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

Silveira, Fernando Tobias; Sousa Junior, Edivaldo Costa; Silvestre, Rodrigo Vellasco Duarte; Vasconcelos dos Santos, Thiago; Sosa-Ochoa, Wilfredo; Valeriano, Concepción Zúniga; Ramos, Patrícia Karla Santos; Casseb, Samir Mansour Moraes; Lima, Luciana Vieira do Rêgo; Campos, Marliane Batista; da Matta, Vania Lucia; Gomes, Claudia Maria; Flores, Gabriela V. Araujo; Sandoval Pacheco, Carmen M.; Corbett, Carlos Eduardo; Laurenti, Márcia Dalastra

doi:10.3390/microorganisms11010025

Open AccessArticle

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

by

Fernando Tobias Silveira

^1,2,*,†

,

Edivaldo Costa Sousa Junior

¹,

Rodrigo Vellasco Duarte Silvestre

³,

Thiago Vasconcelos dos Santos

¹

,

Wilfredo Sosa-Ochoa

⁴

,

Concepción Zúniga Valeriano

⁵,

Patrícia Karla Santos Ramos

¹,

Samir Mansour Moraes Casseb

⁶,

Luciana Vieira do Rêgo Lima

¹

,

Marliane Batista Campos

¹,

Vania Lucia da Matta

⁷

,

Claudia Maria Gomes

⁷

,

Gabriela V. Araujo Flores

⁷,

Carmen M. Sandoval Pacheco

⁷,

Carlos Eduardo Corbett

⁷ and

Márcia Dalastra Laurenti

^7,†

¹

Parasitology Department, Evandro Chagas Institute, Ananindeua 67030-000, Pará State, Brazil

²

Tropical Medicine Nucleus, Federal University of Pará, Belém 66055-240, Pará State, Brazil

³

Virology Department, Evandro Chagas Institute, Ananindeua 67030-000, Pará State, Brazil

⁴

Microbiology School, National Autonomous University of Honduras, Tegucigalpa 11101, Honduras

⁵

Health Surveillance Department, School Hospital, Autonomous University of Honduras, Tegucigalpa 11101, Honduras

⁶

Arbovirology Department, Evandro Chagas Institute, Ananindeua 67030-000, Pará State, Brazil

⁷

Pathology Laboratory of Infectious Diseases (LIM50), Pathology Department, Medical School, São Paulo University, São Paulo 1246-903, São Paulo State, Brazil

^*

Author to whom correspondence should be addressed.

^†

These authors contributed equally to this work.

Microorganisms 2023, 11(1), 25; https://doi.org/10.3390/microorganisms11010025

Submission received: 27 October 2022 / Revised: 5 December 2022 / Accepted: 16 December 2022 / Published: 21 December 2022

(This article belongs to the Special Issue Advances in Leishmania Research: From Basic Parasite Biology to Disease Control)

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Abstract

Visceral leishmaniasis (VL), also known as kala-azar, is an anthropozoonotic disease affecting human populations on five continents. Aetiologic agents belong to the Leishmania (L.) donovani complex. Until the 1990s, three leishmanine parasites comprised this complex: L. (L.) donovani Laveran & Mesnil 1903, L. (L.) infantum Nicolle 1908, and L. (L.) chagasi Lainson & Shaw 1987 (=L. chagasi Cunha & Chagas 1937). The VL causal agent in the New World (NW) was previously identified as L. (L.) chagasi. After the development of molecular characterization, however, comparisons between L. (L.) chagasi and L. (L.) infantum showed high similarity, and L. (L.) chagasi was then regarded as synonymous with L. (L.) infantum. It was, therefore, suggested that L. (L.) chagasi 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 (Lutzomyia longipalpis) and a wild mammal reservoir (the fox, Cerdocyon thous), we have recently analyzed by molecular clock comparisons of the DNA polymerase alpha subunit gene the whole-genome sequence of L. (L.) infantum chagasi 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 L. (L.) donovani (India) and L. (L.) infantum (Europe), which revealed that the Honduran parasite is older ancestry (382,800 ya) than the parasite from Brazil (143,300 ya), L. (L.) donovani (33,776 ya), or L. (L.) infantum (13,000 ya). 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 L. (L.) donovani], 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 ya) represent strong evidence that L. (L.) chagasi/L. (L.) infantum chagasi 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 Leishmania species causing ADL in Central America.

Keywords: New and Old World; visceral leishmaniasis agents; Leishmania (L.) donovani; Leishmania (L.) infantum; Leishmania (L.) infantum chagasi; comparative genomic analyses

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MDPI and ACS Style

Silveira, F.T.; Sousa Junior, E.C.; Silvestre, R.V.D.; Vasconcelos dos Santos, T.; Sosa-Ochoa, W.; Valeriano, C.Z.; Ramos, P.K.S.; Casseb, S.M.M.; Lima, L.V.d.R.; Campos, M.B.; et al. Comparative Genomic Analyses of New and Old World Viscerotropic Leishmanine Parasites: Further Insights into the Origins of Visceral Leishmaniasis Agents. Microorganisms 2023, 11, 25. https://doi.org/10.3390/microorganisms11010025

AMA Style

Silveira FT, Sousa Junior EC, Silvestre RVD, Vasconcelos dos Santos T, Sosa-Ochoa W, Valeriano CZ, Ramos PKS, Casseb SMM, Lima LVdR, Campos MB, et al. Comparative Genomic Analyses of New and Old World Viscerotropic Leishmanine Parasites: Further Insights into the Origins of Visceral Leishmaniasis Agents. Microorganisms. 2023; 11(1):25. https://doi.org/10.3390/microorganisms11010025

Chicago/Turabian Style

Silveira, Fernando Tobias, 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, and et al. 2023. "Comparative Genomic Analyses of New and Old World Viscerotropic Leishmanine Parasites: Further Insights into the Origins of Visceral Leishmaniasis Agents" Microorganisms 11, no. 1: 25. https://doi.org/10.3390/microorganisms11010025

APA Style

Silveira, F. T., Sousa Junior, E. C., Silvestre, R. V. D., Vasconcelos dos Santos, T., Sosa-Ochoa, W., Valeriano, C. Z., Ramos, P. K. S., Casseb, S. M. M., Lima, L. V. d. R., Campos, M. B., da Matta, V. L., Gomes, C. M., Flores, G. V. A., Sandoval Pacheco, C. M., Corbett, C. E., & Laurenti, M. D. (2023). Comparative Genomic Analyses of New and Old World Viscerotropic Leishmanine Parasites: Further Insights into the Origins of Visceral Leishmaniasis Agents. Microorganisms, 11(1), 25. https://doi.org/10.3390/microorganisms11010025

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

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