Uptake of Plasmodium falciparum Gametocytes During Mosquito Bloodmeal by Direct and Membrane Feeding

Plasmodium falciparum remains one of the leading causes of child mortality, and nearly half of the world’s population is at risk of contracting malaria. While pathogenesis results from replication of asexual forms in human red blood cells, it is the sexually differentiated forms, gametocytes, which...

Full description

Bibliographic Details
Main Authors: Arthur M. Talman, Dinkorma T. D. Ouologuem, Katie Love, Virginia M. Howick, Charles Mulamba, Aboubecrin Haidara, Niawanlou Dara, Daman Sylla, Adama Sacko, Mamadou M. Coulibaly, Francois Dao, Cheick P. O. Sangare, Abdoulaye Djimde, Mara K. N. Lawniczak
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-03-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.00246/full
id doaj-5d33fd19840b4845a41408d7fcc6f885
record_format Article
spelling doaj-5d33fd19840b4845a41408d7fcc6f8852020-11-25T02:35:14ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-03-011110.3389/fmicb.2020.00246495668Uptake of Plasmodium falciparum Gametocytes During Mosquito Bloodmeal by Direct and Membrane FeedingArthur M. Talman0Arthur M. Talman1Dinkorma T. D. Ouologuem2Katie Love3Virginia M. Howick4Charles Mulamba5Aboubecrin Haidara6Niawanlou Dara7Daman Sylla8Adama Sacko9Mamadou M. Coulibaly10Francois Dao11Cheick P. O. Sangare12Abdoulaye Djimde13Mara K. N. Lawniczak14Wellcome Sanger Institute, Hinxton, United KingdomMIVEGEC, IRD, CNRS, University of Montpellier, Montpellier, FranceMalaria Research and Training Centre, University of Science, Techniques and Technologies of Bamako, Bamako, MaliWellcome Sanger Institute, Hinxton, United KingdomWellcome Sanger Institute, Hinxton, United KingdomWellcome Sanger Institute, Hinxton, United KingdomMalaria Research and Training Centre, University of Science, Techniques and Technologies of Bamako, Bamako, MaliMalaria Research and Training Centre, University of Science, Techniques and Technologies of Bamako, Bamako, MaliMalaria Research and Training Centre, University of Science, Techniques and Technologies of Bamako, Bamako, MaliMalaria Research and Training Centre, University of Science, Techniques and Technologies of Bamako, Bamako, MaliMalaria Research and Training Centre, University of Science, Techniques and Technologies of Bamako, Bamako, MaliMalaria Research and Training Centre, University of Science, Techniques and Technologies of Bamako, Bamako, MaliMalaria Research and Training Centre, University of Science, Techniques and Technologies of Bamako, Bamako, MaliMalaria Research and Training Centre, University of Science, Techniques and Technologies of Bamako, Bamako, MaliWellcome Sanger Institute, Hinxton, United KingdomPlasmodium falciparum remains one of the leading causes of child mortality, and nearly half of the world’s population is at risk of contracting malaria. While pathogenesis results from replication of asexual forms in human red blood cells, it is the sexually differentiated forms, gametocytes, which are responsible for the spread of the disease. For transmission to succeed, both mature male and female gametocytes must be taken up by a female Anopheles mosquito during its blood meal for subsequent differentiation into gametes and mating inside the mosquito gut. Observed circulating numbers of gametocytes in the human host are often surprisingly low. A pre-fertilization behavior, such as skin sequestration, has been hypothesized to explain the efficiency of human-to-mosquito transmission but has not been sufficiently tested due to a lack of appropriate tools. In this study, we describe the optimization of a qPCR tool that enables the relative quantification of gametocytes within very small input samples. Such a tool allows for the quantification of gametocytes in different compartments of the host and the vector that could potentially unravel mechanisms that enable highly efficient malaria transmission. We demonstrate the use of our gametocyte quantification method in mosquito blood meals from both direct skin feeding on Plasmodium gametocyte carriers and standard membrane feeding assay. Relative gametocyte abundance was not different between mosquitoes fed through a membrane or directly on the skin suggesting that there is no systematic enrichment of gametocytes picked up in the skin.https://www.frontiersin.org/article/10.3389/fmicb.2020.00246/fullmalariatransmissiongametocytemosquito feedingPlasmodium falciparum
collection DOAJ
language English
format Article
sources DOAJ
author Arthur M. Talman
Arthur M. Talman
Dinkorma T. D. Ouologuem
Katie Love
Virginia M. Howick
Charles Mulamba
Aboubecrin Haidara
Niawanlou Dara
Daman Sylla
Adama Sacko
Mamadou M. Coulibaly
Francois Dao
Cheick P. O. Sangare
Abdoulaye Djimde
Mara K. N. Lawniczak
spellingShingle Arthur M. Talman
Arthur M. Talman
Dinkorma T. D. Ouologuem
Katie Love
Virginia M. Howick
Charles Mulamba
Aboubecrin Haidara
Niawanlou Dara
Daman Sylla
Adama Sacko
Mamadou M. Coulibaly
Francois Dao
Cheick P. O. Sangare
Abdoulaye Djimde
Mara K. N. Lawniczak
Uptake of Plasmodium falciparum Gametocytes During Mosquito Bloodmeal by Direct and Membrane Feeding
Frontiers in Microbiology
malaria
transmission
gametocyte
mosquito feeding
Plasmodium falciparum
author_facet Arthur M. Talman
Arthur M. Talman
Dinkorma T. D. Ouologuem
Katie Love
Virginia M. Howick
Charles Mulamba
Aboubecrin Haidara
Niawanlou Dara
Daman Sylla
Adama Sacko
Mamadou M. Coulibaly
Francois Dao
Cheick P. O. Sangare
Abdoulaye Djimde
Mara K. N. Lawniczak
author_sort Arthur M. Talman
title Uptake of Plasmodium falciparum Gametocytes During Mosquito Bloodmeal by Direct and Membrane Feeding
title_short Uptake of Plasmodium falciparum Gametocytes During Mosquito Bloodmeal by Direct and Membrane Feeding
title_full Uptake of Plasmodium falciparum Gametocytes During Mosquito Bloodmeal by Direct and Membrane Feeding
title_fullStr Uptake of Plasmodium falciparum Gametocytes During Mosquito Bloodmeal by Direct and Membrane Feeding
title_full_unstemmed Uptake of Plasmodium falciparum Gametocytes During Mosquito Bloodmeal by Direct and Membrane Feeding
title_sort uptake of plasmodium falciparum gametocytes during mosquito bloodmeal by direct and membrane feeding
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2020-03-01
description Plasmodium falciparum remains one of the leading causes of child mortality, and nearly half of the world’s population is at risk of contracting malaria. While pathogenesis results from replication of asexual forms in human red blood cells, it is the sexually differentiated forms, gametocytes, which are responsible for the spread of the disease. For transmission to succeed, both mature male and female gametocytes must be taken up by a female Anopheles mosquito during its blood meal for subsequent differentiation into gametes and mating inside the mosquito gut. Observed circulating numbers of gametocytes in the human host are often surprisingly low. A pre-fertilization behavior, such as skin sequestration, has been hypothesized to explain the efficiency of human-to-mosquito transmission but has not been sufficiently tested due to a lack of appropriate tools. In this study, we describe the optimization of a qPCR tool that enables the relative quantification of gametocytes within very small input samples. Such a tool allows for the quantification of gametocytes in different compartments of the host and the vector that could potentially unravel mechanisms that enable highly efficient malaria transmission. We demonstrate the use of our gametocyte quantification method in mosquito blood meals from both direct skin feeding on Plasmodium gametocyte carriers and standard membrane feeding assay. Relative gametocyte abundance was not different between mosquitoes fed through a membrane or directly on the skin suggesting that there is no systematic enrichment of gametocytes picked up in the skin.
topic malaria
transmission
gametocyte
mosquito feeding
Plasmodium falciparum
url https://www.frontiersin.org/article/10.3389/fmicb.2020.00246/full
work_keys_str_mv AT arthurmtalman uptakeofplasmodiumfalciparumgametocytesduringmosquitobloodmealbydirectandmembranefeeding
AT arthurmtalman uptakeofplasmodiumfalciparumgametocytesduringmosquitobloodmealbydirectandmembranefeeding
AT dinkormatdouologuem uptakeofplasmodiumfalciparumgametocytesduringmosquitobloodmealbydirectandmembranefeeding
AT katielove uptakeofplasmodiumfalciparumgametocytesduringmosquitobloodmealbydirectandmembranefeeding
AT virginiamhowick uptakeofplasmodiumfalciparumgametocytesduringmosquitobloodmealbydirectandmembranefeeding
AT charlesmulamba uptakeofplasmodiumfalciparumgametocytesduringmosquitobloodmealbydirectandmembranefeeding
AT aboubecrinhaidara uptakeofplasmodiumfalciparumgametocytesduringmosquitobloodmealbydirectandmembranefeeding
AT niawanloudara uptakeofplasmodiumfalciparumgametocytesduringmosquitobloodmealbydirectandmembranefeeding
AT damansylla uptakeofplasmodiumfalciparumgametocytesduringmosquitobloodmealbydirectandmembranefeeding
AT adamasacko uptakeofplasmodiumfalciparumgametocytesduringmosquitobloodmealbydirectandmembranefeeding
AT mamadoumcoulibaly uptakeofplasmodiumfalciparumgametocytesduringmosquitobloodmealbydirectandmembranefeeding
AT francoisdao uptakeofplasmodiumfalciparumgametocytesduringmosquitobloodmealbydirectandmembranefeeding
AT cheickposangare uptakeofplasmodiumfalciparumgametocytesduringmosquitobloodmealbydirectandmembranefeeding
AT abdoulayedjimde uptakeofplasmodiumfalciparumgametocytesduringmosquitobloodmealbydirectandmembranefeeding
AT maraknlawniczak uptakeofplasmodiumfalciparumgametocytesduringmosquitobloodmealbydirectandmembranefeeding
_version_ 1724804581818368000