Tripartite interactions: Leishmania, microbiota and Lutzomyia longipalpis

Campolina, Thaís Bonifácio; Villegas, Luis Eduardo Martínez; Monteiro, Carolina Cunha; Pimenta, Paulo Filemon Paolucci; Secundino, Nágila Francinete Costa

doi:10.1371/journal.pntd.0008666

Cited by 24 publications

(29 citation statements)

References 58 publications

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“…An Erwinia species from D. radicum larval gut is highly resistant to isothiocyanate compounds [ 53 ], which are toxic to herbivorous insects [ 54 ] and are emitted by plants as a defense [ 55 ]. While Erwinia protect Lutzomyia longipalpis sandflies against parasitism by Leishmania [ 56 ], they are on the contrary pathogenic for their pea aphids hosts Acyrthosiphon pisum [ 57 , 58 ]. Similarly to our study, Wolbachia and Erwinia seem strikingly unable to cohabit in pea aphids [ 59 ] or in D. radicum adult flies [ 32 , 50 ].…”

Section: Discussionmentioning

confidence: 99%

“…The abundance of the seven other bacteria negatively correlated to Wolbachia infection was far less drastically impacted than that of Erwinia , and these bacteria often play positive roles in their insect hosts. The Bacilli Staphylococcus reduces parasitism by Leishmania in sandflies [ 56 ] and also frequently occurs in the order of Lepidoptera, where it may overcome plant protease inhibitor defenses [ 14 ]. The Bacteroidia Flavobacterium helps digesting plant material by producing cellulase in three phytophagous insect species [ 52 ] while Sphingobacterium induces resistance against fungal infection in Delia antiqua larvae [ 66 ].…”

Section: Discussionmentioning

confidence: 99%

“…We demonstrated that Wolbachia was positively correlated to Providencia and Serratia . The γ-proteobacterial Providencia is resistant to plant defense isothiocyanates [ 53 ] and might provide protection to the host gut, where it might also reduce parasite abundance [ 56 ]. Serratia has various functions that could clearly benefit the host—such as producing cellulase [ 52 ], resisting plant defenses [ 53 ], promoting the host resistance against parasites [ 56 ] and fungi [ 66 ]—but it can also be entomopathogenic [ 76 ].…”

Section: Discussionmentioning

confidence: 99%

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Influential Insider: Wolbachia, an Intracellular Symbiont, Manipulates Bacterial Diversity in Its Insect Host

et al. 2021

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Facultative intracellular symbionts like the α-proteobacteria Wolbachia influence their insect host phenotype but little is known about how much they affect their host microbiota. Here, we quantified the impact of Wolbachia infection on the bacterial community of the cabbage root fly Delia radicum by comparing the microbiota of Wolbachia-free and infected adult flies of both sexes. We used high-throughput DNA sequencing (Illumina MiSeq, 16S rRNA, V5-V7 region) and performed a community and a network analysis. In both sexes, Wolbachia infection significantly decreased the diversity of D. radicum bacterial communities and modified their structure and composition by reducing abundance in some taxa but increasing it in others. Infection by Wolbachia was negatively correlated to 8 bacteria genera (Erwinia was the most impacted), and positively correlated to Providencia and Serratia. We suggest that Wolbachia might antagonize Erwinia for being entomopathogenic (and potentially intracellular), but would favor Providencia and Serratia because they might protect the host against chemical plant defenses. Although they might seem prisoners in a cell, endocellular symbionts can impact the whole microbiota of their host, hence its extended phenotype, which provides them with a way to interact with the outside world.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Influential Insider: Wolbachia, an Intracellular Symbiont, Manipulates Bacterial Diversity in Its Insect Host

et al. 2021

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“…A recent 16S rRNA sequence profiling of the gut microbiota from Lutzomyia longipalpis, the primary vector of VL in Brazil, revealed 13 distinct bacterial genera (Bacillus, Enterococcus, Erwinia, Enterobacter, Escherichia, Klebsiella, Lysinibacillus, Pseudocitrobacter, Providencia, Pseudomonas, Serratia, Staphylococcus, and Solibacillus) (Campolina et al, 2020).…”

Section: Sandfly Vector Transcriptomicsmentioning

confidence: 99%

Advances in Understanding Leishmania Pathobiology: What Does RNA-Seq Tell Us?

Salloum

Tokajian

Hirt

2021

Front. Cell Dev. Biol.

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Leishmaniasis is a vector-borne disease caused by a protozoa parasite from over 20 Leishmania species. The clinical manifestations and the outcome of the disease vary greatly. Global RNA sequencing (RNA-Seq) analyses emerged as a powerful technique to profile the changes in the transcriptome that occur in the Leishmania parasites and their infected host cells as the parasites progresses through their life cycle. Following the bite of a sandfly vector, Leishmania are transmitted to a mammalian host where neutrophils and macrophages are key cells mediating the interactions with the parasites and result in either the elimination the infection or contributing to its proliferation. This review focuses on RNA-Seq based transcriptomics analyses and summarizes the main findings derived from this technology. In doing so, we will highlight caveats in our understanding of the parasite’s pathobiology and suggest novel directions for research, including integrating more recent data highlighting the role of the bacterial members of the sandfly gut microbiota and the mammalian host skin microbiota in their potential role in influencing the quantitative and qualitative aspects of leishmaniasis pathology.

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“…Several studies with phlebotomines from America have also demonstrated the importance and potential role of intestinal microbiota in susceptibility and competence in developing Leishmania infection [2]. Recently, in vivo trials of Lutzomyia longipalpis coinfection with different Leishmania species and bacterial isolates (Lysinibacillus, Serratia, and Pseudocitrobacter) reported significant differences, suggesting a powerful effect on inhibiting Leishmania survival, and causing the death of promastigotes in a few hours or days [4]. Other studies showed that bacterial richness and diversity progressively decreased in Leishmania infantum-infected sand flies as the parasite numbers increased [3].…”

Section: Introductionmentioning

confidence: 99%

Gut Microbiota Dynamics in Natural Populations of Pintomyia evansi under Experimental Infection with Leishmania infantum

et al. 2021

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Pintomyia evansi is recognized by its vectorial competence in the transmission of parasites that cause fatal visceral leishmaniasis in rural and urban environments of the Caribbean coast of Colombia. The effect on and the variation of the gut microbiota in female P. evansi infected with Leishmania infantum were evaluated under experimental conditions using 16S rRNA Illumina MiSeq sequencing. In the coinfection assay with L. infantum, 96.8% of the midgut microbial population was composed mainly of Proteobacteria (71.0%), followed by Cyanobacteria (20.4%), Actinobacteria (2.7%), and Firmicutes (2.7%). In insect controls (uninfected with L. infantum) that were treated or not with antibiotics, Ralstonia was reported to have high relative abundance (55.1–64.8%), in contrast to guts with a high load of infection from L. infantum (23.4–35.9%). ASVs that moderately increased in guts infected with Leishmania were Bacillus and Aeromonas. Kruskal–Wallis nonparametric variance statistical inference showed statistically significant intergroup differences in the guts of P. evansi infected and uninfected with L. infantum (p < 0.05), suggesting that some individuals of the microbiota could induce or restrict Leishmania infection. This assay also showed a negative effect of the antibiotic treatment and L. infantum infection on the gut microbiota diversity. Endosymbionts, such as Microsporidia infections (<2%), were more often associated with guts without Leishmania infection, whereas Arsenophonus was only found in guts with a high load of Leishmania infection and treated with antibiotics. Finally, this is the first report that showed the potential role of intestinal microbiota in natural populations of P. evansi in susceptibility to L. infantum infection.

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Tripartite interactions: Leishmania, microbiota and Lutzomyia longipalpis

Cited by 24 publications

References 58 publications

Influential Insider: Wolbachia, an Intracellular Symbiont, Manipulates Bacterial Diversity in Its Insect Host

Influential Insider: Wolbachia, an Intracellular Symbiont, Manipulates Bacterial Diversity in Its Insect Host

Advances in Understanding Leishmania Pathobiology: What Does RNA-Seq Tell Us?

Gut Microbiota Dynamics in Natural Populations of Pintomyia evansi under Experimental Infection with Leishmania infantum

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