The virulence of Salmonella Enteritidis in Galleria mellonella is improved by N-dodecanoyl-homoserine lactone

Freitas, Leonardo Luiz de; Silva, Fernanda Pereira da; Fernandes, Kenner Morais; Carneiro, Deisy Guimarães; Oliveira, Leandro Licursi de; Martins, Gustavo Ferreira; Vanetti, Maria Cristina Dantas

doi:10.1016/j.micpath.2021.104730

Cited by 15 publications

(8 citation statements)

References 86 publications

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“…It is also possible that the priming event engages the innate response of the resident larval population of hemocytes, which are then unavailable to potentially control subsequent infection. Many studies have demonstrated the binding of bacterial pathogens to larval hemocytes and their subsequent uptake, for example recent studies with Yersinia pseudotuberculosis [69], Salmonella Enteritidis [70] and Coxiella burnetti [71]. In preliminary confocal experiments we did see an association of gonococci with hemocytes in extracted hemolymph (data not shown), but more detailed studies are necessary to examine these bacterial-larval innate cell interactions, and are outside the scope of the current manuscript.…”

Section: Discussionmentioning

confidence: 78%

Establishing an invertebrate Galleria mellonella greater wax moth larval model of Neisseria gonorrhoeae infection

et al. 2021

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Neisseria gonorrhoeae (gonococcus) causes the human sexually transmitted disease gonorrhea. Studying gonococcal pathogenesis and developing new vaccines and therapies to combat the increasing prevalence of multi-antibiotic resistant bacteria has made use of many ex vivo models based on human cells and tissues, and in vivo vertebrate models, for example, rodent, pig and human. The focus of the current study was to examine the utility of the invertebrate greater wax moth Galleria mellonella as an in vivo model of gonococcal infection. We observed that a threshold of ~10 6 -10 7 gonococci/larva was required to kill >50% of larvae (P < 0.05), and increased toxicity correlated with reduced health index scores and pronounced histopathological changes such as increases in the total lesion grade, melanized nodules, hemocyte reaction, and multifocal adipose body degeneration. Larval death was independent of the expression of pilus or Opa protein or LOS sialylation within a single gonococcal species studied, but the model could demonstrate relative toxicity of different isolates. N. meningitidis, N. lacatamica and gonococci all killed larvae equally, but were significantly less toxic (P > 0.05) than Pseudomonas aeruginosa. Larvae primed with nontoxic doses of gonococci were more susceptible to subsequent challenge with homologous and heterologous bacteria, and larval survival was significantly reduced (P < 0.05) in infected larvae after depletion of their hemocytes with clodronate-liposomes. The model was used to test the anti-gonococcal properties of antibiotics and novel antimicrobials. Ceftriaxone (P < 0.05) protected larvae from infection with different gonococcal isolates, but not azithromycin or monocaprin or ligand-coated silver nanoclusters (P > 0.05).

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Section: Discussionmentioning

confidence: 78%

Establishing an invertebrate Galleria mellonella greater wax moth larval model of Neisseria gonorrhoeae infection

et al. 2021

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“…This conclusion is consistent with prior studies in the American cockroach which speculated that hemocytes limit infection of the hemolymph by S. Typhimurium (Klowden and Greenberg 1977). In contrast, in the model G. mellonella , proliferation of S. Typhimurium in the hemolymph and within hemocytes is pronounced (Viegas et al 2013, Luiz de Freitas et al 2021, Silva et al 2021). S. Typhimurium can also establish intracellular infection in Drosophila melanogaster hemocytes (Brandt et al 2004, Shinzawa et al 2009).…”

Section: Discussionmentioning

confidence: 86%

Survival of Salmonella Typhimurium in the hemolymph of the German cockroach vector is limited by both humoral immune factors and hemocytes but not by trehalose metabolism

Turner,

Van Hulzen,

Peta

et al. 2023

Journal of Medical Entomology

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The German cockroach (Blattella germanica) has been linked to transmission of Salmonella enterica serovar Typhimurium (S. Typhimurium), but infection dynamics within this vector are poorly characterized. Our recent work has focused on S. Typhimurium infection in the cockroach gut. However, microbial dissemination to the hemolymph is an essential aspect of many vector-borne pathogen transmission cycles and could potentially contribute to S. Typhimurium colonization of cockroaches. Therefore, the goal of this study was to examine the ability of S. Typhimurium to disseminate, survive, and proliferate in the hemolymph of cockroaches after oral infection. We detected only low numbers of bacteria in the hemolymph of a minority of insects (~26%) after oral infection. Further, S. Typhimurium was unable to survive overnight in cell-free hemolymph. Several hypotheses to explain the inability of S. Typhimurium to colonize hemolymph were tested. First, we investigated the ability of S. Typhimurium to metabolize trehalose, the primary sugar in hemolymph. S. Typhimurium grew efficiently in vitro using trehalose as a sole carbon source and mutant strains lacking trehalose metabolism genes exhibited no growth deficiencies in media mimicking the composition of hemolymph, suggesting that trehalose metabolism ability is not a factor involved in restricting survival in hemolymph. On the other hand, heat-inactivated cell-free hemolymph was permissive of S. Typhimurium growth, demonstrating that survival in hemolymph is limited specifically by heat-labile humoral factors. The involvement of cellular immune responses was also investigated and cockroach hemocytes in culture were observed to internalize S. Typhimurium within 1 h of exposure. Most hemocytes harbored few to no bacteria after 24 h, indicating that hemocyte responses are additionally involved in clearing infection from the hemolymph. However, dense intracellular clusters of S. Typhimurium were observed sporadically, suggesting a small subset of hemocytes may serve as reservoirs for bacterial replication. Together, our results reveal that a minute proportion of ingested S. Typhimurium is able to escape the cockroach gut and enter the hemolymph, but this systemic population is limited by both humoral effectors and hemocytes. Thus, we conclude that invasion of the hemolymph appears minimally important for colonization of the cockroach vector and that colonization of the gut is the main driver of vector-borne transmission. Our insight into the antimicrobial mechanisms of cockroach hemolymph also highlights the strong ability of these prevalent pests/vectors to cope with frequent infectious challenges in septic habitats.

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“…These enzymes have been previously shown to act in sequence ( Oliveira et al., 2021 ). Additionally, population density and quorum sensing, as N-dodecanoyl-homoserine lactone, which played important roles in the regulation of SOD and CAT enzymes in Salmonella enteritidis ( Luiz de Freitas et al., 2021 ), and in response to herbicides, including the strain P. fluorescens CMA-55, studied in this work, in response to glyphosate ( Freitas et al., 2021 ).…”

Section: Resultsmentioning

confidence: 99%

Changes in fatty acid composition as a response to glyphosate toxicity in Pseudomonas fluorescens

Oliveira

Marchi

Emiliano

et al. 2022

Heliyon

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The virulence of Salmonella Enteritidis in Galleria mellonella is improved by N-dodecanoyl-homoserine lactone

Cited by 15 publications

References 86 publications

Establishing an invertebrate Galleria mellonella greater wax moth larval model of Neisseria gonorrhoeae infection

Establishing an invertebrate Galleria mellonella greater wax moth larval model of Neisseria gonorrhoeae infection

Survival of Salmonella Typhimurium in the hemolymph of the German cockroach vector is limited by both humoral immune factors and hemocytes but not by trehalose metabolism

Changes in fatty acid composition as a response to glyphosate toxicity in Pseudomonas fluorescens

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