communication. In this work, we conducted targeted genome sequencing to achieve a comprehensive and balanced taxon sampling within this complex. Our results from genome-wide sequence identity, core genome phylogeny, and gene content not only supported that those recognized genomospecies are distinct biological entities but also identified novel genomospecies. Based on the fully resolved phylogeny, we further investigated the evolution of genes critical in Agrobacterium fitness and ecology. For the type VI secretion system (T6SS) involved in interbacterial competition, multiple losses and one horizontal gene transfer (HGT) event were inferred. For the tumor-inducing plasmids (pTi) and the pTi-encoded type IV secretion system (T4SS) that determine Agrobacterium phytopathogenicity, the evolution of these accessory replicons was decoupled from the chromosomes, thus contributing to another level of complexity. Intriguingly, for both T6SS and T4SS, genes that encode the structural components are highly conserved, whereas extensive diversity exists at multiple levels (i.e., between-species, within-species, intra-genome, and intra-gene) for genes that encode effectors and associated proteins. These findings suggest that opposite modes of selection may act on components conferring different functions within a system. In conclusion, this work provides insights into the genomic diversification of these bacteria and sheds light on the modularity of their molecular evolution.

scholarly journals A New Front in Microbial Warfare—Delivery of Antifungal Effectors by the Type VI Secretion System

2019 ◽  
Vol 5 (2) ◽  
pp. 50 ◽  
Author(s):  
Katharina Trunk ◽  
Sarah J. Coulthurst ◽  
Janet Quinn
Keyword(s):  
Bacterial Species ◽  
Fungal Species ◽  
Secretion System ◽  
Effector Proteins ◽  
Primary Role ◽  
Bacterial Cells ◽  
Type Vi Secretion System ◽  
Type Vi Secretion ◽  
Bacteria And Fungi ◽  
Polymicrobial Communities

Microbes typically exist in mixed communities and display complex synergistic and antagonistic interactions. The Type VI secretion system (T6SS) is widespread in Gram-negative bacteria and represents a contractile nano-machine that can fire effector proteins directly into neighbouring cells. The primary role assigned to the T6SS is to function as a potent weapon during inter-bacterial competition, delivering antibacterial effectors into rival bacterial cells. However, it has recently emerged that the T6SS can also be used as a powerful weapon against fungal competitors, and the first fungal-specific T6SS effector proteins, Tfe1 and Tfe2, have been identified. These effectors act via distinct mechanisms against a variety of fungal species to cause cell death. Tfe1 intoxication triggers plasma membrane depolarisation, whilst Tfe2 disrupts nutrient uptake and induces autophagy. Based on the frequent coexistence of bacteria and fungi in microbial communities, we propose that T6SS-dependent antifungal activity is likely to be widespread and elicited by a suite of antifungal effectors. Supporting this hypothesis, homologues of Tfe1 and Tfe2 are found in other bacterial species, and a number of T6SS-elaborating species have been demonstrated to interact with fungi. Thus, we envisage that antifungal T6SS will shape many polymicrobial communities, including the human microbiota and disease-causing infections.

scholarly journals Molecular and Structural Analysis of the Helicobacter pylori cag Type IV Secretion System Core Complex

mBio ◽  
2016 ◽  
Vol 7 (1) ◽  
Author(s):  
Arwen E. Frick-Cheng ◽  
Tasia M. Pyburn ◽  
Bradley J. Voss ◽  
W. Hayes McDonald ◽  
Melanie D. Ohi ◽  
...  
Keyword(s):  
Helicobacter Pylori ◽  
Bacterial Species ◽  
Secretion System ◽  
Effector Proteins ◽  
Type Iv Secretion ◽  
Secretion Systems ◽  
Core Complex ◽  
Type Iv ◽  
Membrane Spanning ◽  
H Pylori

ABSTRACT Bacterial type IV secretion systems (T4SSs) can function to export or import DNA, and can deliver effector proteins into a wide range of target cells. Relatively little is known about the structural organization of T4SSs that secrete effector proteins. In this report, we describe the isolation and analysis of a membrane-spanning core complex from the Helicobacter pylori cag T4SS, which has an important role in the pathogenesis of gastric cancer. We show that this complex contains five H. pylori proteins, CagM, CagT, Cag3, CagX, and CagY, each of which is required for cag T4SS activity. CagX and CagY are orthologous to the VirB9 and VirB10 components of T4SSs in other bacterial species, and the other three Cag proteins are unique to H. pylori . Negative stain single-particle electron microscopy revealed complexes 41 nm in diameter, characterized by a 19-nm-diameter central ring linked to an outer ring by spoke-like linkers. Incomplete complexes formed by Δ cag3 or Δ cagT mutants retain the 19-nm-diameter ring but lack an organized outer ring. Immunogold labeling studies confirm that Cag3 is a peripheral component of the complex. The cag T4SS core complex has an overall diameter and structural organization that differ considerably from the corresponding features of conjugative T4SSs. These results highlight specialized features of the H. pylori cag T4SS that are optimized for function in the human gastric mucosal environment. IMPORTANCE Type IV secretion systems (T4SSs) are versatile macromolecular machines that are present in many bacterial species. In this study, we investigated a T4SS found in the bacterium Helicobacter pylori. H. pylori is an important cause of stomach cancer, and the H. pylori T4SS contributes to cancer pathogenesis by mediating entry of CagA (an effector protein regarded as a “bacterial oncoprotein”) into gastric epithelial cells. We isolated and analyzed the membrane-spanning core complex of the H. pylori T4SS and showed that it contains unique proteins unrelated to components of T4SSs in other bacterial species. These results constitute the first structural analysis of the core complex from this important secretion system.

Comparative genomics of JapaneseErwinia pyrifoliaestrain Ejp617 with closely related erwinias

Genome ◽  
2013 ◽  
Vol 56 (2) ◽  
pp. 83-90 ◽  
Author(s):  
Shree P. Thapa ◽  
Duck H. Park ◽  
Won S. Kim ◽  
Beom S. Choi ◽  
Jong S. Lim ◽  
...  
Keyword(s):  
Dna Sequences ◽  
Secretion System ◽  
Open Reading Frames ◽  
Whole Genome Sequence ◽  
Type Vi Secretion System ◽  
Secretion Systems ◽  
Type Iii Secretion Systems ◽  
Central Regions ◽  
Shoot Blight ◽  
Protein Secretion System

Japanese Erwinia pyrifoliae strains cause bacterial shoot blight of pear (BSBP) in Japan. The genetics of Japanese Erwinia remains largely unknown relative to the abundant genomic information available for other Erwinia strains. We compared the genome of Japanese and Korean E. pyrifoliae strains along with those of E. amylovora and E. tasmaniensis. Comparisons with the Korean E. pyrifoliae strain revealed numerous gene insertions/deletions, rearrangements, and inversions in the central regions of the chromosomes. Approximately 80% (2843) of coding DNA sequences (CDSs) are shared by these two genomes which represent about three-quarters of the genome, and there are about 20% unique CDSs. Comparative analysis with closely related erwinias showed that 1942 (more than 50%) core open reading frames (ORF) are shared by all these strains. In addition to two type III secretion systems (hrp/dsp and inv/spa), the genome of Ejp617 encodes numerous virulence factors, including a type VI secretion system, an exopolysaccharide synthesis cluster, and another protein secretion system present in plant pathogenic Erwinia strains. The availability of whole genome sequence should provide a resource to further improve the understanding of pathogenesis in Japanese E. pyrifoliae Ejp617 and to facilitate evolutionary studies among the species of the genus Erwinia.

scholarly journals Chlamydial Type III Secretion System Is Encoded on Ten Operons Preceded by Sigma 70-Like Promoter Elements

2006 ◽  
Vol 189 (1) ◽  
pp. 198-206 ◽  
Author(s):  
P. Scott Hefty ◽  
Richard S. Stephens
Keyword(s):  
Type Iii Secretion ◽  
Transcriptional Start Site ◽  
Type Iii Secretion System ◽  
Regulatory Elements ◽  
Secretion System ◽  
Secretion Systems ◽  
Promoter Elements ◽  
Type Iii ◽  
Type Iii Secretion Systems ◽  
Genes Encoding

ABSTRACT Many gram-negative bacterial pathogens employ type III secretion systems for infectious processes. Chlamydiae are obligate intracellular bacteria that encode a conserved type III secretion system that is likely requisite for growth. Typically, genes encoding type III secretion systems are located in a single locus; however, for chlamydiae these genes are scattered throughout the genome. Little is known regarding the gene regulatory mechanisms for this essential virulence determinant. To facilitate identification of cis-acting transcriptional regulatory elements, the operon structure was determined. This analysis revealed 10 operons that contained 37 genes associated with the type III secretion system. Linkage within these operons suggests a role in type III secretion for each of these genes, including 13 genes encoding proteins with unknown function. The transcriptional start site for each operon was determined. In conjunction with promoter activity assays, this analysis revealed that the type III secretion system operons encode σ70-like promoter elements. Transcriptional initiation by a sigma factor responsible for constitutive gene expression indicates that undefined activators or repressors regulate developmental stage-specific expression of chlamydial type III secretion system genes.

scholarly journals VipA N-terminal linker and VipB-VipB interaction modulate the contraction of Type VI secretion system sheath

2017 ◽  
Author(s):  
Maximilian Brackmann ◽  
Jing Wang ◽  
Marek Basler
Keyword(s):  
Protein Translocation ◽  
Secretion System ◽  
Mass Spectrometry Analysis ◽  
Target Cells ◽  
Extended State ◽  
Type Vi Secretion System ◽  
Secretion Systems ◽  
Spectrometry Analysis ◽  
Type Vi Secretion ◽  
Bacterial Type

AbstractSecretion systems are essential for bacteria to survive and manipulate their environment. The bacterial Type VI Secretion System (T6SS) generates the force needed for protein translocation by the contraction of a long polymer called sheath, which is composed of interconnected VipA/VipB subunits forming a six-start helix. The mechanism of T6SS sheath contraction and the structure of its extended state are unknown. Here we show that elongating the N-terminal VipA linker or eliminating charge of a specific VipB residue abolished sheath contraction and delivery of effectors into target cells. The assembly of the non-contractile sheaths was dependent on the baseplate component TssE and mass-spectrometry analysis identified Hcp, VgrG and other components of the T6SS baseplate specifically associated with stable non-contractile sheaths. The ability to lock T6SS in the pre-firing state opens new possibilities for understanding its mode of action.

scholarly journals Mutations in Salmonella Pathogenicity Island 2 (SPI2) Genes Affecting Transcription of SPI1 Genes and Resistance to Antimicrobial Agents

1998 ◽  
Vol 180 (18) ◽  
pp. 4775-4780 ◽  
Author(s):  
Jörg Deiwick ◽  
Thomas Nikolaus ◽  
Jaqueline E. Shea ◽  
Colin Gleeson ◽  
David W. Holden ◽  
...  
Keyword(s):  
Type Iii Secretion ◽  
Antimicrobial Agents ◽  
Type Iii Secretion System ◽  
Polymyxin B ◽  
Secretion System ◽  
Effector Proteins ◽  
Secretion Systems ◽  
Type Iii ◽  
Genes Encoding

ABSTRACT The Salmonella typhimurium genome contains two pathogenicity islands (SPI) with genes encoding type III secretion systems for virulence proteins. SPI1 is required for the penetration of the epithelial layer of the intestine. SPI2 is important for the subsequent proliferation of bacteria in the spleens of infected hosts. Although most mutations in SPI2 lead to a strong reduction of virulence, they have different effects in vitro, with some mutants having significantly increased sensitivity to gentamicin and the antibacterial peptide polymyxin B. Previously we showed that certain mutations in SPI2 affect the ability of S. typhimurium to secrete SPI1 effector proteins and to invade cultured eukaryotic cells. In this study, we show that these SPI2 mutations affect the expression of the SPI1 invasion genes. Analysis of reporter fusions to various SPI1 genes reveals highly reduced expression of sipC,prgK, and hilA, the transcriptional activator of SPI1 genes. These observations indicate that the expression of one type III secretion system can be influenced dramatically by mutations in genes encoding a second type III secretion system in the same cell.

scholarly journals A family of Type VI secretion system effector proteins that form ion-selective pores

2019 ◽  
Vol 10 (1) ◽  
Author(s):  
Giuseppina Mariano ◽  
Katharina Trunk ◽  
David J. Williams ◽  
Laura Monlezun ◽  
Henrik Strahl ◽  
...  
Keyword(s):  
Opportunistic Pathogen ◽  
Effector Proteins ◽  
Type Vi Secretion System ◽  
Secretion Systems ◽  
New Family ◽  
Type Vi Secretion ◽  
Genes Encoding ◽  
Outer Membrane Permeability ◽  
Bacterial Effectors

AbstractType VI secretion systems (T6SSs) are nanomachines widely used by bacteria to deliver toxic effector proteins directly into neighbouring cells. However, the modes of action of many effectors remain unknown. Here we report that Ssp6, an anti-bacterial effector delivered by a T6SS of the opportunistic pathogen Serratia marcescens, is a toxin that forms ion-selective pores. Ssp6 inhibits bacterial growth by causing depolarisation of the inner membrane in intoxicated cells, together with increased outer membrane permeability. Reconstruction of Ssp6 activity in vitro demonstrates that it forms cation-selective pores. A survey of bacterial genomes reveals that genes encoding Ssp6-like effectors are widespread in Enterobacteriaceae and often linked with T6SS genes. We conclude that Ssp6 and similar proteins represent a new family of T6SS-delivered anti-bacterial effectors.

scholarly journals Comparative Analysis of Two Emerging Rice Seed Bacterial Pathogens

2014 ◽  
Vol 104 (5) ◽  
pp. 436-444 ◽  
Author(s):  
P. A. Fory ◽  
L. Triplett ◽  
C. Ballen ◽  
J. F. Abello ◽  
J. Duitama ◽  
...  
Keyword(s):  
Bacterial Species ◽  
Central American ◽  
Yield Reduction ◽  
Genotypic Differences ◽  
Rice Seed ◽  
Secretion Systems ◽  
Burkholderia Glumae ◽  
Phenotypic Differences ◽  
Genes Encoding ◽  
Inoculation Assay

Seed sterility and grain discoloration limit rice production in Colombia and several Central American countries. In samples of discolored rice seed grown in Colombian fields, the species Burkholderia glumae and B. gladioli were isolated, and field isolates were compared phenotypically. An artificial inoculation assay was used to determine that, although both bacterial species cause symptoms on rice grains, B. glumae is a more aggressive pathogen, causing yield reduction and higher levels of grain sterility. To identify putative virulence genes differing between B. glumae and B. gladioli, four previously sequenced genomes of Asian and U.S. strains of the two pathogens were compared with each other and with two draft genomes of Colombian B. glumae and B. gladioli isolates generated for this study. Whereas previously characterized Burkholderia virulence factors are highly conserved between the two species, B. glumae and B. gladioli strains are predicted to encode distinct groups of genes encoding type VI secretion systems, transcriptional regulators, and membrane-sensing proteins. This study shows that both B. glumae and B. gladioli can threaten grain quality, although only one species affects yield. Furthermore, genotypic differences between the two strains are identified that could contribute to disease phenotypic differences.

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