Quantitative single-cell characterization of bacterial interactions reveals type VI secretion is a double-edged sword

LeRoux, Michele; Leon, Justin A. De; Kuwada, Nathan J.; Russell, Alan D.; Pinto-Santini, Delia; Hood, Rachel D.; Agnello, Danielle M.; Robertson, Stephen M.; Wiggins, Paul A.; Mougous, Joseph D.

doi:10.1073/pnas.1213963109

Cited by 87 publications

(113 citation statements)

References 35 publications

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“…By comparison, Xac cell lysis was very rarely observed in these experiments. The rapid and violent cell death that we observe contrasts with that which has been reported for T6SS-mediated killing by Pseudomonas aeruginosa, in which target cells change their morphology (cell rounding, blebbing and plasmolysis) over a period of many minutes before lysis 29,30 .…”

Section: Resultscontrasting

confidence: 53%

“…We have provided evidence that the Xac T4SS, and by extension its homologues in other Xanthomonadaceae species, target toxins (X-Tfes or XVIPs) to bacterial cells, thereby providing Xanthomonas an advantage to survive in an environment populated by a number of different bacterial species in a manner similar to that recently described for several T6SSs [29][30][31][32][33] . Using the presence of a XVIPCD as search criteria, we have identified 500 potential X-Tfes in the public databases, of which all but two are derived from members of the Xanthomonadaceae family (Table 1).…”

Section: Discussionmentioning

confidence: 79%

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Bacterial killing via a type IV secretion system

et al. 2015

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Section: Resultscontrasting

confidence: 53%

Section: Discussionmentioning

confidence: 79%

Bacterial killing via a type IV secretion system

et al. 2015

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“…Third, our experiments used T6S-negative recipient populations. P. aeruginosa cells display an elevated propensity to activate T6S in response to a T6S attack (24,25). Although this phenomenon has not been investigated in Bacteroides, the S strain and 14-species community in these experiments are T6S-negative and would not induce this increased transmission rate that may occur between T6S-positive (D) individuals.…”

Section: Discussionmentioning

confidence: 89%

“…Second, the model assumes that a single effector transmission event into an S individual results in the death and subsequent removal of that individual from the population. However, if some proportion of transmission events into S cells does not result in the death of the recipient, then those individuals will not be removed from the population, representing transmission events that do not produce an observable change in S. Indeed, in vitro studies of the opportunistic proteobacterial pathogen Pseudomonas aeruginosa suggest that its T6SS kills recipient cells at rates of ∼5% or less per hour of contact (24). Third, our experiments used T6S-negative recipient populations.…”

Section: Discussionmentioning

confidence: 99%

Human symbionts inject and neutralize antibacterial toxins to persist in the gut

Wexler

Bao

Whitney

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The human gut microbiome is a dynamic and densely populated microbial community that can provide important benefits to its host. Cooperation and competition for nutrients among its constituents only partially explain community composition and interpersonal variation. Notably, certain human-associated Bacteroidetes—one of two major phyla in the gut—also encode machinery for contact-dependent interbacterial antagonism, but its impact within gut microbial communities remains unknown. Here we report that prominent human gut symbionts persist in the gut through continuous attack on their immediate neighbors. Our analysis of just one of the hundreds of species in these communities reveals 12 candidate antibacterial effector loci that can exist in 32 combinations. Through the use of secretome studies, in vitro bacterial interaction assays and multiple mouse models, we uncover strain-specific effector/immunity repertoires that can predict interbacterial interactions in vitro and in vivo, and find that some of these strains avoid contact-dependent killing by accumulating immunity genes to effectors that they do not encode. Effector transmission rates in live animals can exceed 1 billion events per minute per gram of colonic contents, and multiphylum communities of human gut commensals can partially protect sensitive strains from these attacks. Together, these results suggest that gut microbes can determine their interactions through direct contact. An understanding of the strategies human gut symbionts have evolved to target other members of this community may provide new approaches for microbiome manipulation.

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“…Thus, elucidating the formation of these gradients at early stages of microcolony development may help us to understand better the mechanisms responsible for physiological heterogeneities in biofilms and their role in pathogenicity. Contact-dependent interactions between bacteria are known to operate via tube-like secretion systems that bridge the periplasms of two neighboring bacteria (45)(46)(47). In contrast, Pvd must diffuse in the environment to chelate iron.…”

Section: Discussionmentioning

confidence: 99%

Cell–cell contacts confine public goods diffusion inside Pseudomonas aeruginosa clonal microcolonies

Julou

Mora

Guillon

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

133

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The maintenance of cooperation in populations where public goods are equally accessible to all but inflict a fitness cost on individual producers is a long-standing puzzle of evolutionary biology. An example of such a scenario is the secretion of siderophores by bacteria into their environment to fetch soluble iron. In a planktonic culture, these molecules diffuse rapidly, such that the same concentration is experienced by all bacteria. However, on solid substrates, bacteria form dense and packed colonies that may alter the diffusion dynamics through cell-cell contact interactions. In Pseudomonas aeruginosa microcolonies growing on solid substrate, we found that the concentration of pyoverdine, a secreted iron chelator, is heterogeneous, with a maximum at the center of the colony. We quantitatively explain the formation of this gradient by local exchange between contacting cells rather than by global diffusion of pyoverdine. In addition, we show that this local trafficking modulates the growth rate of individual cells. Taken together, these data provide a physical basis that explains the stability of public goods production in packed colonies.biofilm | evolution | noise | variability | ecology I ron is required for many enzymatic processes, and is therefore an essential nutrient. To overcome the low abundance of free iron in aerobic environments, bacteria, as well as other microorganisms, synthesize and secrete iron-chelating molecules called siderophores (1). Once released in the extracellular environment, siderophores diffuse and complex with iron. Because other bacteria can import them, siderophores can be regarded as public goods (2) and siderophore secretion is often cited as a model system for studying the stability of cooperation (3, 4). In this context, nonproducing mutants, which can enjoy the benefit of siderophores without bearing the cost of their production, have a selective advantage over the WT-producing strain and could, in principle, displace them on evolutionary time scales.This argument usually assumes that public good molecules are readily available to all, as is the case in planktonic cultures, where molecules diffuse freely and rapidly between cells. In liquid conditions, mutants that do not produce siderophores have, in fact, been shown to outcompete WT strains (5-8). However, the limited spatial dispersal of public goods can challenge this picture and has been proposed as a general mechanism for explaining the maintenance of cooperation (8-12). When dispersal is limited, public good molecules tend to stay in the vicinity of the producing subpopulations, allowing them to benefit preferentially from their own production, and thus to balance the advantage of opportunistic nonproducing strains. In many ecological situations, bacteria form complex, tightly packed, and spatially structured colonies, such as biofilms, where public good dispersal may be severely reduced compared with planktonic cultures. This raises the questions of how public good molecules circulate between cells in these natur...

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Quantitative single-cell characterization of bacterial interactions reveals type VI secretion is a double-edged sword

Cited by 87 publications

References 35 publications

Bacterial killing via a type IV secretion system

Bacterial killing via a type IV secretion system

Human symbionts inject and neutralize antibacterial toxins to persist in the gut

Cell–cell contacts confine public goods diffusion inside Pseudomonas aeruginosa clonal microcolonies

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