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      Transcriptomic responses of Biomphalaria pfeifferi to Schistosoma mansoni: Investigation of a neglected African snail that supports more S. mansoni transmission than any other snail species

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Background

          Biomphalaria pfeifferi is highly compatible with the widespread human-infecting blood fluke Schistosoma mansoni and transmits more cases of this parasite to people than any other snail species. For these reasons, B. pfeifferi is the world’s most important vector snail for S. mansoni, yet we know relatively little at the molecular level regarding the interactions between B. pfeifferi and S. mansoni from early-stage sporocyst transformation to the development of cercariae.

          Methodology/Principal findings

          We sought to capture a portrait of the response of B. pfeifferi to S. mansoni as it occurs in nature by undertaking Illumina dual RNA-Seq on uninfected control B. pfeifferi and three intramolluscan developmental stages (1- and 3-days post infection and patent, cercariae-producing infections) using field-derived west Kenyan specimens. A high-quality, well-annotated de novo B. pfeifferi transcriptome was assembled from over a half billion non- S. mansoni paired-end reads. Reads associated with potential symbionts were noted. Some infected snails yielded fewer normalized S. mansoni reads and showed different patterns of transcriptional response than others, an indication that the ability of field-derived snails to support and respond to infection is variable. Alterations in transcripts associated with reproduction were noted, including for the oviposition-related hormone ovipostatin and enzymes involved in metabolism of bioactive amines like dopamine or serotonin. Shedding snails exhibited responses consistent with the need for tissue repair. Both generalized stress and immune factors immune factors (VIgLs, PGRPs, BGBPs, complement C1q-like, chitinases) exhibited complex transcriptional responses in this compatible host-parasite system.

          Significance

          This study provides for the first time a large sequence data set to help in interpreting the important vector role of the neglected snail B. pfeifferi in transmission of S. mansoni, including with an emphasis on more natural, field-derived specimens. We have identified B. pfeifferi targets particularly responsive during infection that enable further dissection of the functional role of these candidate molecules.

          Author summary

          Biomphalaria pfeifferi is the world’s most important snail vector for the widespread human-infecting blood fluke Schistosoma mansoni. Despite this, we know relatively little about the biology of this highly compatible African snail host of S. mansoni, especially for specimens from the field. Using an Illumina-based dual-seq approach, we captured a portrait of the transcriptional responses of Kenyan snails that were either uninfected with S. mansoni, or that harbored 1-day, 3-day, or cercariae-producing infections. Responses to infection were influenced both by the extent of schistosome gene expression and infection duration. We note and discuss several alterations in transcriptional activity in immune, stress and reproduction related genes in infected snails and the B. pfeifferi symbionts detected. Several host genes were highly up-regulated following infection and these might comprise excellent candidates for disruption to diminish compatibility. This study provides for the first time a large sequence dataset to help in interpreting the important vector role of B. pfeifferi in transmission of S. mansoni, including with an emphasis on more natural, field-derived specimens.

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          Most cited references 156

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          Gene ontology: tool for the unification of biology. The Gene Ontology Consortium.

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            Fast gapped-read alignment with Bowtie 2.

            As the rate of sequencing increases, greater throughput is demanded from read aligners. The full-text minute index is often used to make alignment very fast and memory-efficient, but the approach is ill-suited to finding longer, gapped alignments. Bowtie 2 combines the strengths of the full-text minute index with the flexibility and speed of hardware-accelerated dynamic programming algorithms to achieve a combination of high speed, sensitivity and accuracy.
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              Trimmomatic: a flexible trimmer for Illumina sequence data

              Motivation: Although many next-generation sequencing (NGS) read preprocessing tools already existed, we could not find any tool or combination of tools that met our requirements in terms of flexibility, correct handling of paired-end data and high performance. We have developed Trimmomatic as a more flexible and efficient preprocessing tool, which could correctly handle paired-end data. Results: The value of NGS read preprocessing is demonstrated for both reference-based and reference-free tasks. Trimmomatic is shown to produce output that is at least competitive with, and in many cases superior to, that produced by other tools, in all scenarios tested. Availability and implementation: Trimmomatic is licensed under GPL V3. It is cross-platform (Java 1.5+ required) and available at http://www.usadellab.org/cms/index.php?page=trimmomatic Contact: usadel@bio1.rwth-aachen.de Supplementary information: Supplementary data are available at Bioinformatics online.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: Data curationRole: MethodologyRole: SoftwareRole: SupervisionRole: ValidationRole: Writing – original draft
                Role: Funding acquisitionRole: Project administrationRole: ResourcesRole: Supervision
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                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
                18 October 2017
                October 2017
                : 11
                : 10
                Affiliations
                [1 ] Department of Biology, Center for Evolutionary and Theoretical Immunology, University of New Mexico, Albuquerque, New Mexico, United States of America
                [2 ] National Center for Genome Resources, Santa Fe, New Mexico, United States of America
                [3 ] Center for Biotechnology Research and Development, Kenya Medical Research Institute, Nairobi, KEN
                George Washington University School of Medicine and Health Sciences, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Article
                PNTD-D-17-01253
                10.1371/journal.pntd.0005984
                5685644
                29045404
                © 2017 Buddenborg 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.

                Page count
                Figures: 11, Tables: 6, Pages: 42
                Product
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: R01 AI101438
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: P20GM103452
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000057, National Institute of General Medical Sciences;
                Award ID: P30GM110907
                Award Recipient :
                Technical assistance at the University of New Mexico Molecular Biology Facility was supported by the National Institute of General Medical Sciences of the National Institutes of Health under Award Number P30GM110907 ( https://www.nigms.nih.gov) and National Institutes of Health CETI COBRE grant P20GM103452 ( https://www.nigms.nih.gov). The National Institutes of Health grant R01 AI101438 was the main funding source for this study. Research reported in this publication was supported by the New Mexico Institutional Development Award (IDeA) Network for Biomedical Research Excellence (NM-INBRE) Sequencing and Bioinformatics core at the National Center for Genome Resources (NCGR) from the National Institute of General Medical Sciences of the National Institutes of Health under grant number P20GM103451. 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
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Helminths
                Schistosoma
                Schistosoma Mansoni
                Biology and Life Sciences
                Physiology
                Physiological Processes
                Molting
                Medicine and Health Sciences
                Physiology
                Physiological Processes
                Molting
                Biology and Life Sciences
                Immunology
                Immune System Proteins
                Immune Receptors
                Toll-like Receptors
                Medicine and Health Sciences
                Immunology
                Immune System Proteins
                Immune Receptors
                Toll-like Receptors
                Biology and Life Sciences
                Biochemistry
                Proteins
                Immune System Proteins
                Immune Receptors
                Toll-like Receptors
                Biology and Life Sciences
                Cell Biology
                Signal Transduction
                Immune Receptors
                Toll-like Receptors
                Biology and Life Sciences
                Computational Biology
                Genome Analysis
                Transcriptome Analysis
                Biology and Life Sciences
                Genetics
                Genomics
                Genome Analysis
                Transcriptome Analysis
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Molluscs
                Gastropods
                Snails
                Biomphalaria
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Molluscs
                Gastropods
                Snails
                Biology and Life Sciences
                Genetics
                Genomics
                Animal Genomics
                Invertebrate Genomics
                Medicine and Health Sciences
                Parasitic Diseases
                Custom metadata
                vor-update-to-uncorrected-proof
                2017-11-14
                The raw and assembled sequence data are available at NCBI under BioProject ID PRJNA383396. Additional relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology

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