Comparative Genomic Analyses of New and Old World Viscerotropic Leishmanine Parasites: Further Insights into the Origins of Visceral Leishmaniasis Agents

Visceral leishmaniasis (VL), also known as kala-azar, is an anthropozoonotic disease affecting human populations on five continents. Aetiologic agents belong to the <i>Leishmania (L.) donovani</i> complex. Until the 1990s, three leishmanine parasites comprised this complex: <i>L. (...

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Main Authors: Fernando Tobias Silveira, Edivaldo Costa Sousa Junior, Rodrigo Vellasco Duarte Silvestre, Thiago Vasconcelos dos Santos, Wilfredo Sosa-Ochoa, Concepción Zúniga Valeriano, Patrícia Karla Santos Ramos, Samir Mansour Moraes Casseb, Luciana Vieira do Rêgo Lima, Marliane Batista Campos, Vania Lucia da Matta, Claudia Maria Gomes, Gabriela V. Araujo Flores, Carmen M. Sandoval Pacheco, Carlos Eduardo Corbett, Márcia Dalastra Laurenti
Format: Article
Language:English
Published: MDPI AG 2022-12-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/11/1/25
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author Fernando Tobias Silveira
Edivaldo Costa Sousa Junior
Rodrigo Vellasco Duarte Silvestre
Thiago Vasconcelos dos Santos
Wilfredo Sosa-Ochoa
Concepción Zúniga Valeriano
Patrícia Karla Santos Ramos
Samir Mansour Moraes Casseb
Luciana Vieira do Rêgo Lima
Marliane Batista Campos
Vania Lucia da Matta
Claudia Maria Gomes
Gabriela V. Araujo Flores
Carmen M. Sandoval Pacheco
Carlos Eduardo Corbett
Márcia Dalastra Laurenti
author_facet Fernando Tobias Silveira
Edivaldo Costa Sousa Junior
Rodrigo Vellasco Duarte Silvestre
Thiago Vasconcelos dos Santos
Wilfredo Sosa-Ochoa
Concepción Zúniga Valeriano
Patrícia Karla Santos Ramos
Samir Mansour Moraes Casseb
Luciana Vieira do Rêgo Lima
Marliane Batista Campos
Vania Lucia da Matta
Claudia Maria Gomes
Gabriela V. Araujo Flores
Carmen M. Sandoval Pacheco
Carlos Eduardo Corbett
Márcia Dalastra Laurenti
author_sort Fernando Tobias Silveira
collection DOAJ
description Visceral leishmaniasis (VL), also known as kala-azar, is an anthropozoonotic disease affecting human populations on five continents. Aetiologic agents belong to the <i>Leishmania (L.) donovani</i> complex. Until the 1990s, three leishmanine parasites comprised this complex: <i>L. (L.) donovani</i> Laveran & Mesnil 1903, <i>L. (L.) infantum</i> Nicolle 1908, and <i>L. (L.) chagasi</i> Lainson & Shaw 1987 (=<i>L. chagasi</i> Cunha & Chagas 1937). The VL causal agent in the New World (NW) was previously identified as <i>L. (L.) chagasi</i>. After the development of molecular characterization, however, comparisons between <i>L. (L.) chagasi</i> and <i>L. (L.) infantum</i> showed high similarity, and <i>L. (L.) chagasi</i> was then regarded as synonymous with <i>L. (L.) infantum</i>. It was, therefore, suggested that <i>L. (L.) chagasi</i> was not native to the NW but had been introduced from the Old World by Iberian colonizers. However, in light of ecological evidence from the NW parasite’s enzootic cycle involving a wild phlebotomine vector (<i>Lutzomyia longipalpis</i>) and a wild mammal reservoir (the fox, <i>Cerdocyon thous</i>), we have recently analyzed by molecular clock comparisons of the DNA polymerase alpha subunit gene the whole-genome sequence of <i>L. (L.) infantum chagasi</i> of the most prevalent clinical form, atypical dermal leishmaniasis (ADL), from Honduras (Central America) with that of the same parasite from Brazil (South America), as well as those of <i>L. (L.) donovani</i> (India) and <i>L. (L.) infantum</i> (Europe), which revealed that the Honduran parasite is older ancestry (382,800 <i>ya</i>) than the parasite from Brazil (143,300 <i>ya</i>), <i>L. (L.) donovani</i> (33,776 <i>ya</i>), or <i>L. (L.) infantum</i> (13,000 <i>ya</i>). In the present work, we have now amplified the genomic comparisons among these leishmanine parasites, exploring mainly the variations in the genome for each chromosome, and the number of genomic SNPs for each chromosome. Although the results of this new analysis have confirmed a high genomic similarity (~99%) among these parasites [except <i>L. (L.) donovani</i>], the Honduran parasite revealed a single structural variation on chromosome 17, and the highest frequency of genomic SNPs (more than twice the number seen in the Brazilian one), which together to its extraordinary ancestry (382,800 <i>ya</i>) represent strong evidence that <i>L. (L.) chagasi</i>/<i>L. (L.) infantum chagasi</i> is, in fact, native to the NW, and therefore with valid taxonomic status. Furthermore, the Honduran parasite, the most ancestral viscerotropic leishmanine parasite, showed genomic and clinical taxonomic characteristics compatible with a new <i>Leishmania</i> species causing ADL in Central America.
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spelling doaj.art-8906e17baf6b434da8acce9c3bd758252023-11-30T23:35:19ZengMDPI AGMicroorganisms2076-26072022-12-011112510.3390/microorganisms11010025Comparative Genomic Analyses of New and Old World Viscerotropic Leishmanine Parasites: Further Insights into the Origins of Visceral Leishmaniasis AgentsFernando Tobias Silveira0Edivaldo Costa Sousa Junior1Rodrigo Vellasco Duarte Silvestre2Thiago Vasconcelos dos Santos3Wilfredo Sosa-Ochoa4Concepción Zúniga Valeriano5Patrícia Karla Santos Ramos6Samir Mansour Moraes Casseb7Luciana Vieira do Rêgo Lima8Marliane Batista Campos9Vania Lucia da Matta10Claudia Maria Gomes11Gabriela V. Araujo Flores12Carmen M. Sandoval Pacheco13Carlos Eduardo Corbett14Márcia Dalastra Laurenti15Parasitology Department, Evandro Chagas Institute, Ananindeua 67030-000, Pará State, BrazilParasitology Department, Evandro Chagas Institute, Ananindeua 67030-000, Pará State, BrazilVirology Department, Evandro Chagas Institute, Ananindeua 67030-000, Pará State, BrazilParasitology Department, Evandro Chagas Institute, Ananindeua 67030-000, Pará State, BrazilMicrobiology School, National Autonomous University of Honduras, Tegucigalpa 11101, HondurasHealth Surveillance Department, School Hospital, Autonomous University of Honduras, Tegucigalpa 11101, HondurasParasitology Department, Evandro Chagas Institute, Ananindeua 67030-000, Pará State, BrazilArbovirology Department, Evandro Chagas Institute, Ananindeua 67030-000, Pará State, BrazilParasitology Department, Evandro Chagas Institute, Ananindeua 67030-000, Pará State, BrazilParasitology Department, Evandro Chagas Institute, Ananindeua 67030-000, Pará State, BrazilPathology Laboratory of Infectious Diseases (LIM50), Pathology Department, Medical School, São Paulo University, São Paulo 1246-903, São Paulo State, BrazilPathology Laboratory of Infectious Diseases (LIM50), Pathology Department, Medical School, São Paulo University, São Paulo 1246-903, São Paulo State, BrazilPathology Laboratory of Infectious Diseases (LIM50), Pathology Department, Medical School, São Paulo University, São Paulo 1246-903, São Paulo State, BrazilPathology Laboratory of Infectious Diseases (LIM50), Pathology Department, Medical School, São Paulo University, São Paulo 1246-903, São Paulo State, BrazilPathology Laboratory of Infectious Diseases (LIM50), Pathology Department, Medical School, São Paulo University, São Paulo 1246-903, São Paulo State, BrazilPathology Laboratory of Infectious Diseases (LIM50), Pathology Department, Medical School, São Paulo University, São Paulo 1246-903, São Paulo State, BrazilVisceral leishmaniasis (VL), also known as kala-azar, is an anthropozoonotic disease affecting human populations on five continents. Aetiologic agents belong to the <i>Leishmania (L.) donovani</i> complex. Until the 1990s, three leishmanine parasites comprised this complex: <i>L. (L.) donovani</i> Laveran & Mesnil 1903, <i>L. (L.) infantum</i> Nicolle 1908, and <i>L. (L.) chagasi</i> Lainson & Shaw 1987 (=<i>L. chagasi</i> Cunha & Chagas 1937). The VL causal agent in the New World (NW) was previously identified as <i>L. (L.) chagasi</i>. After the development of molecular characterization, however, comparisons between <i>L. (L.) chagasi</i> and <i>L. (L.) infantum</i> showed high similarity, and <i>L. (L.) chagasi</i> was then regarded as synonymous with <i>L. (L.) infantum</i>. It was, therefore, suggested that <i>L. (L.) chagasi</i> was not native to the NW but had been introduced from the Old World by Iberian colonizers. However, in light of ecological evidence from the NW parasite’s enzootic cycle involving a wild phlebotomine vector (<i>Lutzomyia longipalpis</i>) and a wild mammal reservoir (the fox, <i>Cerdocyon thous</i>), we have recently analyzed by molecular clock comparisons of the DNA polymerase alpha subunit gene the whole-genome sequence of <i>L. (L.) infantum chagasi</i> of the most prevalent clinical form, atypical dermal leishmaniasis (ADL), from Honduras (Central America) with that of the same parasite from Brazil (South America), as well as those of <i>L. (L.) donovani</i> (India) and <i>L. (L.) infantum</i> (Europe), which revealed that the Honduran parasite is older ancestry (382,800 <i>ya</i>) than the parasite from Brazil (143,300 <i>ya</i>), <i>L. (L.) donovani</i> (33,776 <i>ya</i>), or <i>L. (L.) infantum</i> (13,000 <i>ya</i>). In the present work, we have now amplified the genomic comparisons among these leishmanine parasites, exploring mainly the variations in the genome for each chromosome, and the number of genomic SNPs for each chromosome. Although the results of this new analysis have confirmed a high genomic similarity (~99%) among these parasites [except <i>L. (L.) donovani</i>], the Honduran parasite revealed a single structural variation on chromosome 17, and the highest frequency of genomic SNPs (more than twice the number seen in the Brazilian one), which together to its extraordinary ancestry (382,800 <i>ya</i>) represent strong evidence that <i>L. (L.) chagasi</i>/<i>L. (L.) infantum chagasi</i> is, in fact, native to the NW, and therefore with valid taxonomic status. Furthermore, the Honduran parasite, the most ancestral viscerotropic leishmanine parasite, showed genomic and clinical taxonomic characteristics compatible with a new <i>Leishmania</i> species causing ADL in Central America.https://www.mdpi.com/2076-2607/11/1/25New and Old Worldvisceral leishmaniasis agents<i>Leishmania (L.) donovani</i><i>Leishmania (L.) infantum</i><i>Leishmania (L.) infantum chagasi</i>comparative genomic analyses
spellingShingle Fernando Tobias Silveira
Edivaldo Costa Sousa Junior
Rodrigo Vellasco Duarte Silvestre
Thiago Vasconcelos dos Santos
Wilfredo Sosa-Ochoa
Concepción Zúniga Valeriano
Patrícia Karla Santos Ramos
Samir Mansour Moraes Casseb
Luciana Vieira do Rêgo Lima
Marliane Batista Campos
Vania Lucia da Matta
Claudia Maria Gomes
Gabriela V. Araujo Flores
Carmen M. Sandoval Pacheco
Carlos Eduardo Corbett
Márcia Dalastra Laurenti
Comparative Genomic Analyses of New and Old World Viscerotropic Leishmanine Parasites: Further Insights into the Origins of Visceral Leishmaniasis Agents
Microorganisms
New and Old World
visceral leishmaniasis agents
<i>Leishmania (L.) donovani</i>
<i>Leishmania (L.) infantum</i>
<i>Leishmania (L.) infantum chagasi</i>
comparative genomic analyses
title Comparative Genomic Analyses of New and Old World Viscerotropic Leishmanine Parasites: Further Insights into the Origins of Visceral Leishmaniasis Agents
title_full Comparative Genomic Analyses of New and Old World Viscerotropic Leishmanine Parasites: Further Insights into the Origins of Visceral Leishmaniasis Agents
title_fullStr Comparative Genomic Analyses of New and Old World Viscerotropic Leishmanine Parasites: Further Insights into the Origins of Visceral Leishmaniasis Agents
title_full_unstemmed Comparative Genomic Analyses of New and Old World Viscerotropic Leishmanine Parasites: Further Insights into the Origins of Visceral Leishmaniasis Agents
title_short Comparative Genomic Analyses of New and Old World Viscerotropic Leishmanine Parasites: Further Insights into the Origins of Visceral Leishmaniasis Agents
title_sort comparative genomic analyses of new and old world viscerotropic leishmanine parasites further insights into the origins of visceral leishmaniasis agents
topic New and Old World
visceral leishmaniasis agents
<i>Leishmania (L.) donovani</i>
<i>Leishmania (L.) infantum</i>
<i>Leishmania (L.) infantum chagasi</i>
comparative genomic analyses
url https://www.mdpi.com/2076-2607/11/1/25
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