Culturable bacteria associated with Anopheles darlingi and their paratransgenesis potential

Rocha, Elerson Matos; Marinotti, Osvaldo; Serrão, Deidre Machado; Correa, Laura Viana; Katak, Ricardo de Melo; Oliveira, Juan Campos de; Muniz, Veranilce Alves; Oliveira, Marta Rodrigues de; Neto, Joaquim Ferreira do Nascimento; Pessoa, Marcos Cézar Fernandes; Roque, Rosemary Aparecida; Mota, Adolfo José da; Onorati, Piero; Souza-Neto, Jayme A.; Terenius, Olle; Tadei, Wanderli Pedro

doi:10.1186/s12936-020-03574-1

Cited by 18 publications

(30 citation statements)

References 60 publications

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“…It is efficient, cost effective, and minimally invasive compared to feeding and/or injecting synthetic antagomirs, and as such, this approach serves as an efficacious alternative to investigate microRNA related functions in the tsetse fly gut. This strategy can similarly be employed in any arthropod that houses genetically modifiable commensal gut symbionts that reside within host cells [ 70 , 71 ].…”

Section: Discussionmentioning

confidence: 99%

Paratransgenic manipulation of a tsetse microRNA alters the physiological homeostasis of the fly’s midgut environment

et al. 2021

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Tsetse flies are vectors of parasitic African trypanosomes, the etiological agents of human and animal African trypanosomoses. Current disease control methods include fly-repelling pesticides, fly trapping, and chemotherapeutic treatment of infected people and animals. Inhibiting tsetse’s ability to transmit trypanosomes by strengthening the fly’s natural barriers can serve as an alternative approach to reduce disease. The peritrophic matrix (PM) is a chitinous and proteinaceous barrier that lines the insect midgut and serves as a protective barrier that inhibits infection with pathogens. African trypanosomes must cross tsetse’s PM in order to establish an infection in the fly, and PM structural integrity negatively correlates with trypanosome infection outcomes. Bloodstream form trypanosomes shed variant surface glycoproteins (VSG) into tsetse’s gut lumen early during the infection establishment, and free VSG molecules are internalized by the fly’s PM-producing cardia. This process results in a reduction in the expression of a tsetse microRNA (miR275) and a sequential molecular cascade that compromises PM integrity. miRNAs are small non-coding RNAs that are critical in regulating many physiological processes. In the present study, we investigated the role(s) of tsetse miR275 by developing a paratransgenic expression system that employs tsetse’s facultative bacterial endosymbiont, Sodalis glossinidius, to express tandem antagomir-275 repeats (or miR275 sponges). This system induces a constitutive, 40% reduction in miR275 transcript abundance in the fly’s midgut and results in obstructed blood digestion (gut weights increased by 52%), a significant increase (p-value < 0.0001) in fly survival following infection with an entomopathogenic bacteria, and a 78% increase in trypanosome infection prevalence. RNA sequencing of cardia and midgut tissues from paratransgenic tsetse confirmed that miR275 regulates processes related to the expression of PM-associated proteins and digestive enzymes as well as genes that encode abundant secretory proteins. Our study demonstrates that paratransgenesis can be employed to study microRNA regulated pathways in arthropods that house symbiotic bacteria.

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Section: Discussionmentioning

confidence: 99%

Paratransgenic manipulation of a tsetse microRNA alters the physiological homeostasis of the fly’s midgut environment

et al. 2021

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“…et al [53] considered that" paratransgenesis" could be a promising alternative for controlling malaria transmission by Anopheles darlingi in the Amazon region. "Paratransgenesis aims to inhibit the development of parasites within the vector through the action of genetically modified bacteria".…”

Section: Rochamentioning

confidence: 99%

Transgenesis of Bioluminescence (BL) Gene and Its Potential Use for Malaria Residual Transmission Issue and Other Vector Borne Diseases: New Considerations for Vector and Vector Borne Diseases (VBD) Control

Carnevale¹,

Carnevale²

2021

AJRID

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The present article considers the potential of transgenesis of the bioluminescent gene for malaria and other vector borne diseases (VBD) control. Vector control is an important component of every vector control operations for the vector borne disease control. Actually the bioluminescence phenomena and the green fluorescent protein GPF open great field of researches and “On December 10, 2008 Osamu Shimomura, Martin Chalfie and Roger Tsien were awarded the Nobel Prize in Chemistry for "the discovery and development of the green fluorescent protein, GFP". Bio-molecular technologies and transgenesis open the field for getting BL mosquitoes such as Plasmodium (several references) for “Transmission Reducing Activity” (TRA) without any hazard on human beings and ecological level. For exemple BL mosquitoes would be of paramount importance for mark-release-recapture becoming easier to implement and giving more relevant and reliable data on relation between density (size of the population) and distance (and wind) as the vector population size decrease with increasing distance from the source of production (breeding site) or release point. BL appeared already of great interest to understand the relation vector/parasite and to assess transmission intensity. Our idea is to genetically produce “Bioluminescent Mosquitoes” allowing a better identification of their presence, behavior, densities, infected specimens, risk of transmission before/after vector control operations which could be greatly improved thanks to the targeting of mosquitoes resting site or flight range and any other biological component.

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“…However, several bacterial isolates have been consistently detected in breeding sites, mosquito gut, and other mosquito-associated sources (Guégan et al, 2018). This is the case with Klebsiella, a genus of bacteria frequently reported in mosquitoes and their breeding sites (Gusmão et al, 2010;Chandel et al, 2013;Dada et al, 2014;Yadav et al, 2015;Wang et al, 2018;Hery et al, 2020;Alvarado et al, 2021;Rocha et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

“…Several authors have identified Klebsiella associated with Aedes , Anopheles , and Culex mosquitoes using both culture-dependent and independent methods ( Chandel et al, 2013 ; Yadav et al, 2015 ; Rocha et al, 2021 ). Therefore, it seems that these enteric bacteria maintain a stable relationship with the insects.…”

Section: Introductionmentioning

confidence: 99%

Multi-Omic Analysis of Symbiotic Bacteria Associated With Aedes aegypti Breeding Sites

et al. 2021

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Mosquito breeding sites are complex aquatic environments with wide microbial diversity and physicochemical parameters that can change over time during the development of immature insect stages. Changes in biotic and abiotic conditions in water can alter life-history traits of adult mosquitos but this area remains understudied. Here, using microbial genomic and metabolomics analyses, we explored the metabolites associated with Aedes aegypti breeding sites as well as the potential contribution of Klebsiella sp., symbiotic bacteria highly associated with mosquitoes. We sought to address whether breeding sites have a signature metabolic profile and understand the metabolite contribution of the bacteria in the aquatic niches where Ae. aegypti larvae develop. An analysis of 32 mosquito-associated bacterial genomes, including Klebsiella, allowed us to identify gene clusters involved in primary metabolic pathways. From them, we inferred metabolites that could impact larval development (e.g., spermidine), as well as influence the quality assessment of a breeding site by a gravid female (e.g., putrescine), if produced by bacteria in the water. We also detected significant variance in metabolite presence profiles between water samples representing a decoupled oviposition event (oviposition by single females and manually deposited eggs) versus a control where no mosquito interactions occurred (PERMANOVA: p < 0.05; R2 = 24.64% and R2 = 30.07%). Five Klebsiella metabolites were exclusively linked to water samples where oviposition and development occurred. These data suggest metabolomics can be applied to identify compounds potentially used by female Ae. aegypti to evaluate the quality of a breeding site. Elucidating the physiological mechanisms by which the females could integrate these sensory cues while ovipositing constitutes a growing field of interest, which could benefit from a more depurated list of candidate molecules.

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Culturable bacteria associated with Anopheles darlingi and their paratransgenesis potential

Cited by 18 publications

References 60 publications

Paratransgenic manipulation of a tsetse microRNA alters the physiological homeostasis of the fly’s midgut environment

Paratransgenic manipulation of a tsetse microRNA alters the physiological homeostasis of the fly’s midgut environment

Transgenesis of Bioluminescence (BL) Gene and Its Potential Use for Malaria Residual Transmission Issue and Other Vector Borne Diseases: New Considerations for Vector and Vector Borne Diseases (VBD) Control

Multi-Omic Analysis of Symbiotic Bacteria Associated With Aedes aegypti Breeding Sites

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