Virulence factors of the human opportunistic pathogen Serratia marcescens identified by in vivo screening

Kurz, C. Léopold; Chauvet, Sophie; Andrès, Emmanuel; Aurouze, Marianne; Vallet-Gély, Isabelle; Michel, Gérard; Uh, Mitch; Celli, Jean; Filloux, Alain; Bentzmann, Sophie de; Steinmetz, Ivo; Hoffmann, Jules A.; Finlay, B. Brett; Gorvel, Jean‐Pierre; Ferrandon, Dominique; Ewbank, Jonathan J.

doi:10.1093/emboj/cdg159

Cited by 322 publications

(314 citation statements)

References 52 publications

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“…For our parasite, we used S. marcescens , a virulent bacterium that infects many plant and animal species (Grimont & Grimont, 1978). The C. elegans – S. marcescens interaction has been used to study the genetics of parasite infectivity, host resistance, and host avoidance behavior (Kurz et al., 2003; Mallo et al., 2002; Pradel et al., 2007; Schulenburg & Ewbank, 2004). …”

Section: Methodsmentioning

confidence: 99%

Turnover in local parasite populations temporarily favors host outcrossing over self‐fertilization during experimental evolution

Lynch

Penley

Morran

2018

Ecology and Evolution

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The ubiquity of outcrossing in plants and animals is difficult to explain given its costs relative to self‐fertilization. Despite these costs, exposure to changing environmental conditions can temporarily favor outcrossing over selfing. Therefore, recurring episodes of environmental change are predicted to favor the maintenance of outcrossing. Studies of host–parasite coevolution have provided strong support for this hypothesis. However, it is unclear whether multiple exposures to novel parasite genotypes in the absence of coevolution are sufficient to favor outcrossing. Using the nematode Caenorhabditis elegans and the bacterial parasite Serratia marcescens, we studied host responses to parasite turnover. We passaged several replicates of a host population that was well‐adapted to the S. marcescens strain Sm2170 with either Sm2170 or one of three novel S. marcescens strains, each derived from Sm2170, for 18 generations. We found that hosts exposed to novel parasites maintained higher outcrossing rates than hosts exposed to Sm2170. Nonetheless, host outcrossing rates declined over time against all but the most virulent novel parasite strain. Hosts exposed to the most virulent novel strain exhibited increased outcrossing rates for approximately 12 generations, but did not maintain elevated levels of outcrossing throughout the experiment. Thus, parasite turnover can transiently increase host outcrossing. These results suggest that recurring episodes of parasite turnover have the potential to favor the maintenance of host outcrossing. However, such maintenance may require frequent exposure to novel virulent parasites, rapid rates of parasite turnover, and substantial host gene flow.

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Section: Methodsmentioning

confidence: 99%

Turnover in local parasite populations temporarily favors host outcrossing over self‐fertilization during experimental evolution

Lynch

Penley

Morran

2018

Ecology and Evolution

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“…Although mouse models have been used for these purposes, simpler invertebrates such as Caenorhabditis elegans have recently become more attractive for assessing the in vivo biological costs of antibiotic resistance (23,24). Many bacterial genes known to be required for mammalian pathogenesis are needed also in the nematode (1,9,11,15,16,27,28). Some bacterial pathogens, such as Salmonella enterica serovar Typhimurium are able to establish a persistent infection in the intestine of C. elegans, reducing the life span of the host.…”

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confidence: 99%

Caenorhabditis elegans as a Model To Determine Fitness of Antibiotic-Resistant Salmonella enterica Serovar Typhimurium

Paulander

Pennhag

Andersson

et al. 2007

Antimicrob Agents Chemother

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We used the ability of Salmonella enterica serovar Typhimurium to colonize the gut of Caenorhabditis elegans to measure the fitness costs imposed by antibiotic resistance mutations. The fitness costs determined in the nematode were similar to those measured in mice, validating its use as a simple host model to evaluate bacterial fitness.The persistence of antibiotic-resistant bacteria largely depends on the effect of the resistance mechanism on fitness (reviewed in references 3 and 4). The cost caused by resistance mutations can be decreased by second-site mutations that restore fitness without a loss of resistance (3,17,18). This process has been observed in many cases both in vitro (13,17,19,22,25) and in clinical settings (6,8,20,26). These findings suggest that antibiotic resistance may persist in the population for a long time and that the determination of fitness parameters is of great importance for predicting the risk of resistance development.Fitness costs are usually determined by comparing the growth rates of resistant and susceptible bacteria (3). Although mouse models have been used for these purposes, simpler invertebrates such as Caenorhabditis elegans have recently become more attractive for assessing the in vivo biological costs of antibiotic resistance (23, 24). Many bacterial genes known to be required for mammalian pathogenesis are needed also in the nematode (1,9,11,15,16,27,28). Some bacterial pathogens, such as Salmonella enterica serovar Typhimurium are able to establish a persistent infection in the intestine of C. elegans, reducing the life span of the host. Several genes needed for virulence in mammals are also required for pathogenesis in C. elegans (2,10,16,28), implying that the invasion and proliferation of serovar Typhimurium in the host intestine depend on mechanisms common to the nematode and mammals. This makes C. elegans a relevant model for determining the infectivity and fitness of antibiotic-resistant bacteria during a host infection.Virulence assays were performed as previously described (2) using C. elegans SS104 [glp-4 (ts)] (5), a temperature-sensitive mutant that produces progeny at 15°C but not at 25°C. At least 50 synchronized worms in larval stage L4 were transferred on solid nematode growth medium (NGM) (12) seeded with 10 l of serovar Typhimurium mixed 1:100 with the nonpathogenic Escherichia coli strain OP50 and maintained at 25°C. Both bacterial species grow on NGM agar with no mutual inhibition. The number of viable worms was monitored every day, and the percentages of nematode survival calculated by the KaplanMeier method (14) were used for plotting the percent survival as a function of time. Survival kinetics were compared by using the nonparametric log-rank test and were considered statistically different when P was Ͻ0.05. We found that the time to death for 50% of the nematodes was 9 days when fed with E. coli OP50 and 7 days after ingestion of the virulent wild-type strain LT2 of serovar Typhimurium (Fig. 1). As previously shown, the glp-4 (ts) strain resp...

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“…Proteases are a known virulence factor in S. marcescens as well as in other pathogen species (e.g. Bidochka & Khachatourians 1990, Kurz et al 2003, Liehl et al 2006. They are especially important for parasites in penetrating the insect gut membrane or even the outer cuticle of the body (Bidochka & Khachatourians 1990, Abuhatab et al 1995, Ffrench-Constant et al 2003.…”

Section: Discussionmentioning

confidence: 99%

Lepidopteran species have a variety of defence strategies against bacterial infections

Mikonranta

Dickel

Mappes

et al. 2017

Journal of Invertebrate Pathology

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Virulence factors of the human opportunistic pathogen Serratia marcescens identified by in vivo screening

Cited by 322 publications

References 52 publications

Turnover in local parasite populations temporarily favors host outcrossing over self‐fertilization during experimental evolution

Turnover in local parasite populations temporarily favors host outcrossing over self‐fertilization during experimental evolution

Caenorhabditis elegans as a Model To Determine Fitness of Antibiotic-Resistant Salmonella enterica Serovar Typhimurium

Lepidopteran species have a variety of defence strategies against bacterial infections

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