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      The Dynamics of Lateral Gene Transfer in Genus Leishmania - A Route for Adaptation and Species Diversification

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          Abstract

          Background

          The genome of Leishmania major harbours a comparably high proportion of genes of prokaryote origin, acquired by lateral gene transfer (LGT). Some of these are present in closely related trypanosomatids, while some are detected in Leishmania only. We have evaluated the impact and destiny of LGT in genus Leishmania.

          Methodology/Principal Findings

          To study the dynamics and fate of LGTs we have performed phylogenetic, as well as nucleotide and amino acid composition analyses within orthologous groups of LGTs detected in Leishmania. A set of universal trypanosomatid LGTs was added as a reference group. Both groups of LGTs have, to some extent, ameliorated to resemble the recipient genomes. However, while virtually all of the universal trypanosomatid LGTs are distributed and conserved in the entire genus Leishmania, the LGTs uniquely present in genus Leishmania are more prone to gene loss and display faster rates of evolution. Furthermore, a PCR based approach has been employed to ascertain the presence of a set of twenty LGTs uniquely present in genus Leishmania, and three universal trypanosomatid LGTs, in ten additional strains of Leishmania. Evolutionary rates and predicted expression levels of these LGTs have also been estimated. Ten of the twenty LGTs are distributed and conserved in all species investigated, while the remainder have been subjected to modifications, or undergone pseudogenization, degradation or loss in one or more species.

          Conclusions/Significance

          LGTs unique to the genus Leishmania have been acquired after the divergence of Leishmania from the other trypanosomatids, and are evolving faster than their recipient genomes. This implies that LGT in genus Leishmania is a continuous and dynamic process contributing to species differentiation and speciation. This study also highlights the importance of carefully evaluating these dynamic genes, e.g. as LGTs have been suggested as potential drug targets.

          Author Summary

          Leishmania parasites cause leishmaniasis, a neglected tropical disease, estimated to threaten 350 million people in 88 countries worldwide according to the WHO. The genome of Leishmania major harbours a number of genes, which have been proposed as acquired by lateral gene transfer (LGT) from a broad variety of prokaryote donors. Such genes may prove beneficial for the parasites, e.g. by promoting survival of the parasite in new environments. We have studied orthologs to LGTs previously detected uniquely in L. major as well as LGTs shared also by other trypanosomatids. The universal trypanosomatid LGTs are more conserved within genus Leishmania, as compared to LGTs that are exclusively present in genus Leishmania. One possible explanation to this observation is that these have resided in their host genomes for a longer time period. This explanation strengthens the hypothesis that the LGTs unique to genus Leishmaina were acquired after the divergence from the trypanosomes, rather than before the divergence, and then subsequently lost from the trypanosome lineage. An in-depth analysis of a subset of the LGTs, which are present only in genus Leishmania showed that LGT within genus Leishmania is a dynamic process. LGTs, providing beneficial capabilities to the parasite, are demonstrated to become conserved throughout generic diversification, hence contributing to species differentiation, while LGTs of limited use are degraded and lost.

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          Most cited references45

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          The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications.

          P. Sharp, W Li (1987)
          A simple, effective measure of synonymous codon usage bias, the Codon Adaptation Index, is detailed. The index uses a reference set of highly expressed genes from a species to assess the relative merits of each codon, and a score for a gene is calculated from the frequency of use of all codons in that gene. The index assesses the extent to which selection has been effective in moulding the pattern of codon usage. In that respect it is useful for predicting the level of expression of a gene, for assessing the adaptation of viral genes to their hosts, and for making comparisons of codon usage in different organisms. The index may also give an approximate indication of the likely success of heterologous gene expression.
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            The genome of the African trypanosome Trypanosoma brucei.

            African trypanosomes cause human sleeping sickness and livestock trypanosomiasis in sub-Saharan Africa. We present the sequence and analysis of the 11 megabase-sized chromosomes of Trypanosoma brucei. The 26-megabase genome contains 9068 predicted genes, including approximately 900 pseudogenes and approximately 1700 T. brucei-specific genes. Large subtelomeric arrays contain an archive of 806 variant surface glycoprotein (VSG) genes used by the parasite to evade the mammalian immune system. Most VSG genes are pseudogenes, which may be used to generate expressed mosaic genes by ectopic recombination. Comparisons of the cytoskeleton and endocytic trafficking systems with those of humans and other eukaryotic organisms reveal major differences. A comparison of metabolic pathways encoded by the genomes of T. brucei, T. cruzi, and Leishmania major reveals the least overall metabolic capability in T. brucei and the greatest in L. major. Horizontal transfer of genes of bacterial origin has contributed to some of the metabolic differences in these parasites, and a number of novel potential drug targets have been identified.
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              Horizontal gene transfer in eukaryotic evolution.

              Horizontal gene transfer (HGT; also known as lateral gene transfer) has had an important role in eukaryotic genome evolution, but its importance is often overshadowed by the greater prevalence and our more advanced understanding of gene transfer in prokaryotes. Recurrent endosymbioses and the generally poor sampling of most nuclear genes from diverse lineages have also complicated the search for transferred genes. Nevertheless, the number of well-supported cases of transfer from both prokaryotes and eukaryotes, many with significant functional implications, is now expanding rapidly. Major recent trends include the important role of HGT in adaptation to certain specialized niches and the highly variable impact of HGT in different lineages.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                5 January 2016
                January 2016
                : 10
                : 1
                : e0004326
                Affiliations
                [1 ]Division of Pharmacognosy, Department of Medicinal Chemistry, Biomedical Centre, Uppsala University, Uppsala, Sweden
                [2 ]Department of Microbiology, National Veterinary Institute (SVA), Uppsala, Sweden
                Seattle Biomedical Research Institute, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: CA. Performed the experiments: EV CA. Analyzed the data: EV CA AB. Contributed reagents/materials/analysis tools: CA AB. Wrote the paper: CA EV AB.

                Article
                PNTD-D-15-01117
                10.1371/journal.pntd.0004326
                4711719
                26730948
                9e8e6372-93ba-43d0-b63b-e5fd82d7a2cd
                © 2016 Vikeved et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 25 June 2015
                : 4 December 2015
                Page count
                Figures: 3, Tables: 4, Pages: 21
                Funding
                This work was funded by Grant number 2008-1366, The Swedish Research Council, FORMAS, http://www.formas.se/, CA. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                All obtained sequences are uploaded to GenBank and allocated the following accession numbers: KM411704-KM411876.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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