Exposure of Anopheles mosquitoes to trypanosomes reduces reproductive fitness and enhances susceptibility to Plasmodium

Dieme, Constentin; Zmarlak, Natalia Marta; Brito-Fravallo, Emma; Travaillé, Christelle; Pain, Adrien; Cherrier, Floriane; Genève, Corinne; Calvo-Álvarez, Estefanía; Riehle, Michelle M.; Vernick, Kenneth D.; Rotureau, Brice; Mitri, Christian

doi:10.1371/journal.pntd.0008059

Cited by 11 publications

(11 citation statements)

References 56 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In African mosquitoes (Anopheles coluzzii) that become infected with trypanosomes, Trypanosoma brucei, qPCR revealed a five-fold increase in the total enteric bacterial population within two days after infection and again after a blood meal. The effects were similar regardless of the blood source [66]. The intensity of Plasmodium infection in its mosquito host also may be directly correlated with the abundance of midgut Enterobacteriaceae populations.…”

Section: How Do the Microbial Symbionts Affect Vector Health And Reproduction And Contribute To Fitness Of The Vector Host?mentioning

confidence: 79%

Microbiomes of Blood-Feeding Arthropods: Genes Coding for Essential Nutrients and Relation to Vector Fitness and Pathogenic Infections. A Review

Sonenshine

Stewart

2021

Microorganisms

View full text Add to dashboard Cite

Background: Blood-feeding arthropods support a diverse array of symbiotic microbes, some of which facilitate host growth and development whereas others are detrimental to vector-borne pathogens. We found a common core constituency among the microbiota of 16 different arthropod blood-sucking disease vectors, including Bacillaceae, Rickettsiaceae, Anaplasmataceae, Sphingomonadaceae, Enterobacteriaceae, Pseudomonadaceae, Moraxellaceae and Staphylococcaceae. By comparing 21 genomes of common bacterial symbionts in blood-feeding vectors versus non-blooding insects, we found that certain enteric bacteria benefit their hosts by upregulating numerous genes coding for essential nutrients. Bacteria of blood-sucking vectors expressed significantly more genes (p < 0.001) coding for these essential nutrients than those of non-blooding insects. Moreover, compared to endosymbionts, the genomes of enteric bacteria also contained significantly more genes (p < 0.001) that code for the synthesis of essential amino acids and proteins that detoxify reactive oxygen species. In contrast, microbes in non-blood-feeding insects expressed few gene families coding for these nutrient categories. We also discuss specific midgut bacteria essential for the normal development of pathogens (e.g., Leishmania) versus others that were detrimental (e.g., bacterial toxins in mosquitoes lethal to Plasmodium spp.).

show abstract

Section: How Do the Microbial Symbionts Affect Vector Health And Reproduction And Contribute To Fitness Of The Vector Host?mentioning

confidence: 79%

Microbiomes of Blood-Feeding Arthropods: Genes Coding for Essential Nutrients and Relation to Vector Fitness and Pathogenic Infections. A Review

Sonenshine

Stewart

2021

Microorganisms

View full text Add to dashboard Cite

show abstract

“…Yet, the organism displays the hallmarks of a parasitic infection as oocysts are ingested from the larval water, enter epithelial cells, and use host cell mitochondria to supply the energy required to mature ( Chen and Wu, 1997 ). Trypanosoma brucei , a protist parasite and causative agent of trypanosomiases, normally carried by tsetse flies, can survive in mosquito midguts for up to 48 h. Co-infection of mosquitoes with Trypanosoma and Plasmodium increased the malarial parasite load in the mosquito, potentially increasing the risk of malarial spread ( Dieme et al, 2020 ). Thus, there is evidence that the microbiome of the mosquito may host a population of protists, but their roles and interactions with the host are essentially undescribed.…”

Section: A Path Forward: a Most Wanted List For Microbes In Gnotobiotic Studiesmentioning

confidence: 99%

The Axenic and Gnotobiotic Mosquito: Emerging Models for Microbiome Host Interactions

et al. 2021

View full text Add to dashboard Cite

The increasing availability of modern research tools has enabled a revolution in studies of non-model organisms. Yet, one aspect that remains difficult or impossible to control in many model and most non-model organisms is the presence and composition of the host-associated microbiota or the microbiome. In this review, we explore the development of axenic (microbe-free) mosquito models and what these systems reveal about the role of the microbiome in mosquito biology. Additionally, the axenic host is a blank template on which a microbiome of known composition can be introduced, also known as a gnotobiotic organism. Finally, we identify a “most wanted” list of common mosquito microbiome members that show the greatest potential to influence host phenotypes. We propose that these are high-value targets to be employed in future gnotobiotic studies. The use of axenic and gnotobiotic organisms will transition the microbiome into another experimental variable that can be manipulated and controlled. Through these efforts, the mosquito will be a true model for examining host microbiome interactions.

show abstract

“…Instead, our findings may suggest a second model in which sensing pathogen infection leads to the induction of genes that play a role in surveillance and resistance to possible coinfecting pathogens. Coinfections are commonly observed in natural populations of various species [93–95]. It has been demonstrated that coinfection can lead to decreased host resistance in nature and laboratory experiments [95–97], and negatively impact host health [94, 98].…”

Section: Discussionmentioning

confidence: 99%

“…Coinfections are commonly observed in natural populations of various species [93–95]. It has been demonstrated that coinfection can lead to decreased host resistance in nature and laboratory experiments [95–97], and negatively impact host health [94, 98]. These previous findings suggest that avoidance of coinfection would increase host fitness, and support a model in which infection by any pathogen may provoke a generalized prophylactic response against coinfection alongside the specific response to the primary pathogen.…”

Section: Discussionmentioning

confidence: 99%

Meta-analysis of immune induced gene expression changes in diverse Drosophila melanogaster innate immune responses

Waring

Hill

Allen

et al. 2021

Preprint

View full text Add to dashboard Cite

Background: Organisms are commonly infected by a diverse array of pathogen types including bacteria, fungi, viruses, and parasites, and mount functionally distinct responses to each of these varied immune challenges. Host immune responses are characterized by the induction of gene expression in response to infection. However, the extent to which expression changes are shared among responses to distinct pathogens is largely unknown. Results: We performed meta-analysis of gene expression data collected from Drosophila melanogaster following infection with a wide array of pathogens. We identified 62 genes that are significantly induced by infection. While many of these infection-induced genes encode known immune response factors, we also identified 21 genes that have not been previously associated with host immunity. Examination of the upstream flanking sequences of the infection-induced genes lead to the identification of two conserved enhancer sites. These sites correspond to conserved binding sites for GATA and nuclear factor κB (NFκB) family transcription factors and are associated with higher levels of transcript induction. We further identified 31 genes with predicted functions in metabolism and organismal development that are significantly downregulated following infection by diverse pathogens. Conclusions: Our study identifies conserved gene expression changes in Drosophila melanogaster following infection with varied pathogens, and transcription factor families that may regulate this immune induction. These findings provide new insight into transcriptional changes that accompany Drosophila immunity. They may suggest possible roles for the differentially regulated genes in innate immune responses to diverse classes of pathogens, and serve to identify candidate genes for further empirical study of these processes.

show abstract

Exposure of Anopheles mosquitoes to trypanosomes reduces reproductive fitness and enhances susceptibility to Plasmodium

Abstract: During a blood meal,

Cited by 11 publications

References 56 publications

Microbiomes of Blood-Feeding Arthropods: Genes Coding for Essential Nutrients and Relation to Vector Fitness and Pathogenic Infections. A Review

Microbiomes of Blood-Feeding Arthropods: Genes Coding for Essential Nutrients and Relation to Vector Fitness and Pathogenic Infections. A Review

The Axenic and Gnotobiotic Mosquito: Emerging Models for Microbiome Host Interactions

Meta-analysis of immune induced gene expression changes in diverse Drosophila melanogaster innate immune responses

Contact Info

Product

Resources

About