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      Host-to-Pathogen Gene Transfer Facilitated Infection of Insects by a Pathogenic Fungus

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          Abstract

          Metarhizium robertsii is a plant root colonizing fungus that is also an insect pathogen. Its entomopathogenicity is a characteristic that was acquired during evolution from a plant endophyte ancestor. This transition provides a novel perspective on how new functional mechanisms important for host switching and virulence have evolved. From a random T-DNA insertion library, we obtained a pathogenicity defective mutant that resulted from the disruption of a sterol carrier gene ( Mr-npc2a). Phylogenetic analysis revealed that Metarhizium acquired Mr-npc2a from an insect by horizontal gene transfer (HGT). Mr-NPC2a binds to cholesterol, an animal sterol, rather than the fungal sterol ergosterol, indicating it retains the specificity of insect NPC2 proteins. Mr-NPC2a is an intracellular protein and is exclusively expressed in the hemolymph of living insects. The disruption of Mr-npc2a reduced the amount of sterol in cell membranes of the yeast-like hyphal bodies that facilitate dispersal in the host body. These were consequently more susceptible to insect immune responses than the wild type. Transgenic expression of Mr-NPC2a increased the virulence of Beauveria bassiana, an endophytic insect-pathogenic fungus that lacks a Mr-NPC2a homolog.

          Author Summary

          The ability of infectious agents to evolve different host ranges contributes to the emergence of new diseases, and this host switching could also account for the wide variety of fungal associations with animals, plants and other fungi. There must be mechanisms for such host shifts, but these remain largely unknown. In this study, we phylogenetically predict that the endophytic fungus Metarhizium robertsii acquired a sterol carrier gene from insects through horizontal gene transfer (HGT). This sterol carrier is involved in maintaining cell membrane sterols, and thus membrane integrity, when M. robertsii proliferates in the haemocoel of living insects. Therefore, the acquisition of genetic material from a host has contributed to the development of fungal entomopathogenicity. In order to simulate this evolutionary event, the sterol carrier gene was transformed into an endophytic insect-pathogenic fungus ( Beauveria bassiana) that lacks an endogenous Mr-NPC2a homolog. The virulence of B. bassiana was increased by expression of Mr-NPC2a.

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          Most cited references 42

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          MRBAYES: Bayesian inference of phylogenetic trees.

          The program MRBAYES performs Bayesian inference of phylogeny using a variant of Markov chain Monte Carlo. MRBAYES, including the source code, documentation, sample data files, and an executable, is available at http://brahms.biology.rochester.edu/software.html.
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            ProtTest: selection of best-fit models of protein evolution.

            Using an appropriate model of amino acid replacement is very important for the study of protein evolution and phylogenetic inference. We have built a tool for the selection of the best-fit model of evolution, among a set of candidate models, for a given protein sequence alignment. ProtTest is available under the GNU license from http://darwin.uvigo.es
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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 Pathog
                PLoS Pathog
                plos
                plospath
                PLoS Pathogens
                Public Library of Science (San Francisco, USA )
                1553-7366
                1553-7374
                April 2014
                10 April 2014
                : 10
                : 4
                Affiliations
                [1 ]Institute of Microbiology, College of Life Science, Zhejiang University, Hangzhou, China
                [2 ]Department of Entomology, University of Maryland, College Park, Maryland, United States of America
                Geisel School of Medicine at Dartmouth, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: HZ CX WF. Performed the experiments: HZ CX HLL XC WF. Analyzed the data: HZ CX HLL XC WF. Wrote the paper: HZ CX RJSL WF.

                Article
                PPATHOGENS-D-13-02829
                10.1371/journal.ppat.1004009
                3983072
                24722668

                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.

                Page count
                Pages: 10
                Funding
                This work was funded by the National Natural Science Foundation of China (31272097) and Zhejiang Provincial Natural Science Foundation of China (LR13C010001) and “1000 Young Talents Program of China” to WF and funded by United States Department of Agriculture Cooperative State Research, Education, and Extension Service (2010-65106-20580) to RJSL. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Agriculture
                Pest Control
                Evolutionary Biology
                Evolutionary Genetics
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Microbial Control
                Mycology
                Medicine and Health Sciences
                Infectious Diseases
                Emerging Infectious Diseases
                Pathology and Laboratory Medicine
                Pathogenesis
                Host-Pathogen Interactions

                Infectious disease & Microbiology

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