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      Genome of the ramshorn snail Biomphalaria straminea—an obligate intermediate host of schistosomiasis

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          Abstract

          Background

          Schistosomiasis, or bilharzia, is a parasitic disease caused by trematode flatworms of the genus Schistosoma. Infection by Schistosoma mansoni in humans results when cercariae emerge into water from freshwater snails in the genus Biomphalaria and seek out and penetrate human skin. The snail Biomphalaria straminea is native to South America and is now also present in Central America and China, and represents a potential vector host for spreading schistosomiasis. To date, genomic information for the genus is restricted to the neotropical species Biomphalaria glabrata. This limits understanding of the biology and management of other schistosomiasis vectors, such as B. straminea.

          Findings

          Using a combination of Illumina short‐read, 10X Genomics linked‐read, and Hi‐C sequencing data, our 1.005 Gb B. straminea genome assembly is of high contiguity, with a scaffold N50 of 25.3 Mb. Transcriptomes from adults were also obtained. Developmental homeobox genes, hormonal genes, and stress-response genes were identified, and repeat content was annotated (40.68% of genomic content). Comparisons with other mollusc genomes (including Gastropoda, Bivalvia, and Cephalopoda) revealed syntenic conservation, patterns of homeobox gene linkage indicative of evolutionary changes to gene clusters, expansion of heat shock protein genes, and the presence of sesquiterpenoid and cholesterol metabolic pathway genes in Gastropoda. In addition, hormone treatment together with RT-qPCR assay reveal a sesquiterpenoid hormone responsive system in B. straminea, illustrating that this renowned insect hormonal system is also present in the lophotrochozoan lineage.

          Conclusion

          This study provides the first genome assembly for the snail B. straminea and offers an unprecedented opportunity to address a variety of phenomena related to snail vectors of schistosomiasis, as well as evolutionary and genomics questions related to molluscs more widely.

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          Most cited references85

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          clusterProfiler: an R package for comparing biological themes among gene clusters.

          Increasing quantitative data generated from transcriptomics and proteomics require integrative strategies for analysis. Here, we present an R package, clusterProfiler that automates the process of biological-term classification and the enrichment analysis of gene clusters. The analysis module and visualization module were combined into a reusable workflow. Currently, clusterProfiler supports three species, including humans, mice, and yeast. Methods provided in this package can be easily extended to other species and ontologies. The clusterProfiler package is released under Artistic-2.0 License within Bioconductor project. The source code and vignette are freely available at http://bioconductor.org/packages/release/bioc/html/clusterProfiler.html.
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            Fast and accurate short read alignment with Burrows–Wheeler transform

            Motivation: The enormous amount of short reads generated by the new DNA sequencing technologies call for the development of fast and accurate read alignment programs. A first generation of hash table-based methods has been developed, including MAQ, which is accurate, feature rich and fast enough to align short reads from a single individual. However, MAQ does not support gapped alignment for single-end reads, which makes it unsuitable for alignment of longer reads where indels may occur frequently. The speed of MAQ is also a concern when the alignment is scaled up to the resequencing of hundreds of individuals. Results: We implemented Burrows-Wheeler Alignment tool (BWA), a new read alignment package that is based on backward search with Burrows–Wheeler Transform (BWT), to efficiently align short sequencing reads against a large reference sequence such as the human genome, allowing mismatches and gaps. BWA supports both base space reads, e.g. from Illumina sequencing machines, and color space reads from AB SOLiD machines. Evaluations on both simulated and real data suggest that BWA is ∼10–20× faster than MAQ, while achieving similar accuracy. In addition, BWA outputs alignment in the new standard SAM (Sequence Alignment/Map) format. Variant calling and other downstream analyses after the alignment can be achieved with the open source SAMtools software package. Availability: http://maq.sourceforge.net Contact: rd@sanger.ac.uk
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              Basic local alignment search tool.

              A new approach to rapid sequence comparison, basic local alignment search tool (BLAST), directly approximates alignments that optimize a measure of local similarity, the maximal segment pair (MSP) score. Recent mathematical results on the stochastic properties of MSP scores allow an analysis of the performance of this method as well as the statistical significance of alignments it generates. The basic algorithm is simple and robust; it can be implemented in a number of ways and applied in a variety of contexts including straightforward DNA and protein sequence database searches, motif searches, gene identification searches, and in the analysis of multiple regions of similarity in long DNA sequences. In addition to its flexibility and tractability to mathematical analysis, BLAST is an order of magnitude faster than existing sequence comparison tools of comparable sensitivity.
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                Author and article information

                Contributors
                Journal
                Gigascience
                Gigascience
                gigascience
                GigaScience
                Oxford University Press
                2047-217X
                15 February 2022
                2022
                15 February 2022
                : 11
                : giac012
                Affiliations
                School of Life Science, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong , Hong Kong, China
                School of Life Science, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong , Hong Kong, China
                The Scottish Oceans Institute, Gatty Marine Laboratory, School of Biology, University of St. Andrews , St. Andrews, UK
                School of Life Science, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong , Hong Kong, China
                School of Life Science, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong , Hong Kong, China
                School of Life Science, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong , Hong Kong, China
                School of Life Science, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong , Hong Kong, China
                University of Exeter , Exeter, UK
                School of Life Science, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong , Hong Kong, China
                School of Life Science, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong , Hong Kong, China
                Dovetail Genomics , California, USA
                Dovetail Genomics , California, USA
                Institute of Agro-food Standard and Testing Technology, Shanghai Academy of Agricultural Sciences , Shanghai, China
                School of Chemical and Environmental Engineering, Shanghai Institute of Technology , Shanghai, China
                Sun Yat-sen University , Guangdong, China
                Sun Yat-sen University , Guangdong, China
                University of Exeter , Exeter, UK
                The Scottish Oceans Institute, Gatty Marine Laboratory, School of Biology, University of St. Andrews , St. Andrews, UK
                School of Life Science, Simon F.S. Li Marine Science Laboratory, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong , Hong Kong, China
                Author notes
                Correspondence address. Jerome H.L. Hui, E-mail: jeromehui@ 123456cuhk.edu.hk
                Correspondence address. David Ferrier, E-mail: dekf@ 123456st-andrews.ac.uk

                Contributed equally.

                Senior author.

                Author information
                https://orcid.org/0000-0002-3277-716X
                https://orcid.org/0000-0001-6829-0815
                https://orcid.org/0000-0002-1744-5749
                https://orcid.org/0000-0001-5048-5454
                https://orcid.org/0000-0002-1404-7147
                https://orcid.org/0000-0003-4861-942X
                https://orcid.org/0000-0003-2213-2763
                https://orcid.org/0000-0001-5879-9757
                https://orcid.org/0000-0001-7413-718X
                https://orcid.org/0000-0003-3247-6233
                https://orcid.org/0000-0003-1355-8495
                Article
                giac012
                10.1093/gigascience/giac012
                8848322
                35166339
                1a46ab1d-c378-4c81-9e48-6cee7480e20b
                © The Author(s) 2022. Published by Oxford University Press GigaScience.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 10 August 2021
                : 02 January 2022
                : 25 January 2022
                Page count
                Pages: 13
                Funding
                Funded by: National Natural Science Foundation of China, DOI 10.13039/501100001809;
                Award ID: N_CUHK401/21
                Funded by: Chinese University of Hong Kong, DOI 10.13039/501100004853;
                Award ID: 4053433
                Award ID: 4053489
                Funded by: Biotechnology and Biological Sciences Research Council, DOI 10.13039/501100000268;
                Award ID: BB/N020146/1
                Categories
                Research
                AcademicSubjects/SCI00960
                AcademicSubjects/SCI02254

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