Evolutionary genomics of epidemic visceral leishmaniasis in the Indian subcontinent

Hideo Imamura; Tim Downing; Frederik Van den Broeck; Mandy J Sanders; Suman Rijal; Shyam  Sundar; An Mannaert; Manu Vanaerschot; Maya Berg; Géraldine De Muylder; Franck Dumetz; Bart Cuypers; Ilse Maes; Malgorzata Domagalska; Saskia Decuypere; Keshav Rai; Surendra Uranw; Narayan Raj Bhattarai; Basudha  Khanal; Vijay Kumar Prajapati; Smriti Sharma; Olivia Stark; Gabriele Schönian; Harry P  De Koning; Luca Settimo; Benoit Vanhollebeke; Syamal Roy; Bart Ostyn; Marleen Boelaert; Louis Maes; Matthew Berriman; Jean-Claude Dujardin; James A Cotton

doi:10.7554/eLife.12613

Evolutionary genomics of epidemic visceral leishmaniasis in the Indian subcontinent

Hideo Imamura, Tim Downing, Frederik Van den Broeck, Mandy J Sanders, Suman Rijal, Shyam Sundar, An Mannaert, Manu Vanaerschot, Maya Berg, Géraldine De Muylder, Franck Dumetz, Bart Cuypers, Ilse Maes, Malgorzata Domagalska, Saskia Decuypere, Keshav Rai, Surendra Uranw, Narayan Raj Bhattarai, Basudha Khanal, Vijay Kumar PrajapatiSmriti Sharma, Olivia Stark, Gabriele Schönian, Harry P De Koning, Luca Settimo, Benoit Vanhollebeke, Syamal Roy, Bart Ostyn, Marleen Boelaert, Louis Maes, Matthew Berriman, Jean-Claude Dujardin, James A Cotton

Molecular Parasitology

Research output: Contribution to journal › A1: Web of Science-article › peer-review

92 Downloads (Pure)

Abstract

Leishmania donovani causes visceral leishmaniasis (VL), the second most deadly vector-borne parasitic disease. A recent epidemic in the Indian subcontinent (ISC) caused up to 80% of global VL and over 30,000 deaths per year. Resistance against antimonial drugs has probably been a contributing factor in the persistence of this epidemic. Here we use whole genome sequences from 204 clinical isolates to track the evolution and epidemiology of L. donovani from the ISC. We identify independent radiations that have emerged since a bottleneck coincident with 1960s DDT spraying campaigns. A genetically distinct population frequently resistant to antimonials has a two base-pair insertion in the aquaglyceroporin gene LdAQP1 that prevents the transport of trivalent antimonials. We find evidence of genetic exchange between ISC populations, and show that the mutation in LdAQP1 has spread by recombination. Our results reveal the complexity of L. donovani evolution in the ISC in response to drug treatment.

Original language	English
Article number	e12613
Journal	eLIFE
Volume	5
Number of pages	39
ISSN	2050-084X
DOIs	https://doi.org/10.7554/eLife.12613
Publication status	Published - 2016

Access to Document

10.7554/eLife.12613Licence: Unspecified

2016elife12613Final published version, 2.15 MBLicence: Unspecified

Cite this

Imamura, H., Downing, T., Van den Broeck, F., Sanders, M. J., Rijal, S., Sundar, S., Mannaert, A., Vanaerschot, M., Berg, M., De Muylder, G., Dumetz, F., Cuypers, B., Maes, I., Domagalska, M., Decuypere, S., Rai, K., Uranw, S., Bhattarai, N. R., Khanal, B., ... Cotton, J. A. (2016). Evolutionary genomics of epidemic visceral leishmaniasis in the Indian subcontinent. eLIFE, 5, Article e12613. https://doi.org/10.7554/eLife.12613

@article{901f8832a923464d9756cf8e5efbe23d,

title = "Evolutionary genomics of epidemic visceral leishmaniasis in the Indian subcontinent",

abstract = "Leishmania donovani causes visceral leishmaniasis (VL), the second most deadly vector-borne parasitic disease. A recent epidemic in the Indian subcontinent (ISC) caused up to 80% of global VL and over 30,000 deaths per year. Resistance against antimonial drugs has probably been a contributing factor in the persistence of this epidemic. Here we use whole genome sequences from 204 clinical isolates to track the evolution and epidemiology of L. donovani from the ISC. We identify independent radiations that have emerged since a bottleneck coincident with 1960s DDT spraying campaigns. A genetically distinct population frequently resistant to antimonials has a two base-pair insertion in the aquaglyceroporin gene LdAQP1 that prevents the transport of trivalent antimonials. We find evidence of genetic exchange between ISC populations, and show that the mutation in LdAQP1 has spread by recombination. Our results reveal the complexity of L. donovani evolution in the ISC in response to drug treatment.",

author = "Hideo Imamura and Tim Downing and {Van den Broeck}, Frederik and Sanders, {Mandy J} and Suman Rijal and Shyam Sundar and An Mannaert and Manu Vanaerschot and Maya Berg and {De Muylder}, G{\'e}raldine and Franck Dumetz and Bart Cuypers and Ilse Maes and Malgorzata Domagalska and Saskia Decuypere and Keshav Rai and Surendra Uranw and Bhattarai, {Narayan Raj} and Basudha Khanal and Prajapati, {Vijay Kumar} and Smriti Sharma and Olivia Stark and Gabriele Sch{\"o}nian and {De Koning}, {Harry P} and Luca Settimo and Benoit Vanhollebeke and Syamal Roy and Bart Ostyn and Marleen Boelaert and Louis Maes and Matthew Berriman and Jean-Claude Dujardin and Cotton, {James A}",

note = "FTX; DOAJ",

year = "2016",

doi = "10.7554/eLife.12613",

language = "English",

volume = "5",

journal = "eLIFE",

issn = "2050-084X",

publisher = "eLife Sciences Publications",

}

Imamura, H, Downing, T, Van den Broeck, F, Sanders, MJ, Rijal, S, Sundar, S, Mannaert, A, Vanaerschot, M, Berg, M, De Muylder, G, Dumetz, F, Cuypers, B, Maes, I, Domagalska, M , Decuypere, S, Rai, K, Uranw, S, Bhattarai, NR, Khanal, B, Prajapati, VK, Sharma, S, Stark, O, Schönian, G, De Koning, HP, Settimo, L, Vanhollebeke, B, Roy, S, Ostyn, B, Boelaert, M, Maes, L, Berriman, M, Dujardin, J-C & Cotton, JA 2016, 'Evolutionary genomics of epidemic visceral leishmaniasis in the Indian subcontinent', eLIFE, vol. 5, e12613. https://doi.org/10.7554/eLife.12613

TY - JOUR

T1 - Evolutionary genomics of epidemic visceral leishmaniasis in the Indian subcontinent

AU - Imamura, Hideo

AU - Downing, Tim

AU - Van den Broeck, Frederik

AU - Sanders, Mandy J

AU - Rijal, Suman

AU - Sundar, Shyam

AU - Mannaert, An

AU - Vanaerschot, Manu

AU - Berg, Maya

AU - De Muylder, Géraldine

AU - Dumetz, Franck

AU - Cuypers, Bart

AU - Maes, Ilse

AU - Domagalska, Malgorzata

AU - Decuypere, Saskia

AU - Rai, Keshav

AU - Uranw, Surendra

AU - Bhattarai, Narayan Raj

AU - Khanal, Basudha

AU - Prajapati, Vijay Kumar

AU - Sharma, Smriti

AU - Stark, Olivia

AU - Schönian, Gabriele

AU - De Koning, Harry P

AU - Settimo, Luca

AU - Vanhollebeke, Benoit

AU - Roy, Syamal

AU - Ostyn, Bart

AU - Boelaert, Marleen

AU - Maes, Louis

AU - Berriman, Matthew

AU - Dujardin, Jean-Claude

AU - Cotton, James A

N1 - FTX; DOAJ

PY - 2016

Y1 - 2016

N2 - Leishmania donovani causes visceral leishmaniasis (VL), the second most deadly vector-borne parasitic disease. A recent epidemic in the Indian subcontinent (ISC) caused up to 80% of global VL and over 30,000 deaths per year. Resistance against antimonial drugs has probably been a contributing factor in the persistence of this epidemic. Here we use whole genome sequences from 204 clinical isolates to track the evolution and epidemiology of L. donovani from the ISC. We identify independent radiations that have emerged since a bottleneck coincident with 1960s DDT spraying campaigns. A genetically distinct population frequently resistant to antimonials has a two base-pair insertion in the aquaglyceroporin gene LdAQP1 that prevents the transport of trivalent antimonials. We find evidence of genetic exchange between ISC populations, and show that the mutation in LdAQP1 has spread by recombination. Our results reveal the complexity of L. donovani evolution in the ISC in response to drug treatment.

AB - Leishmania donovani causes visceral leishmaniasis (VL), the second most deadly vector-borne parasitic disease. A recent epidemic in the Indian subcontinent (ISC) caused up to 80% of global VL and over 30,000 deaths per year. Resistance against antimonial drugs has probably been a contributing factor in the persistence of this epidemic. Here we use whole genome sequences from 204 clinical isolates to track the evolution and epidemiology of L. donovani from the ISC. We identify independent radiations that have emerged since a bottleneck coincident with 1960s DDT spraying campaigns. A genetically distinct population frequently resistant to antimonials has a two base-pair insertion in the aquaglyceroporin gene LdAQP1 that prevents the transport of trivalent antimonials. We find evidence of genetic exchange between ISC populations, and show that the mutation in LdAQP1 has spread by recombination. Our results reveal the complexity of L. donovani evolution in the ISC in response to drug treatment.

U2 - 10.7554/eLife.12613

DO - 10.7554/eLife.12613

M3 - A1: Web of Science-article

SN - 2050-084X

VL - 5

JO - eLIFE

JF - eLIFE

M1 - e12613

ER -

Evolutionary genomics of epidemic visceral leishmaniasis in the Indian subcontinent

Abstract

Access to Document

Fingerprint

Cite this