Molecular and Functional Characterization of Trehalase in the Mosquito Anopheles stephensi
Like other insects, in blood-feeding mosquitoes, trehalase (TRE; EC 3.2.1.28), an enzyme that metabolizes trehalose, may influence a wide array of functions including flight, survival, reproduction, and vectorial capacity, but its role has not been investigated in detail. Here, we characterized a 1,...
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doaj-d44fac410bdc44d4b126065de20ecea12020-11-25T04:11:22ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2020-11-011110.3389/fphys.2020.575718575718Molecular and Functional Characterization of Trehalase in the Mosquito Anopheles stephensiSanjay Tevatiya0Seena Kumari1Punita Sharma2Jyoti Rani3Charu Chauhan4Tanwee Das De5Kailash C. Pandey6Veena Pande7Rajnikant Dixit8Laboratory of Host-Parasite Interaction Studies, ICMR-National Institute of Malaria Research, New Delhi, IndiaLaboratory of Host-Parasite Interaction Studies, ICMR-National Institute of Malaria Research, New Delhi, IndiaLaboratory of Host-Parasite Interaction Studies, ICMR-National Institute of Malaria Research, New Delhi, IndiaLaboratory of Host-Parasite Interaction Studies, ICMR-National Institute of Malaria Research, New Delhi, IndiaLaboratory of Host-Parasite Interaction Studies, ICMR-National Institute of Malaria Research, New Delhi, IndiaLaboratory of Host-Parasite Interaction Studies, ICMR-National Institute of Malaria Research, New Delhi, IndiaLaboratory of Host-Parasite Interaction Studies, ICMR-National Institute of Malaria Research, New Delhi, IndiaDepartment of Biotechnology, Kumaun University, Nainital, IndiaLaboratory of Host-Parasite Interaction Studies, ICMR-National Institute of Malaria Research, New Delhi, IndiaLike other insects, in blood-feeding mosquitoes, trehalase (TRE; EC 3.2.1.28), an enzyme that metabolizes trehalose, may influence a wide array of functions including flight, survival, reproduction, and vectorial capacity, but its role has not been investigated in detail. Here, we characterized a 1,839-bp-long transcript, encoding a 555-aa-long trehalase-2 homolog protein from the mosquito Anopheles stephensi. With a conserved insect homology, and in silico predicted membrane-bound protein, we tested whether trehalase (As-TreH) also plays a role in mosquito physiologies. Constitutive expression during aquatic development or adult mosquito tissues, and a consistent upregulation until 42 h of starvation, which was restored to basal levels after sugar supply, together indicated that As-TreH may have a key role in stress tolerance. A multifold enrichment in the midgut (p < 0.001819) and salivary glands (p < 4.37E-05) of the Plasmodium vivax-infected mosquitoes indicated that As-TreH may favor parasite development and survival in the mosquito host. However, surprisingly, after the blood meal, a consistent upregulation until 24 h in the fat body, and 48 h in the ovary, prompted to test its possible functional correlation in the reproductive physiology of the adult female mosquitoes. A functional knockdown by dsRNA-mediated silencing confers As-TreH ability to alter reproductive potential, causing a significant loss in the egg numbers (p < 0.001), possibly by impairing energy metabolism in the developing oocytes. Conclusively, our data provide initial evidence that As-TreH regulates multiple physiologies and may serve as a suitable target for designing novel strategies for vector control.https://www.frontiersin.org/articles/10.3389/fphys.2020.575718/fullmosquitomigduttrehalase (E.C 3.2.1.28)energy metabolismreproductionPlasmodium vivax |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Sanjay Tevatiya Seena Kumari Punita Sharma Jyoti Rani Charu Chauhan Tanwee Das De Kailash C. Pandey Veena Pande Rajnikant Dixit |
spellingShingle |
Sanjay Tevatiya Seena Kumari Punita Sharma Jyoti Rani Charu Chauhan Tanwee Das De Kailash C. Pandey Veena Pande Rajnikant Dixit Molecular and Functional Characterization of Trehalase in the Mosquito Anopheles stephensi Frontiers in Physiology mosquito migdut trehalase (E.C 3.2.1.28) energy metabolism reproduction Plasmodium vivax |
author_facet |
Sanjay Tevatiya Seena Kumari Punita Sharma Jyoti Rani Charu Chauhan Tanwee Das De Kailash C. Pandey Veena Pande Rajnikant Dixit |
author_sort |
Sanjay Tevatiya |
title |
Molecular and Functional Characterization of Trehalase in the Mosquito Anopheles stephensi |
title_short |
Molecular and Functional Characterization of Trehalase in the Mosquito Anopheles stephensi |
title_full |
Molecular and Functional Characterization of Trehalase in the Mosquito Anopheles stephensi |
title_fullStr |
Molecular and Functional Characterization of Trehalase in the Mosquito Anopheles stephensi |
title_full_unstemmed |
Molecular and Functional Characterization of Trehalase in the Mosquito Anopheles stephensi |
title_sort |
molecular and functional characterization of trehalase in the mosquito anopheles stephensi |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Physiology |
issn |
1664-042X |
publishDate |
2020-11-01 |
description |
Like other insects, in blood-feeding mosquitoes, trehalase (TRE; EC 3.2.1.28), an enzyme that metabolizes trehalose, may influence a wide array of functions including flight, survival, reproduction, and vectorial capacity, but its role has not been investigated in detail. Here, we characterized a 1,839-bp-long transcript, encoding a 555-aa-long trehalase-2 homolog protein from the mosquito Anopheles stephensi. With a conserved insect homology, and in silico predicted membrane-bound protein, we tested whether trehalase (As-TreH) also plays a role in mosquito physiologies. Constitutive expression during aquatic development or adult mosquito tissues, and a consistent upregulation until 42 h of starvation, which was restored to basal levels after sugar supply, together indicated that As-TreH may have a key role in stress tolerance. A multifold enrichment in the midgut (p < 0.001819) and salivary glands (p < 4.37E-05) of the Plasmodium vivax-infected mosquitoes indicated that As-TreH may favor parasite development and survival in the mosquito host. However, surprisingly, after the blood meal, a consistent upregulation until 24 h in the fat body, and 48 h in the ovary, prompted to test its possible functional correlation in the reproductive physiology of the adult female mosquitoes. A functional knockdown by dsRNA-mediated silencing confers As-TreH ability to alter reproductive potential, causing a significant loss in the egg numbers (p < 0.001), possibly by impairing energy metabolism in the developing oocytes. Conclusively, our data provide initial evidence that As-TreH regulates multiple physiologies and may serve as a suitable target for designing novel strategies for vector control. |
topic |
mosquito migdut trehalase (E.C 3.2.1.28) energy metabolism reproduction Plasmodium vivax |
url |
https://www.frontiersin.org/articles/10.3389/fphys.2020.575718/full |
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