Comparative genomics of Leishmania braziliensis promastigotes subjected to different temperatures

The leishmaniases are complex neglected diseases caused by the protozoan parasite Leishmania. Cutaneous leishmaniasis is the most common clinical manifestation around the world, and in the Americas the main aetiological agent is Leishmania braziliensis. In recent studies, chromosome and gene copy nu...

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2019
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Universidad del Rosario
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Repositorio EdocUR - U. Rosario
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spa
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oai:repository.urosario.edu.co:10336/19033
Acceso en línea:
https://doi.org/10.48713/10336_19033
http://repository.urosario.edu.co/handle/10336/19033
Palabra clave:
Leishmania braziliensis
Promastigote
Temperature increase
Gene copy number variation
Aneuploidy
Enfermedades
Leishmania braziliensis
Promastigote
Temperature increase
Gene copy number variation
Aneuploidy
Leishmaniasis
Infecciones por protozoarios
Rights
License
Atribución-NoComercial-SinDerivadas 2.5 Colombia
id EDOCUR2_204946cd26609e41218c61ad906f3133
oai_identifier_str oai:repository.urosario.edu.co:10336/19033
network_acronym_str EDOCUR2
network_name_str Repositorio EdocUR - U. Rosario
repository_id_str
dc.title.spa.fl_str_mv Comparative genomics of Leishmania braziliensis promastigotes subjected to different temperatures
title Comparative genomics of Leishmania braziliensis promastigotes subjected to different temperatures
spellingShingle Comparative genomics of Leishmania braziliensis promastigotes subjected to different temperatures
Leishmania braziliensis
Promastigote
Temperature increase
Gene copy number variation
Aneuploidy
Enfermedades
Leishmania braziliensis
Promastigote
Temperature increase
Gene copy number variation
Aneuploidy
Leishmaniasis
Infecciones por protozoarios
title_short Comparative genomics of Leishmania braziliensis promastigotes subjected to different temperatures
title_full Comparative genomics of Leishmania braziliensis promastigotes subjected to different temperatures
title_fullStr Comparative genomics of Leishmania braziliensis promastigotes subjected to different temperatures
title_full_unstemmed Comparative genomics of Leishmania braziliensis promastigotes subjected to different temperatures
title_sort Comparative genomics of Leishmania braziliensis promastigotes subjected to different temperatures
dc.contributor.advisor.none.fl_str_mv Ramírez, Juan David
dc.contributor.none.fl_str_mv Ballesteros, Nathalia
Patiño, Luz Helena
Cruz-Saavedra, Lissa
dc.subject.spa.fl_str_mv Leishmania braziliensis
Promastigote
Temperature increase
Gene copy number variation
Aneuploidy
topic Leishmania braziliensis
Promastigote
Temperature increase
Gene copy number variation
Aneuploidy
Enfermedades
Leishmania braziliensis
Promastigote
Temperature increase
Gene copy number variation
Aneuploidy
Leishmaniasis
Infecciones por protozoarios
dc.subject.ddc.spa.fl_str_mv Enfermedades
dc.subject.keyword.spa.fl_str_mv Leishmania braziliensis
Promastigote
Temperature increase
Gene copy number variation
Aneuploidy
dc.subject.lemb.spa.fl_str_mv Leishmaniasis
Infecciones por protozoarios
description The leishmaniases are complex neglected diseases caused by the protozoan parasite Leishmania. Cutaneous leishmaniasis is the most common clinical manifestation around the world, and in the Americas the main aetiological agent is Leishmania braziliensis. In recent studies, chromosome and gene copy number variations (CNVs) have been highlighted as some mechanisms used by Leishmania species to adapt to environmental changes such as host change or drug pressure. However, no studies have described the impact of temperature shifts across the genome of Leishmania promastigotes and particularly in L. braziliensis. Therefore, we sequenced the genome (DNA-Seq) of L. braziliensis promastigotes from cultures subjected to three different temperatures, 24, 28, and 30°C; then, we analysed the aneuploidy, gene CNVs, SNPs and Indels compared with those at the control temperature (26°C). We found that the increase in temperature at 30°C had a negative effect on promastigotes proliferation; although, there were no changes in the somy, SNPs and Indels on the DNA among the three temperatures compared to the control. Only around 3% of the genes having significant copy number variation (CNVs) at each temperature showed some important genes for adaptation to temperature shifts. In conclusion, there is not a relevant genome response to the temperature shift in short-term, therefore the adaptation of this species to abiotic change could be occurring at transcriptome level. The ecological consequences are herein discussed.
publishDate 2019
dc.date.accessioned.none.fl_str_mv 2019-02-11T14:04:29Z
dc.date.available.none.fl_str_mv 2019-02-11T14:04:29Z
dc.date.created.none.fl_str_mv 2019-01-17
dc.date.issued.none.fl_str_mv 2019
dc.type.eng.fl_str_mv bachelorThesis
dc.type.coar.fl_str_mv http://purl.org/coar/resource_type/c_7a1f
dc.type.document.spa.fl_str_mv Trabajo de grado
dc.type.spa.spa.fl_str_mv Trabajo de grado
dc.identifier.doi.none.fl_str_mv https://doi.org/10.48713/10336_19033
dc.identifier.uri.none.fl_str_mv http://repository.urosario.edu.co/handle/10336/19033
url https://doi.org/10.48713/10336_19033
http://repository.urosario.edu.co/handle/10336/19033
dc.language.iso.none.fl_str_mv spa
language spa
dc.rights.spa.fl_str_mv Atribución-NoComercial-SinDerivadas 2.5 Colombia
dc.rights.coar.fl_str_mv http://purl.org/coar/access_right/c_abf2
dc.rights.acceso.spa.fl_str_mv Abierto (Texto Completo)
dc.rights.uri.none.fl_str_mv http://creativecommons.org/licenses/by-nc-nd/2.5/co/
rights_invalid_str_mv Atribución-NoComercial-SinDerivadas 2.5 Colombia
Abierto (Texto Completo)
http://creativecommons.org/licenses/by-nc-nd/2.5/co/
http://purl.org/coar/access_right/c_abf2
dc.format.mimetype.none.fl_str_mv application/pdf
dc.publisher.spa.fl_str_mv Universidad del Rosario
dc.publisher.department.spa.fl_str_mv Facultad de Ciencias Naturales y Matemáticas
dc.publisher.program.spa.fl_str_mv Biología
institution Universidad del Rosario
dc.source.bibliographicCitation.spa.fl_str_mv 1. Liang L, Gong P. Climate change and human infectious diseases: A synthesis of research findings from global and spatio-temporal perspectives. Environ Int. 2017;103:99–108.
2. Lafferty KD, Mordecai EA. The rise and fall of infectious disease in a warmer world. F1000Research. 2016;5(0):2040.
3. Wu X, Lu Y, Zhou S, Chen L, Xu B. Impact of climate change on human infectious diseases: Empirical evidence and human adaptation. Environ Int [Internet]. 2016;86:14–23. Available from: http://dx.doi.org/10.1016/j.envint.2015.09.007
4. Ramírez JD, Hernández C, León CM, Ayala MS, Flórez C, González C. Taxonomy, diversity, temporal and geographical distribution of Cutaneous Leishmaniasis in Colombia: A retrospective study. Sci Rep [Internet]. 2016;6(March):1–10. Available from: http://dx.doi.org/10.1038/srep28266
5. Patino LH, Mendez C, Rodriguez O, Romero Y, Velandia D, Alvarado M, et al. Spatial distribution, Leishmania species and clinical traits of Cutaneous Leishmaniasis cases in the Colombian army. PLoS Negl Trop Dis. 2017;11(8):1–15.
6. Hlavacova J, Votypka J, Volf P. The Effect of Temperature on Leishmania (Kinetoplastida: Trypanosomatidae) Development in Sand Flies. J Med Entomol. 2013;50(4):1–4.
7. Leon LL, Soares MJ, Temporal RM. Effects of Temperature on Promastigotes of Several Species of Leishmania. 1995;42(3):219–23.
8. Zilberstein D, Shapira M. THE ROLE OF pH AND TEMPERATURE IN THE DEVELOPMENT OF LEISHMANIA PARASITES. Annu Rev Microbiol. 1994;48:449–70.
9. Cardenas R, Sandoval C, Rodriguez-Morales a. P530 Impact of climate variability in the occurrence of leishmaniasis in Southern departments of Colombia. Int J Antimicrob Agents. 2007;29(2):S117–8.
10. González C, Wang O, Strutz SE, González-Salazar C, Sánchez-Cordero V, Sarkar S. Climate change and risk of leishmaniasis in North America: Predictions from ecological niche models of vector and reservoir species. PLoS Negl Trop Dis. 2010;4(1).
11. Koch LK, Kochmann J, Klimpel S, Cunze S. Modeling the climatic suitability of leishmaniasis vector species in Europe. Sci Rep [Internet]. 2017;7(1):1–10. Available from: http://dx.doi.org/10.1038/s41598-017-13822-1.
12. Rajesh K, Sanjay K. Change in global Climate and Prevalence of Visceral Leishmaniasis. Int J Sci Res Publ. 2013;3(1):2250–3153.
13. Lawrence F, Robert-gero M. Induction of heat shock and stress proteins promastigotes of three Leishmania species. Proc Natl Acad Sci USA. 1985;82(July):4414–7.
14. Folgueira C, Quijada L, Soto M, Abanades DR, Alonso C, Requena JM. The translational efficiencies of the two Leishmania infantum HSP70 mRNAs, differing in their 3′-untranslated regions, are affected by shifts in the temperature of growth through different mechanisms. J Biol Chem. 2005;280(42):35172–83.
15. Toye, Philip and HR "The influence of temperature and serum deprivation on the synthesis of heat-shock proteins and alpha and beta tubulin in promastigotes of L major. . M and biochemical parasitology 35. . (1989): 1-10. Leishmania major. 1988;167(March):1–10.
16. Rastrojo A, García-Hernández R, Vargas P, Camacho E, Corvo L, Imamura H, et al. Genomic and transcriptomic alterations in Leishmania donovani lines experimentally resistant to antileishmanial drugs. Int J Parasitol Drugs Drug Resist. 2018;8(2).
17. Dumetz F, Imamura H, Sanders M, Seblova V, Myskova J, Pescher P. Modulation of Aneuploidy in Leishmania In Vitro and In Vivo Environments and Its. MBio. 2017;8(3):e00599-17.
18. Giovanni Bussotti, a B, Evi Gouzelou B, Mariana Côrtes Boité, c Ihcen Kherachi D, Zoubir Harrat, d Naouel Eddaikra D, Jeremy C. Mottram, e Maria Antoniou F, Vasiliki Christodoulou F, et al. crossm Leishmania Genome Dynamics during Environmental Adaptation Reveal Strain-Specific Differences in Gene Copy. 2018;9(6):1–18.
19. Barja PP, Pescher P, Bussotti G, Dumetz F, Imamura H, Kedra D, et al. Haplotype selection as an adaptive mechanism in the protozoan pathogen Leishmania donovani. Nat Ecol Evol. 2017;1(12):1961.
20. Shaw CD, Lonchamp J, Downing T, Imamura H, Freeman TM, Cotton JA, et al. In vitro selection of miltefosine resistance in promastigotes of Leishmania donovani from Nepal: Genomic and metabolomic characterization. Mol Microbiol. 2016;99(6):1134–48.
21. Mondelaers A, Sanchez-Cañete MP, Hendrickx S, Eberhardt E, Garcia-Hernandez R, Lachaud L, et al. Genomic and Molecular Characterization of Miltefosine Resistance in Leishmania infantum Strains with Either Natural or Acquired Resistance through Experimental Selection of Intracellular Amastigotes. PLoS One. 2016;11(4):e0154101.
22. Downing T, Imamura H, Decuypere S. Whole genome sequencing of multiple Leishmania donovani clinical isolates provides insights into population structure and mechanisms of drug resistance. Genome [Internet]. 2011;21:2143–56. Available from: http://genome.cshlp.org/content/early/2011/10/27/gr.123430.111.abstract
23. Vanaerschot M, Decuypere S, Downing T, Imamura H, Stark O, De Doncker S, et al. Genetic markers for SSG resistance in leishmania donovani and SSG treatment failure in visceral leishmaniasis patients of the Indian subcontinent. J Infect Dis. 2012;206(5):752–5.
24. Valdivia HO, Reis-Cunha JL, Rodrigues-Luiz GF, Baptista RP, Baldeviano GC, Gerbasi R V., et al. Comparative genomic analysis of Leishmania (Viannia) peruviana and Leishmania (Viannia) braziliensis. BMC Genomics [Internet]. 2015;16(1):1–10. Available from: http://dx.doi.org/10.1186/s12864-015-1928-z
25. Coughlan S, Taylor AS, Feane E, Sanders M, Schonian G, Cotton JA, et al. Leishmania naiffi and Leishmania guyanensis reference genomes highlight genome structure and gene evolution in the Viannia subgenus. R Soc Open Sci. 2018;5(4).
26. Dujardin JC, Mannaert A, Durrant C, Cotton JA. Mosaic aneuploidy in Leishmania: The perspective of whole genome sequencing. Trends Parasitol [Internet]. 2014;30(12):554–5. Available from: http://dx.doi.org/10.1016/j.pt.2014.09.004
27. Lean JL, Rind DH. How will Earth’s surface temperature change in future decades? Geophys Res Lett. 2009;36(15):1–5.
28. Rogers MB, Hilley JD, Dickens NJ, Wilkes J, Bates PA, Depledge DP, et al. Chromosome and gene copy number variation allow major structural change between species and strains of Leishmania. 2011;2129–42.
29. Barria C, Malecki M, Arraiano CM. Bacterial adaptation to cold. Microbiology [Internet]. 2013 Dec 1 [cited 2019 Jan 5];159(Pt_12):2437–43. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24068238
30. Nedwell DB. Effect of low temperature on microbial growth: Lowered affinity for substrates limits growth at low temperature. FEMS Microbiol Ecol. 1999;30(2):101–11.
31. Laffitte M-CN, Leprohon P, Papadopoulou B, Ouellette M. Plasticity of the Leishmania genome leading to gene copy number variations and drug resistance. F1000Research [Internet]. 2016;5:2350. Available from: http://f1000research.com/articles/5-2350/v1
32. Mannaert A, Downing T, Imamura H, Dujardin JC. Adaptive mechanisms in pathogens: Universal aneuploidy in Leishmania. Trends Parasitol [Internet]. 2012;28(9):370–6. Available from: http://dx.doi.org/10.1016/j.pt.2012.06.003
33. Sterkers Y, Lachaud L, Crobu L, Bastien P, Pagès M. FISH analysis reveals aneuploidy and continual generation of chromosomal mosaicism in Leishmania major. Cell Microbiol. 2011;13(2):274–83.
34. Sterkers Y, Crobu L, Lachaud L, Pagès M, Bastien P. Parasexuality and mosaic aneuploidy in Leishmania: Alternative genetics. Trends in Parasitology. 2014.
35. Ghouila A, Guerfali FZ, Atri C, Bali A, Attia H, Sghaier RM, et al. Comparative genomics of Tunisian Leishmania major isolates causing human cutaneous leishmaniasis with contrasting clinical severity. Infect Genet Evol. 2017;50.
36. Nandan D, Yi T, Lopez M, Lai C, Reiner NE. Leishmania EF-1α activates the Src homology 2 domain containing tyrosine phosphatase SHP-1 leading to macrophage deactivation. J Biol Chem. 2002;277(51):50190–7.
37. Hombach A, Ommen G, Macdonald A, Clos J. A small heat shock protein is essential for thermotolerance and intracellular survival of Leishmania donovani. Cell Sci. 2014;127:4762–73.
38. Iantorno SA, Durrant C, Khan A S, MJ, Beverley SM, Warren WC, Berriman M S, DL, Cotton JA GM 2017. G expression, By in L is regulated predominantly, Https://doi.org/ gene dosage. mBio 8:e01393-17., 10.1128/mBio.01393-17. Gene Expression in Leishmania Is Regulated Predominantly by Gene Dosage. 2017;8(5):1–20.
39. Hassani K, Antoniak E, Jardim A, Olivier M. Temperature-induced protein secretion by leishmania mexicana modulates macrophage signalling and function. PLoS One. 2011;6(5).
40. de Koning TJ, Snell K, Duran M, Berger R, Poll-The B-T, Surtees R. L-serine in disease and development. Biochem J [Internet]. 2003 May 1 [cited 2018 Dec 26];371(Pt 3):653–61. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12534373
41. Alves CR, Souza RS de, Charret K dos S, Côrtes LM de C, Sá-Silva MP de, Barral-Veloso L, et al. Understanding serine proteases implications on Leishmania spp lifecycle. Exp Parasitol [Internet]. 2018;184:67–81. Available from: https://doi.org/10.1016/j.exppara.2017.11.008
42. Chaves LF, Calzada JE, Valderrama A, Saldaña A. Cutaneous Leishmaniasis and Sand Fly Fluctuations Are Associated with El Niño in Panamá. PLoS Negl Trop Dis. 2014;8(10).
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spelling Ballesteros, NathaliaPatiño, Luz HelenaCruz-Saavedra, LissaRamírez, Juan David1011716118600Vásquez Carreño, Nubia MarcelaBiólogoFull time98311856-ffbb-42bd-b3c5-15366a9e7e186002019-02-11T14:04:29Z2019-02-11T14:04:29Z2019-01-172019The leishmaniases are complex neglected diseases caused by the protozoan parasite Leishmania. Cutaneous leishmaniasis is the most common clinical manifestation around the world, and in the Americas the main aetiological agent is Leishmania braziliensis. In recent studies, chromosome and gene copy number variations (CNVs) have been highlighted as some mechanisms used by Leishmania species to adapt to environmental changes such as host change or drug pressure. However, no studies have described the impact of temperature shifts across the genome of Leishmania promastigotes and particularly in L. braziliensis. Therefore, we sequenced the genome (DNA-Seq) of L. braziliensis promastigotes from cultures subjected to three different temperatures, 24, 28, and 30°C; then, we analysed the aneuploidy, gene CNVs, SNPs and Indels compared with those at the control temperature (26°C). We found that the increase in temperature at 30°C had a negative effect on promastigotes proliferation; although, there were no changes in the somy, SNPs and Indels on the DNA among the three temperatures compared to the control. Only around 3% of the genes having significant copy number variation (CNVs) at each temperature showed some important genes for adaptation to temperature shifts. In conclusion, there is not a relevant genome response to the temperature shift in short-term, therefore the adaptation of this species to abiotic change could be occurring at transcriptome level. The ecological consequences are herein discussed.2021-02-12 01:01:01: Script de automatizacion de embargos. info:eu-repo/date/embargoEnd/2021-02-11application/pdfhttps://doi.org/10.48713/10336_19033 http://repository.urosario.edu.co/handle/10336/19033spaUniversidad del RosarioFacultad de Ciencias Naturales y MatemáticasBiologíaAtribución-NoComercial-SinDerivadas 2.5 ColombiaAbierto (Texto Completo)EL AUTOR, manifiesta que la obra objeto de la presente autorización es original y la realizó sin violar o usurpar derechos de autor de terceros, por lo tanto la obra es de exclusiva autoría y tiene la titularidad sobre la misma.http://creativecommons.org/licenses/by-nc-nd/2.5/co/http://purl.org/coar/access_right/c_abf21. Liang L, Gong P. Climate change and human infectious diseases: A synthesis of research findings from global and spatio-temporal perspectives. Environ Int. 2017;103:99–108.2. Lafferty KD, Mordecai EA. The rise and fall of infectious disease in a warmer world. F1000Research. 2016;5(0):2040.3. Wu X, Lu Y, Zhou S, Chen L, Xu B. Impact of climate change on human infectious diseases: Empirical evidence and human adaptation. Environ Int [Internet]. 2016;86:14–23. Available from: http://dx.doi.org/10.1016/j.envint.2015.09.0074. Ramírez JD, Hernández C, León CM, Ayala MS, Flórez C, González C. Taxonomy, diversity, temporal and geographical distribution of Cutaneous Leishmaniasis in Colombia: A retrospective study. Sci Rep [Internet]. 2016;6(March):1–10. Available from: http://dx.doi.org/10.1038/srep282665. Patino LH, Mendez C, Rodriguez O, Romero Y, Velandia D, Alvarado M, et al. Spatial distribution, Leishmania species and clinical traits of Cutaneous Leishmaniasis cases in the Colombian army. PLoS Negl Trop Dis. 2017;11(8):1–15.6. Hlavacova J, Votypka J, Volf P. The Effect of Temperature on Leishmania (Kinetoplastida: Trypanosomatidae) Development in Sand Flies. J Med Entomol. 2013;50(4):1–4.7. Leon LL, Soares MJ, Temporal RM. Effects of Temperature on Promastigotes of Several Species of Leishmania. 1995;42(3):219–23.8. Zilberstein D, Shapira M. THE ROLE OF pH AND TEMPERATURE IN THE DEVELOPMENT OF LEISHMANIA PARASITES. Annu Rev Microbiol. 1994;48:449–70.9. Cardenas R, Sandoval C, Rodriguez-Morales a. P530 Impact of climate variability in the occurrence of leishmaniasis in Southern departments of Colombia. Int J Antimicrob Agents. 2007;29(2):S117–8.10. González C, Wang O, Strutz SE, González-Salazar C, Sánchez-Cordero V, Sarkar S. Climate change and risk of leishmaniasis in North America: Predictions from ecological niche models of vector and reservoir species. PLoS Negl Trop Dis. 2010;4(1).11. Koch LK, Kochmann J, Klimpel S, Cunze S. Modeling the climatic suitability of leishmaniasis vector species in Europe. Sci Rep [Internet]. 2017;7(1):1–10. Available from: http://dx.doi.org/10.1038/s41598-017-13822-1.12. Rajesh K, Sanjay K. Change in global Climate and Prevalence of Visceral Leishmaniasis. Int J Sci Res Publ. 2013;3(1):2250–3153.13. Lawrence F, Robert-gero M. Induction of heat shock and stress proteins promastigotes of three Leishmania species. Proc Natl Acad Sci USA. 1985;82(July):4414–7.14. Folgueira C, Quijada L, Soto M, Abanades DR, Alonso C, Requena JM. The translational efficiencies of the two Leishmania infantum HSP70 mRNAs, differing in their 3′-untranslated regions, are affected by shifts in the temperature of growth through different mechanisms. J Biol Chem. 2005;280(42):35172–83.15. Toye, Philip and HR "The influence of temperature and serum deprivation on the synthesis of heat-shock proteins and alpha and beta tubulin in promastigotes of L major. . M and biochemical parasitology 35. . (1989): 1-10. Leishmania major. 1988;167(March):1–10.16. Rastrojo A, García-Hernández R, Vargas P, Camacho E, Corvo L, Imamura H, et al. Genomic and transcriptomic alterations in Leishmania donovani lines experimentally resistant to antileishmanial drugs. Int J Parasitol Drugs Drug Resist. 2018;8(2).17. Dumetz F, Imamura H, Sanders M, Seblova V, Myskova J, Pescher P. Modulation of Aneuploidy in Leishmania In Vitro and In Vivo Environments and Its. MBio. 2017;8(3):e00599-17.18. Giovanni Bussotti, a B, Evi Gouzelou B, Mariana Côrtes Boité, c Ihcen Kherachi D, Zoubir Harrat, d Naouel Eddaikra D, Jeremy C. Mottram, e Maria Antoniou F, Vasiliki Christodoulou F, et al. crossm Leishmania Genome Dynamics during Environmental Adaptation Reveal Strain-Specific Differences in Gene Copy. 2018;9(6):1–18.19. Barja PP, Pescher P, Bussotti G, Dumetz F, Imamura H, Kedra D, et al. Haplotype selection as an adaptive mechanism in the protozoan pathogen Leishmania donovani. Nat Ecol Evol. 2017;1(12):1961.20. Shaw CD, Lonchamp J, Downing T, Imamura H, Freeman TM, Cotton JA, et al. In vitro selection of miltefosine resistance in promastigotes of Leishmania donovani from Nepal: Genomic and metabolomic characterization. Mol Microbiol. 2016;99(6):1134–48.21. Mondelaers A, Sanchez-Cañete MP, Hendrickx S, Eberhardt E, Garcia-Hernandez R, Lachaud L, et al. Genomic and Molecular Characterization of Miltefosine Resistance in Leishmania infantum Strains with Either Natural or Acquired Resistance through Experimental Selection of Intracellular Amastigotes. PLoS One. 2016;11(4):e0154101.22. Downing T, Imamura H, Decuypere S. Whole genome sequencing of multiple Leishmania donovani clinical isolates provides insights into population structure and mechanisms of drug resistance. Genome [Internet]. 2011;21:2143–56. Available from: http://genome.cshlp.org/content/early/2011/10/27/gr.123430.111.abstract23. Vanaerschot M, Decuypere S, Downing T, Imamura H, Stark O, De Doncker S, et al. Genetic markers for SSG resistance in leishmania donovani and SSG treatment failure in visceral leishmaniasis patients of the Indian subcontinent. J Infect Dis. 2012;206(5):752–5.24. Valdivia HO, Reis-Cunha JL, Rodrigues-Luiz GF, Baptista RP, Baldeviano GC, Gerbasi R V., et al. Comparative genomic analysis of Leishmania (Viannia) peruviana and Leishmania (Viannia) braziliensis. BMC Genomics [Internet]. 2015;16(1):1–10. Available from: http://dx.doi.org/10.1186/s12864-015-1928-z25. Coughlan S, Taylor AS, Feane E, Sanders M, Schonian G, Cotton JA, et al. Leishmania naiffi and Leishmania guyanensis reference genomes highlight genome structure and gene evolution in the Viannia subgenus. R Soc Open Sci. 2018;5(4).26. Dujardin JC, Mannaert A, Durrant C, Cotton JA. Mosaic aneuploidy in Leishmania: The perspective of whole genome sequencing. Trends Parasitol [Internet]. 2014;30(12):554–5. Available from: http://dx.doi.org/10.1016/j.pt.2014.09.00427. Lean JL, Rind DH. How will Earth’s surface temperature change in future decades? Geophys Res Lett. 2009;36(15):1–5.28. Rogers MB, Hilley JD, Dickens NJ, Wilkes J, Bates PA, Depledge DP, et al. 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