Blood Meal-Derived Heme Decreases ROS Levels in the Midgut of Aedes aegypti and Allows Proliferation of Intestinal Microbiota

Oliveira, José Henrique M.; Gonçalves, Renata L.S.; Lara, Flávio Alves; Dias, Felipe A.; Gandara, Ana Caroline P.; Menna-Barreto, Rubem F. S.; Edwards, Meredith; Laurindo, Francisco Rafael Martins; Silva-Neto, Mário A.C.; Sorgine, Marcos Henrique Ferreira; Oliveira, Pedro L.

doi:10.1371/journal.ppat.1001320

Cited by 227 publications

(261 citation statements)

References 55 publications

Supporting

Mentioning

244

Contrasting

Unclassified

Order By: Relevance

“…Our study reveals that the toxin oosporein specifically mediates down-regulation of Duox expression in the midgut, which reduces midgut ROS production. Duox-dependent ROS generation plays a major role in gut immunity and the control of gut-associated bacteria (24,46). In Drosophila, opportunistic pathogenic bacteria can be discriminated and controlled by triggering the Duox-dependent gut immunity (47,48).…”

Section: Discussionmentioning

confidence: 99%

Insect pathogenic fungus interacts with the gut microbiota to accelerate mosquito mortality

Lai

Wang

et al. 2017

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

238

201

View full text Add to dashboard Cite

The insect gut microbiota plays crucial roles in modulating the interactions between the host and intestinal pathogens. Unlike viruses, bacteria, and parasites, which need to be ingested to cause disease, entomopathogenic fungi infect insects through the cuticle and proliferate in the hemolymph. However, interactions between the gut microbiota and entomopathogenic fungi are unknown. Here we show that the pathogenic fungus Beauveria bassiana interacts with the gut microbiota to accelerate mosquito death. After topical fungal infection, mosquitoes with gut microbiota die significantly faster than mosquitoes without microbiota. Furthermore, fungal infection causes dysbiosis of mosquito gut microbiota with a significant increase in gut bacterial load and a significant decrease in bacterial diversity. In particular, the opportunistic pathogenic bacterium Serratia marcescens overgrows in the midgut and translocates to the hemocoel, which promotes fungal killing of mosquitoes. We further reveal that fungal infection down-regulates antimicrobial peptide and dual oxidase expression in the midgut. Duox down-regulation in the midgut is mediated by secretion of the toxin oosporein from B. bassiana. Our findings reveal the important contribution of the gut microbiota in B. bassiana-killing activity, providing new insights into the mechanisms of fungal pathogenesis in insects.

show abstract

Section: Discussionmentioning

confidence: 99%

Insect pathogenic fungus interacts with the gut microbiota to accelerate mosquito mortality

Lai

Wang

et al. 2017

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

238

201

View full text Add to dashboard Cite

show abstract

“…Furthermore, the intrinsic peroxidase activity of heme would make the coat a potent antioxidant barrier (25) and hence constitute a suitable protectant against reactive oxygen species (ROS) as key mediators of antimicrobial defense both in the arthropod gut (169,305) and as part of mammal immune defenses (42). ROS release in the arthropod gut is highly regulated, for example, in order to protect symbionts (168), and was found to be decreased in bloodsucking arthropods upon perception of heme in the gut lumen (319). Such a mechanism would potentially allow Bartonella not only to tolerate but also to prevent certain challenge by ROS, though no experimental data are available.…”

Section: Other Virulence Factorsmentioning

confidence: 99%

Intruders below the Radar: Molecular Pathogenesis of Bartonella spp

2012

View full text Add to dashboard Cite

SUMMARY Bartonella spp. are facultative intracellular pathogens that employ a unique stealth infection strategy comprising immune evasion and modulation, intimate interaction with nucleated cells, and intraerythrocytic persistence. Infections with Bartonella are ubiquitous among mammals, and many species can infect humans either as their natural host or incidentally as zoonotic pathogens. Upon inoculation into a naive host, the bartonellae first colonize a primary niche that is widely accepted to involve the manipulation of nucleated host cells, e.g., in the microvasculature. Consistently, in vitro research showed that Bartonella harbors an ample arsenal of virulence factors to modulate the response of such cells, gain entrance, and establish an intracellular niche. Subsequently, the bacteria are seeded into the bloodstream where they invade erythrocytes and give rise to a typically asymptomatic intraerythrocytic bacteremia. While this course of infection is characteristic for natural hosts, zoonotic infections or the infection of immunocompromised patients may alter the path of Bartonella and result in considerable morbidity. In this review we compile current knowledge on the molecular processes underlying both the infection strategy and pathogenesis of Bartonella and discuss their connection to the clinical presentation of human patients, which ranges from minor complaints to life-threatening disease.

show abstract

“…Blood feeding drastically influences microbial abundance and composition in mosquitoes (41)(42)(43). Given that we observed severe blood meal-associated fitness effects in Wolbachia-infected Anopheles, Wolbachia and Asaia levels were assessed in A. stephensi mosquitoes pre-and post-blood feeding.…”

Section: Microbiota-wolbachia Interactions Kill Mosquitoes After a Bloodmentioning

confidence: 99%

Native microbiome impedes vertical transmission of Wolbachia in Anopheles mosquitoes

Hughes¹,

Dodson²,

Johnson

et al. 2014

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

218

199

View full text Add to dashboard Cite

Significance Factors influencing Wolbachia transfer into new species remain poorly understood. This is important as Wolbachia can influence speciation and is being developed as a novel arthropod-borne disease control approach. We show the native microbiota of Anopheles impede vertical transmission of Wolbachia . Antibiotic microbiome perturbation enables Wolbachia transmission in two Anopheles species. Mosquitoes with altered microbiomes do not exhibit blood meal-induced mortality associated with Wolbachia infection, suggesting that mosquitoes are killed by interactions between Wolbachia and other bacteria present in the mosquito. We identified Asaia as the bacterium responsible for inhibiting Wolbachia transmission, and partially responsible for blood meal-induced mortality. These results suggest that microbial interactions profoundly affect the host, and that microbiome incompatibility may influence distribution of Wolbachia in arthropods.

show abstract

Blood Meal-Derived Heme Decreases ROS Levels in the Midgut of Aedes aegypti and Allows Proliferation of Intestinal Microbiota

Cited by 227 publications

References 55 publications

Insect pathogenic fungus interacts with the gut microbiota to accelerate mosquito mortality

Insect pathogenic fungus interacts with the gut microbiota to accelerate mosquito mortality

Intruders below the Radar: Molecular Pathogenesis of Bartonella spp

Native microbiome impedes vertical transmission of Wolbachia in Anopheles mosquitoes

Contact Info

Product

Resources

About