The in vivo transcriptome of Schistosoma mansoni in the prominent vector species Biomphalaria pfeifferi with supporting observations from B . glabrata
Background The full scope of the genes expressed by schistosomes during intramolluscan development has yet to be characterized. Understanding the gene products deployed by larval schistosomes in their snail hosts will provide insights into their establishment, maintenance, asexual reproduction, abil...
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description | Background The full scope of the genes expressed by schistosomes during intramolluscan development has yet to be characterized. Understanding the gene products deployed by larval schistosomes in their snail hosts will provide insights into their establishment, maintenance, asexual reproduction, ability to castrate their hosts, and their prolific production of human-infective cercariae. Using the Illumina platform, the intramolluscan transcriptome of Schistosoma mansoni was investigated in field-derived specimens of the prominent vector species Biomphalaria pfeifferi at 1 and 3 days post infection (d) and from snails shedding cercariae. These S. mansoni samples were derived from the same snails used in our complementary B. pfeifferi transcriptomic study. We supplemented this view with microarray analyses of S. mansoni from B. glabrata at 2d, 4d, 8d, 16d, and 32d to highlight robust features of S. mansoni transcription, even when a different technique and vector species was used. Principal findings Transcripts representing at least 7,740 (66%) of known S. mansoni genes were expressed during intramolluscan development, with the greatest number expressed in snails shedding cercariae. Many transcripts were constitutively expressed throughout development featuring membrane transporters, and metabolic enzymes involved in protein and nucleic acid synthesis and cell division. Several proteases and protease inhibitors were expressed at all stages, including some proteases usually associated with cercariae. Transcripts associated with G-protein coupled receptors, germ cell perpetuation, and stress responses and defense were well represented. We noted transcripts homologous to planarian anti-bacterial factors, several neural development or neuropeptide transcripts including neuropeptide Y, and receptors that may be associated with schistosome germinal cell maintenance that could also impact host reproduction. In at least one snail the presence of larvae of another digenean species (an amphistome) was associated with repressed S. mansoni transcriptional activity. Conclusions/Significance This in vivo study, emphasizing field-derived snails and schistosomes, but supplemented with observations from a lab model, provides a distinct view from previous studies of development of cultured intramolluscan stages from lab-maintained organisms. We found many highly represented transcripts with suspected or unknown functions, with connection to intramolluscan development yet to be |
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Understanding the gene products deployed by larval schistosomes in their snail hosts will provide insights into their establishment, maintenance, asexual reproduction, ability to castrate their hosts, and their prolific production of human-infective cercariae. Using the Illumina platform, the intramolluscan transcriptome of Schistosoma mansoni was investigated in field-derived specimens of the prominent vector species Biomphalaria pfeifferi at 1 and 3 days post infection (d) and from snails shedding cercariae. These S. mansoni samples were derived from the same snails used in our complementary B. pfeifferi transcriptomic study. We supplemented this view with microarray analyses of S. mansoni from B. glabrata at 2d, 4d, 8d, 16d, and 32d to highlight robust features of S. mansoni transcription, even when a different technique and vector species was used. Principal findings Transcripts representing at least 7,740 (66%) of known S. mansoni genes were expressed during intramolluscan development, with the greatest number expressed in snails shedding cercariae. Many transcripts were constitutively expressed throughout development featuring membrane transporters, and metabolic enzymes involved in protein and nucleic acid synthesis and cell division. Several proteases and protease inhibitors were expressed at all stages, including some proteases usually associated with cercariae. Transcripts associated with G-protein coupled receptors, germ cell perpetuation, and stress responses and defense were well represented. We noted transcripts homologous to planarian anti-bacterial factors, several neural development or neuropeptide transcripts including neuropeptide Y, and receptors that may be associated with schistosome germinal cell maintenance that could also impact host reproduction. In at least one snail the presence of larvae of another digenean species (an amphistome) was associated with repressed S. mansoni transcriptional activity. Conclusions/Significance This in vivo study, emphasizing field-derived snails and schistosomes, but supplemented with observations from a lab model, provides a distinct view from previous studies of development of cultured intramolluscan stages from lab-maintained organisms. We found many highly represented transcripts with suspected or unknown functions, with connection to intramolluscan development yet to be elucidated.</description><identifier>ISSN: 1935-2727</identifier><identifier>EISSN: 1935-2735</identifier><identifier>DOI: 10.1371/journal.pntd.0007013</identifier><language>eng</language><publisher>San Francisco: Public Library of Science</publisher><subject>Antibiotics ; Antiinfectives and antibacterials ; Asexual reproduction ; Bacterial infections ; Biology ; Biomphalaria pfeifferi ; Cell division ; Cellular stress response ; Developmental stages ; DNA microarrays ; Gastropoda ; Gene expression ; Gene products ; Genes ; Genomes ; Homology ; Hosts ; Immunology ; In vivo methods and tests ; Infections ; Larvae ; Maintenance ; Mollusks ; Neuropeptide Y ; Parasites ; Parasitic diseases ; Protease inhibitors ; Protein biosynthesis ; Proteinase inhibitors ; Proteins ; R&D ; Receptors ; Reproduction ; Research & development ; Schistosoma mansoni ; Shedding ; Snails ; Species ; Transcription ; Tropical diseases</subject><ispartof>PLoS neglected tropical diseases, 2019-09, Vol.13 (9), p.e0007013</ispartof><rights>2019 Buddenborg et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://journals.plos.org/plosone/article/file?id=10.1371/journal.pntd.0007013&type=printable$$EPDF$$P50$$Gplos$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://journals.plos.org/plosone/article?id=10.1371/journal.pntd.0007013$$EHTML$$P50$$Gplos$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,860,23845,27901,27902,79569,79570</link.rule.ids></links><search><creatorcontrib>Buddenborg, Sarah K</creatorcontrib><creatorcontrib>Kamel, Bishoy</creatorcontrib><creatorcontrib>Hanelt, Ben</creatorcontrib><creatorcontrib>Bu, Lijing</creatorcontrib><creatorcontrib>Si-Ming, Zhang</creatorcontrib><creatorcontrib>Mkoji, Gerald M</creatorcontrib><creatorcontrib>Loker, Eric S</creatorcontrib><title>The in vivo transcriptome of Schistosoma mansoni in the prominent vector species Biomphalaria pfeifferi with supporting observations from B . glabrata</title><title>PLoS neglected tropical diseases</title><description>Background The full scope of the genes expressed by schistosomes during intramolluscan development has yet to be characterized. Understanding the gene products deployed by larval schistosomes in their snail hosts will provide insights into their establishment, maintenance, asexual reproduction, ability to castrate their hosts, and their prolific production of human-infective cercariae. Using the Illumina platform, the intramolluscan transcriptome of Schistosoma mansoni was investigated in field-derived specimens of the prominent vector species Biomphalaria pfeifferi at 1 and 3 days post infection (d) and from snails shedding cercariae. These S. mansoni samples were derived from the same snails used in our complementary B. pfeifferi transcriptomic study. We supplemented this view with microarray analyses of S. mansoni from B. glabrata at 2d, 4d, 8d, 16d, and 32d to highlight robust features of S. mansoni transcription, even when a different technique and vector species was used. Principal findings Transcripts representing at least 7,740 (66%) of known S. mansoni genes were expressed during intramolluscan development, with the greatest number expressed in snails shedding cercariae. Many transcripts were constitutively expressed throughout development featuring membrane transporters, and metabolic enzymes involved in protein and nucleic acid synthesis and cell division. Several proteases and protease inhibitors were expressed at all stages, including some proteases usually associated with cercariae. Transcripts associated with G-protein coupled receptors, germ cell perpetuation, and stress responses and defense were well represented. We noted transcripts homologous to planarian anti-bacterial factors, several neural development or neuropeptide transcripts including neuropeptide Y, and receptors that may be associated with schistosome germinal cell maintenance that could also impact host reproduction. In at least one snail the presence of larvae of another digenean species (an amphistome) was associated with repressed S. mansoni transcriptional activity. Conclusions/Significance This in vivo study, emphasizing field-derived snails and schistosomes, but supplemented with observations from a lab model, provides a distinct view from previous studies of development of cultured intramolluscan stages from lab-maintained organisms. We found many highly represented transcripts with suspected or unknown functions, with connection to intramolluscan development yet to be elucidated.</description><subject>Antibiotics</subject><subject>Antiinfectives and antibacterials</subject><subject>Asexual reproduction</subject><subject>Bacterial infections</subject><subject>Biology</subject><subject>Biomphalaria pfeifferi</subject><subject>Cell division</subject><subject>Cellular stress response</subject><subject>Developmental stages</subject><subject>DNA microarrays</subject><subject>Gastropoda</subject><subject>Gene expression</subject><subject>Gene products</subject><subject>Genes</subject><subject>Genomes</subject><subject>Homology</subject><subject>Hosts</subject><subject>Immunology</subject><subject>In vivo methods and tests</subject><subject>Infections</subject><subject>Larvae</subject><subject>Maintenance</subject><subject>Mollusks</subject><subject>Neuropeptide Y</subject><subject>Parasites</subject><subject>Parasitic diseases</subject><subject>Protease inhibitors</subject><subject>Protein biosynthesis</subject><subject>Proteinase inhibitors</subject><subject>Proteins</subject><subject>R&D</subject><subject>Receptors</subject><subject>Reproduction</subject><subject>Research & development</subject><subject>Schistosoma mansoni</subject><subject>Shedding</subject><subject>Snails</subject><subject>Species</subject><subject>Transcription</subject><subject>Tropical 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glabrata</title><author>Buddenborg, Sarah K ; Kamel, Bishoy ; Hanelt, Ben ; Bu, Lijing ; Si-Ming, Zhang ; Mkoji, Gerald M ; Loker, Eric S</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-p523-945edd3f8b4ffcb13d408345adcd983e80da5ed9ad6278b9c55b994498045fc33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Antibiotics</topic><topic>Antiinfectives and antibacterials</topic><topic>Asexual reproduction</topic><topic>Bacterial infections</topic><topic>Biology</topic><topic>Biomphalaria pfeifferi</topic><topic>Cell division</topic><topic>Cellular stress response</topic><topic>Developmental stages</topic><topic>DNA microarrays</topic><topic>Gastropoda</topic><topic>Gene expression</topic><topic>Gene products</topic><topic>Genes</topic><topic>Genomes</topic><topic>Homology</topic><topic>Hosts</topic><topic>Immunology</topic><topic>In vivo methods and tests</topic><topic>Infections</topic><topic>Larvae</topic><topic>Maintenance</topic><topic>Mollusks</topic><topic>Neuropeptide Y</topic><topic>Parasites</topic><topic>Parasitic diseases</topic><topic>Protease inhibitors</topic><topic>Protein biosynthesis</topic><topic>Proteinase inhibitors</topic><topic>Proteins</topic><topic>R&D</topic><topic>Receptors</topic><topic>Reproduction</topic><topic>Research & development</topic><topic>Schistosoma mansoni</topic><topic>Shedding</topic><topic>Snails</topic><topic>Species</topic><topic>Transcription</topic><topic>Tropical diseases</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Buddenborg, Sarah K</creatorcontrib><creatorcontrib>Kamel, Bishoy</creatorcontrib><creatorcontrib>Hanelt, Ben</creatorcontrib><creatorcontrib>Bu, Lijing</creatorcontrib><creatorcontrib>Si-Ming, Zhang</creatorcontrib><creatorcontrib>Mkoji, Gerald M</creatorcontrib><creatorcontrib>Loker, Eric 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transcriptome of Schistosoma mansoni in the prominent vector species Biomphalaria pfeifferi with supporting observations from B . glabrata</atitle><jtitle>PLoS neglected tropical diseases</jtitle><date>2019-09-01</date><risdate>2019</risdate><volume>13</volume><issue>9</issue><spage>e0007013</spage><pages>e0007013-</pages><issn>1935-2727</issn><eissn>1935-2735</eissn><abstract>Background The full scope of the genes expressed by schistosomes during intramolluscan development has yet to be characterized. Understanding the gene products deployed by larval schistosomes in their snail hosts will provide insights into their establishment, maintenance, asexual reproduction, ability to castrate their hosts, and their prolific production of human-infective cercariae. Using the Illumina platform, the intramolluscan transcriptome of Schistosoma mansoni was investigated in field-derived specimens of the prominent vector species Biomphalaria pfeifferi at 1 and 3 days post infection (d) and from snails shedding cercariae. These S. mansoni samples were derived from the same snails used in our complementary B. pfeifferi transcriptomic study. We supplemented this view with microarray analyses of S. mansoni from B. glabrata at 2d, 4d, 8d, 16d, and 32d to highlight robust features of S. mansoni transcription, even when a different technique and vector species was used. Principal findings Transcripts representing at least 7,740 (66%) of known S. mansoni genes were expressed during intramolluscan development, with the greatest number expressed in snails shedding cercariae. Many transcripts were constitutively expressed throughout development featuring membrane transporters, and metabolic enzymes involved in protein and nucleic acid synthesis and cell division. Several proteases and protease inhibitors were expressed at all stages, including some proteases usually associated with cercariae. Transcripts associated with G-protein coupled receptors, germ cell perpetuation, and stress responses and defense were well represented. We noted transcripts homologous to planarian anti-bacterial factors, several neural development or neuropeptide transcripts including neuropeptide Y, and receptors that may be associated with schistosome germinal cell maintenance that could also impact host reproduction. In at least one snail the presence of larvae of another digenean species (an amphistome) was associated with repressed S. mansoni transcriptional activity. Conclusions/Significance This in vivo study, emphasizing field-derived snails and schistosomes, but supplemented with observations from a lab model, provides a distinct view from previous studies of development of cultured intramolluscan stages from lab-maintained organisms. We found many highly represented transcripts with suspected or unknown functions, with connection to intramolluscan development yet to be elucidated.</abstract><cop>San Francisco</cop><pub>Public Library of Science</pub><doi>10.1371/journal.pntd.0007013</doi><oa>free_for_read</oa></addata></record> |
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subjects | Antibiotics Antiinfectives and antibacterials Asexual reproduction Bacterial infections Biology Biomphalaria pfeifferi Cell division Cellular stress response Developmental stages DNA microarrays Gastropoda Gene expression Gene products Genes Genomes Homology Hosts Immunology In vivo methods and tests Infections Larvae Maintenance Mollusks Neuropeptide Y Parasites Parasitic diseases Protease inhibitors Protein biosynthesis Proteinase inhibitors Proteins R&D Receptors Reproduction Research & development Schistosoma mansoni Shedding Snails Species Transcription Tropical diseases |
title | The in vivo transcriptome of Schistosoma mansoni in the prominent vector species Biomphalaria pfeifferi with supporting observations from B . glabrata |
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