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      Comparative genomics of Leishmania ( Mundinia)

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          Abstract

          Background

          Trypanosomatids of the genus Leishmania are parasites of mammals or reptiles transmitted by bloodsucking dipterans. Many species of these flagellates cause important human diseases with clinical symptoms ranging from skin sores to life-threatening damage of visceral organs. The genus Leishmania contains four subgenera: Leishmania, Sauroleishmania, Viannia, and Mundinia. The last subgenus has been established recently and remains understudied, although Mundinia contains human-infecting species. In addition, it is interesting from the evolutionary viewpoint, representing the earliest branch within the genus and possibly with a different type of vector. Here we analyzed the genomes of L. ( M.) martiniquensis, L. ( M.) enriettii and L. ( M.) macropodum to better understand the biology and evolution of these parasites.

          Results

          All three genomes analyzed were approximately of the same size (~ 30 Mb) and similar to that of L. ( Sauroleishmania) tarentolae, but smaller than those of the members of subgenera Leishmania and Viannia, or the genus Endotrypanum (~ 32 Mb). This difference was explained by domination of gene losses over gains and contractions over expansions at the Mundinia node, although only a few of these genes could be identified. The analysis predicts significant changes in the Mundinia cell surface architecture, with the most important ones relating to losses of LPG-modifying side chain galactosyltransferases and arabinosyltransferases, as well as β-amastins. Among other important changes were gene family contractions for the oxygen-sensing adenylate cyclases and FYVE zinc finger-containing proteins.

          Conclusions

          We suggest that adaptation of Mundinia to different vectors and hosts has led to alternative host-parasite relationships and, thereby, made some proteins redundant. Thus, the evolution of genomes in the genus Leishmania and, in particular, in the subgenus Mundinia was mainly shaped by host (or vector) switches.

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          Most cited references77

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          Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood.

          Count is a software package for the analysis of numerical profiles on a phylogeny. It is primarily designed to deal with profiles derived from the phyletic distribution of homologous gene families, but is suited to study any other integer-valued evolutionary characters. Count performs ancestral reconstruction, and infers family- and lineage-specific characteristics along the evolutionary tree. It implements popular methods employed in gene content analysis such as Dollo and Wagner parsimony, propensity for gene loss, as well as probabilistic methods involving a phylogenetic birth-and-death model. Count is available as a stand-alone Java application, as well as an application bundle for MacOS X, at the web site http://www.iro.umontreal.ca/ approximately csuros/gene_content/count.html. It can also be launched using Java Webstart from the same site. The software is distributed under a BSD-style license. Source code is available upon request from the author.
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            Chromosome and gene copy number variation allow major structural change between species and strains of Leishmania.

            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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              Evolution of parasitism in kinetoplastid flagellates.

              Kinetoplastid protists offer a unique opportunity for studying the evolution of parasitism. While all their close relatives are either photo- or phagotrophic, a number of kinetoplastid species are facultative or obligatory parasites, supporting a hypothesis that parasitism has emerged within this group of flagellates. In this review we discuss origin and evolution of parasitism in bodonids and trypanosomatids and specific adaptations allowing these protozoa to co-exist with their hosts. We also explore the limits of biodiversity of monoxenous (one host) trypanosomatids and some features distinguishing them from their dixenous (two hosts) relatives.
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                Author and article information

                Contributors
                rolando24@yandex.ru
                kostygov@gmail.com
                jovanaS@seznam.cz
                ykleschenko@gmail.com
                tomasbecvar94@gmail.com
                podesvoval@email.cz
                diegohqm@gmail.com
                zihaladavid@gmail.com
                jula@paru.cas.cz
                p.bates@lancaster.ac.uk
                volf@cesnet.cz
                fred.opperdoes@telenet.be
                vyacheslav.yurchenko@osu.cz
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                11 October 2019
                11 October 2019
                2019
                : 20
                : 726
                Affiliations
                [1 ]ISNI 0000 0001 2155 4545, GRID grid.412684.d, Life Science Research Centre, Faculty of Science, , University of Ostrava, ; Ostrava, Czech Republic
                [2 ]ISNI 0000 0001 1015 3316, GRID grid.418095.1, Biology Centre, Institute of Parasitology, , Czech Academy of Sciences, ; České Budejovice (Budweis), Czech Republic
                [3 ]ISNI 0000 0001 2314 7601, GRID grid.439287.3, Zoological Institute of the Russian Academy of Sciences, ; St Petersburg, Russia
                [4 ]ISNI 0000 0004 1937 116X, GRID grid.4491.8, Department of Parasitology, Faculty of Science, , Charles University, ; Prague, Czech Republic
                [5 ]ISNI 0000 0001 2288 8774, GRID grid.448878.f, Martsinovsky Institute of Medical Parasitology, Tropical and Vector Borne Diseases, , Sechenov University, ; Moscow, Russia
                [6 ]ISNI 0000 0001 2166 4904, GRID grid.14509.39, Faculty of Sciences, , University of South Bohemia, ; České Budejovice (Budweis), Czech Republic
                [7 ]ISNI 0000 0000 8190 6402, GRID grid.9835.7, Division of Biomedical and Life Sciences, Faculty of Health and Medicine, , Lancaster University, ; Lancaster, UK
                [8 ]ISNI 0000 0001 2294 713X, GRID grid.7942.8, de Duve Institute, , Université Catholique de Louvain, ; Brussels, Belgium
                Author information
                http://orcid.org/0000-0003-4765-3263
                Article
                6126
                10.1186/s12864-019-6126-y
                6787982
                31601168
                4430afcd-59d5-47fb-9894-750eefc312d7
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 2 April 2019
                : 20 September 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100008530, European Regional Development Fund;
                Award ID: OPVVV 16_019/0000759
                Award ID: OPVVV 16_019/0000759
                Award ID: OPVVV 16_019/0000759
                Award ID: OPVVV 16_019/0000759
                Award ID: OPVVV 16_019/0000759
                Award Recipient :
                Funded by: Grantová Agentura České Republiky (CZ)
                Award ID: 17-10656S
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100006704, Ostravská Univerzita v Ostravě;
                Award ID: SGS08/PrF/2019
                Award ID: SGS08/PrF/2019
                Award Recipient :
                Funded by: Ostravská Univerzita v Ostravě (CZ)
                Award ID: SGS08/PrF/2019
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100006769, Russian Science Foundation;
                Award ID: 17-10656S
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Genetics
                whole genome sequencing,leishmania (mundinia) enriettii,l. (m.) macropodum,l. (m.) martiniquensis

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