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Acinetobacter baumannii utilizes a type VI secretion system for bacterial competition.

ABSTRACT: Type VI secretion systems (T6SS) are a class of macromolecular secretion machines that are utilized by a number of bacteria for inter-bacterial competition or to elicit responses in eukaryotic cells. Acinetobacter baumannii is an opportunistic pathogen that causes severe infections in humans. These infections, including pneumonia and bacteremia, are important, as they are often associated with hospitals and medical-settings where they disproportionally affect critically ill patients like those residing in intensive care units. While it is known that A. baumannii genomes carry genes whose predicted products have homology with T6SS-associated gene products from other bacteria, and secretion of a major T6SS structural protein Hcp has been demonstrated, no additional work on an A. baumannii T6SS has been reported. Herein, we demonstrated that A. baumannii strain M2 secretes Hcp and this secretion was dependent upon TssB, an ortholog of a bacteriophage contractile sheath protein, confirming that strain M2 produces a functional T6SS. Additionally, we demonstrated that the ability of strain M2 to out-compete Escherichia coli was reliant upon the products of tssB and hcp. Collectively, our data have provided the first evidence demonstrating function in inter-bacterial competition, for a T6SS produced by A. baumannii.

SUBMITTER: Carruthers MD

PROVIDER: S-EPMC3602014 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Acinetobacter baumannii utilizes a type VI secretion system for bacterial competition.

Carruthers Michael D MD Nicholson Paul A PA Tracy Erin N EN Munson Robert S RS

PloS one 20130319 3

Type VI secretion systems (T6SS) are a class of macromolecular secretion machines that are utilized by a number of bacteria for inter-bacterial competition or to elicit responses in eukaryotic cells. Acinetobacter baumannii is an opportunistic pathogen that causes severe infections in humans. These infections, including pneumonia and bacteremia, are important, as they are often associated with hospitals and medical-settings where they disproportionally affect critically ill patients like those r ...[more]

PMID: 23527179

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Project description:Protein secretion systems are crucial mediators of bacterial interactions with other organisms. Among them, the type VI secretion system (T6SS) is widespread in Gram-negative bacteria and appears to inject toxins into competitor bacteria and/or eukaryotic cells. Major human pathogens, such as Vibrio cholerae, Burkholderia and Pseudomonas aeruginosa, express T6SSs. Bacteria prevent self-intoxication by their own T6SS toxins by producing immunity proteins, which interact with the cognate toxins. We describe here an environmental P. fluorescens strain, MFE01, displaying an uncommon oversecretion of Hcp (hemolysin-coregulated protein) and VgrG (valine-glycine repeat protein G) into the culture medium. These proteins are characteristic components of a functional T6SS. The aim of this study was to attribute a role to this energy-consuming overexpression of the T6SS. The genome of MFE01 contains at least two hcp genes (hcp1 and hcp2), suggesting that there may be two putative T6SS clusters. Phenotypic studies have shown that MFE01 is avirulent against various eukaryotic cell models (amebas, plant or animal cell models), but has antibacterial activity against a wide range of competitor bacteria, including rhizobacteria and clinical bacteria. Depending on the prey cell, mutagenesis of the hcp2 gene in MFE01 abolishes or reduces this antibacterial killing activity. Moreover, the introduction of T6SS immunity proteins from S. marcescens, which is not killed by MFE01, protects E. coli against MFE01 killing. These findings suggest that the protein encoded by hcp2 is involved in the killing activity of MFE01 mediated by effectors of the T6SS targeting the peptidoglycan of Gram-negative bacteria. Our results indicate that MFE01 can protect potato tubers against Pectobacterium atrosepticum, which causes tuber soft rot. Pseudomonas fluorescens is often described as a major PGPR (plant growth-promoting rhizobacterium), and our results suggest that there may be a connection between the T6SS and the PGPR properties of this bacterium.

Project description:Many Gram-negative bacteria use a type VI secretion system (T6SS) for microbial warfare and/or host manipulation. Acinetobacter baumannii is an important nosocomial pathogen and many A. baumannii strains utilize a T6SS to deliver toxic effector proteins to surrounding bacterial cells. These toxic effectors are usually delivered together with VgrG proteins, which form part of the T6SS tip complex. All previously identified A. baumannii T6SS effectors are encoded within a three- or four-gene locus that also encodes a cognate VgrG and immunity protein, and sometimes a chaperone. In order to characterize the diversity and distribution of T6SS effectors and immunity proteins in this species, we first identified all vgrG genes in 97 A. baumannii strains via the presence of the highly conserved VgrG domain. Most strains encoded between two and four different VgrG proteins. We then analyzed the regions downstream of the identified vgrG genes and identified more than 240 putative effectors. The presence of conserved domains in these effectors suggested a range of functions, including peptidoglycan hydrolases, lipases, nucleases, and nucleic acid deaminases. However, 10 of the effector groups had no functionally characterized domains. Phylogenetic analysis of these putative effectors revealed that they clustered into 32 distinct groups that appear to have been acquired from a diverse set of ancestors. Corresponding immunity proteins were identified for all but two of the effector groups. Effectors from eight of the 32 groups contained N-terminal rearrangement hotspot (RHS) domains. The C-terminal regions of these RHS proteins, which are predicted to confer the toxic effector function, were very diverse, but the N-terminal RHS domains clustered into just two groups. While the majority of A. baumannii strains contained an RHS type effector, no strains encoded two RHS effectors with similar N-terminal sequences, suggesting that the presence of similar N-terminal RHS domains leads to competitive exclusion. Together, these analyses define the extreme diversity of T6SS effectors within A. baumannii and, as many have unknown functions, future detailed characterization of these effectors may lead to the identification of proteins with novel antibacterial properties.

Project description:Pathogenic bacteria of the Acinetobacter genus pose a severe threat to human health worldwide due to their strong adaptability, tolerance, and antibiotic resistance. Most isolates of these bacteria harbor a type VI secretion system (T6SS) that allows them to outcompete co-residing microorganisms, but whether this system is involved in acquiring nutrients from preys remains less studied. In this study, we found that Ab25, a clinical isolate of Acinetobacter nosocomialis, utilizes a T6SS to kill taxonomically diverse microorganisms, including bacteria and fungi. The T6SS of Ab25 is constitutively expressed, and among the three predicted effectors, T6e1, a member of the RHS effector family, contributes the most for its antimicrobial activity. T6e1 undergoes self-cleavage, and a short carboxyl fragment with nuclease activity is sufficient to kill target cells via T6SS injection. Interestingly, strain Ab25 encodes an orphan VgrG protein, which when overexpressed blocks the firing of its T6SS. In niches such as dry plastic surfaces, the T6SS promotes prey microorganism-dependent survival of Ab25. These results reveal that A. nosocomialis employs T6SSs that are highly diverse in their regulation and effector composition to gain a competitive advantage in environments with scarce nutrient supply and competing microbes.IMPORTANCEThe type VI secretion system (T6SS) plays an important role in bacterial adaptation to environmental challenges. Members of the Acinetobacter genus, particularly A. baumannii and A. nosocomialis, are notorious for their multidrug resistance and their ability to survive in harsh environments. In contrast to A. baumannii, whose T6SS has been well-studied, few research works have focused on A. nosocomialis. In this study, we found that an A. nosocomialis strain utilizes a contitutively active T6SS to kill diverse microorganisms, including bacteria and fungi. Although T6SS structural proteins of A. nosocomialis are similar to those of A. baumannii, the effector repertoire differs greatly. Interestingly, the T6SS of the A. nosocomialis strain codes for an ophan VgrG protein, which blocks the firing of the system when overexpressed, suggesting the existence of a new regulatory mechanism for the T6SS. Importantly, although the T6SS does not provide an advantage when the bacterium is grown in nutrient-rich medium, it allows A. nosocomialis to survive better in dry surfaces that contain co-existing bacteria. Our results suggest that killing of co-residing microorganisms may increase the effectiveness of strategies designed to reduce the fitness of Acinetobacter bacteria by targeting their T6SS.

Dataset Information

Acinetobacter baumannii utilizes a type VI secretion system for bacterial competition.

Publications

Acinetobacter baumannii utilizes a type VI secretion system for bacterial competition.

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