Trans-Atlantic Spillover: Deconstructing the Ecological Adaptation of  Leishmania infantum  in the Americas

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Abstract

Pathogen fitness landscapes change when transmission cycles establish in non-native environments or spill over into new vectors and hosts. The introduction of Leishmania infantum in the Americas into the Neotropics during European colonization represents a unique case study to investigate the mechanisms of ecological adaptation of this important parasite. Defining the evolutionary trajectories that drive L. infantum fitness in this new environment are of great public health importance as they will allow unique insight into pathways of host/pathogen co-evolution and their consequences for region-specific changes in disease manifestation. This review summarizes current knowledge on L. infantum genetic and phenotypic diversity in the Americas and its possible role in the unique epidemiology of visceral leishmaniasis (VL) in the New World. We highlight the importance of appreciating adaptive molecular mechanisms in L. infantum to understand the parasite’s successful establishment on the continent.

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A Historical Overview of the Classification, Evolution, and Dispersion of Leishmania Parasites and Sandflies

Mohammad Akhoundi, Katrin Kuhls, Arnaud Cannet … (2016)

Background The aim of this study is to describe the major evolutionary historical events among Leishmania, sandflies, and the associated animal reservoirs in detail, in accordance with the geographical evolution of the Earth, which has not been previously discussed on a large scale. Methodology and Principal Findings Leishmania and sandfly classification has always been a controversial matter, and the increasing number of species currently described further complicates this issue. Despite several hypotheses on the origin, evolution, and distribution of Leishmania and sandflies in the Old and New World, no consistent agreement exists regarding dissemination of the actors that play roles in leishmaniasis. For this purpose, we present here three centuries of research on sandflies and Leishmania descriptions, as well as a complete description of Leishmania and sandfly fossils and the emergence date of each Leishmania and sandfly group during different geographical periods, from 550 million years ago until now. We discuss critically the different approaches that were used for Leishmana and sandfly classification and their synonymies, proposing an updated classification for each species of Leishmania and sandfly. We update information on the current distribution and dispersion of different species of Leishmania (53), sandflies (more than 800 at genus or subgenus level), and animal reservoirs in each of the following geographical ecozones: Palearctic, Nearctic, Neotropic, Afrotropical, Oriental, Malagasy, and Australian. We propose an updated list of the potential and proven sandfly vectors for each Leishmania species in the Old and New World. Finally, we address a classical question about digenetic Leishmania evolution: which was the first host, a vertebrate or an invertebrate? Conclusions and Significance We propose an updated view of events that have played important roles in the geographical dispersion of sandflies, in relation to both the Leishmania species they transmit and the animal reservoirs of the parasites.

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Chromosome and gene copy number variation allow major structural change between species and strains of Leishmania.

Matthew B Rogers, James Hilley, Nicholas J. Dickens … (2011)

Leishmania parasites cause a spectrum of clinical pathology in humans ranging from disfiguring cutaneous lesions to fatal visceral leishmaniasis. We have generated a reference genome for Leishmania mexicana and refined the reference genomes for Leishmania major, Leishmania infantum, and Leishmania braziliensis. This has allowed the identification of a remarkably low number of genes or paralog groups (2, 14, 19, and 67, respectively) unique to one species. These were found to be conserved in additional isolates of the same species. We have predicted allelic variation and find that in these isolates, L. major and L. infantum have a surprisingly low number of predicted heterozygous SNPs compared with L. braziliensis and L. mexicana. We used short read coverage to infer ploidy and gene copy numbers, identifying large copy number variations between species, with 200 tandem gene arrays in L. major and 132 in L. mexicana. Chromosome copy number also varied significantly between species, with nine supernumerary chromosomes in L. infantum, four in L. mexicana, two in L. braziliensis, and one in L. major. A significant bias against gene arrays on supernumerary chromosomes was shown to exist, indicating that duplication events occur more frequently on disomic chromosomes. Taken together, our data demonstrate that there is little variation in unique gene content across Leishmania species, but large-scale genetic heterogeneity can result through gene amplification on disomic chromosomes and variation in chromosome number. Increased gene copy number due to chromosome amplification may contribute to alterations in gene expression in response to environmental conditions in the host, providing a genetic basis for disease tropism.

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Leishmania development in sand flies: parasite-vector interactions overview

Anna Dostálová, Petr Volf (2012)

Leishmaniases are vector-borne parasitic diseases with 0.9 – 1.4 million new human cases each year worldwide. In the vectorial part of the life-cycle, Leishmania development is confined to the digestive tract. During the first few days after blood feeding, natural barriers to Leishmania development include secreted proteolytic enzymes, the peritrophic matrix surrounding the ingested blood meal and sand fly immune reactions. As the blood digestion proceeds, parasites need to bind to the midgut epithelium to avoid being excreted with the blood remnant. This binding is strictly stage-dependent as it is a property of nectomonad and leptomonad forms only. While the attachment in specific vectors (P. papatasi, P. duboscqi and P. sergenti) involves lipophosphoglycan (LPG), this Leishmania molecule is not required for parasite attachment in other sand fly species experimentally permissive for various Leishmania. During late-stage infections, large numbers of parasites accumulate in the anterior midgut and produce filamentous proteophosphoglycan creating a gel-like plug physically obstructing the gut. The parasites attached to the stomodeal valve cause damage to the chitin lining and epithelial cells of the valve, interfering with its function and facilitating reflux of parasites from the midgut. Transformation to metacyclic stages highly infective for the vertebrate host is the other prerequisite for effective transmission. Here, we review the current state of knowledge of molecular interactions occurring in all these distinct phases of parasite colonization of the sand fly gut, highlighting recent discoveries in the field.

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Journal

Journal ID (nlm-ta): Genes (Basel)

Journal ID (iso-abbrev): Genes (Basel)

Journal ID (publisher-id): genes

Title: Genes

Publisher: MDPI

ISSN (Electronic): 2073-4425

Publication date (Electronic): 19 December 2019

Publication date Collection: January 2020

Volume: 11

Issue: 1

Electronic Location Identifier: 4

Affiliations

[1 ]Laboratory of Research on Leishmaniasis, Oswaldo Cruz Institute, FIOCRUZ, 21040-360 Rio de Janeiro, Brazil; renato.porrozzi@ 123456ioc.fiocruz.br (R.P.); morgado@ 123456ioc.fiocruz.br (F.N.M.); elisa.cupolillo@ 123456ioc.fiocruz.br (E.C.)

[2 ]Department of Parasites and Insect Vectors, Laboratory of Molecular Parasitology and Signaling, Institut Pasteur, INSERN U1201, 75015 Paris, France; gerald.spaeth@ 123456pasteur.fr (G.F.S.); giovanni.bussotti@ 123456pasteur.fr (G.B.)

[3 ]Institut Pasteur-Bioinformatics and Biostatistics Hub-C3BI, USR 3756 IP CNRS, 75015 Paris, France

[4 ]Institute of Biodiversity, Animal Health & Comparative Medicine, University of Glasgow, G128QQ Glasgow, UK; martin.llewellyn@ 123456glasgow.ac.uk (M.L.); p.schwabl.1@ 123456research.gla.ac.uk (P.S.)

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[* ]Correspondence: maricboite@ 123456gmail.com ; Tel.: +55-21-38658226

Author information

Mariana C. Boité https://orcid.org/0000-0002-2903-6280

Fernanda N. Morgado https://orcid.org/0000-0002-7188-251X

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Publisher ID: genes-11-00004

DOI: 10.3390/genes11010004

PMC ID: 7017240

PubMed ID: 31861501

SO-VID: 510afd4b-42e9-4653-96ac-e6a3be288591

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Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

Trans-Atlantic Spillover: Deconstructing the Ecological Adaptation of Leishmania infantum in the Americas

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Abstract

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G3: Genes|Genomes|Genetics

Most cited references 58

A Historical Overview of the Classification, Evolution, and Dispersion of Leishmania Parasites and Sandflies

Chromosome and gene copy number variation allow major structural change between species and strains of Leishmania.

Leishmania development in sand flies: parasite-vector interactions overview

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