Ionotropic Receptors Identified within the Tentacle of the Freshwater Snail Biomphalaria glabrata, an Intermediate Host of Schistosoma mansoni
Biomphalaria glabrata (B. glabrata) is an air-breathing aquatic mollusc found in freshwater habitats across the Western Hemisphere. It is most well-known for its recognized capacity to act as a major intermediate host for Schistosoma mansoni, the human blood fluke parasite. Ionotropic receptors (IRs...
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description | Biomphalaria glabrata (B. glabrata) is an air-breathing aquatic mollusc found in freshwater habitats across the Western Hemisphere. It is most well-known for its recognized capacity to act as a major intermediate host for Schistosoma mansoni, the human blood fluke parasite. Ionotropic receptors (IRs), a variant family of the ionotropic glutamate receptors (iGluR), have an evolutionary ancient function in detecting odors to initiate chemosensory signaling. In this study, we applied an array of methods towards the goal of identifying IR-like family members in B. glabrata, ultimately revealing two types, the iGluR and IR. Sequence alignment showed that three ligand-binding residues are conserved in most Biomphalaria iGluR sequences, while the IRs did exhibit a variable pattern, lacking some or all known glutamate-interactingresidues, supporting their distinct classification from the iGluRs. We show that B. glabrata contains 7 putative IRs, some of which are expressed within its chemosensory organs. To further investigate a role for the more ancient IR25a type in chemoreception, we tested its spatial distribution pattern within the snail cephalic tentacle by in situ hybridization. The presence of IR25a within presumptive sensory neurons supports a role for this receptor in olfactory processing, contributing to our understanding of the molecular pathways that are involved in Biomphalaria olfactory processing. |
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It is most well-known for its recognized capacity to act as a major intermediate host for Schistosoma mansoni, the human blood fluke parasite. Ionotropic receptors (IRs), a variant family of the ionotropic glutamate receptors (iGluR), have an evolutionary ancient function in detecting odors to initiate chemosensory signaling. In this study, we applied an array of methods towards the goal of identifying IR-like family members in B. glabrata, ultimately revealing two types, the iGluR and IR. Sequence alignment showed that three ligand-binding residues are conserved in most Biomphalaria iGluR sequences, while the IRs did exhibit a variable pattern, lacking some or all known glutamate-interactingresidues, supporting their distinct classification from the iGluRs. We show that B. glabrata contains 7 putative IRs, some of which are expressed within its chemosensory organs. To further investigate a role for the more ancient IR25a type in chemoreception, we tested its spatial distribution pattern within the snail cephalic tentacle by in situ hybridization. The presence of IR25a within presumptive sensory neurons supports a role for this receptor in olfactory processing, contributing to our understanding of the molecular pathways that are involved in Biomphalaria olfactory processing.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0156380</identifier><identifier>PMID: 27253696</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amino Acid Sequence ; Animals ; Aplysia ; Aquatic habitats ; Biology and Life Sciences ; Biomphalaria ; Biomphalaria - genetics ; Biomphalaria - parasitology ; Biomphalaria glabrata ; Breathing ; Chemoreception ; Chemotherapy ; Conserved sequence ; Crustaceans ; Drosophila melanogaster ; Education ; Fresh Water ; Freshwater environments ; Genetic aspects ; Genomes ; Glutamic acid receptors (ionotropic) ; Host-Parasite Interactions - genetics ; Humans ; Identification methods ; Information processing ; Insects ; Ion channels (ligand-gated) ; Ligands ; Medicine and Health Sciences ; Mollusca ; Neurons ; Neurosciences ; Nucleotide sequence ; Odors ; Organs ; Panulirus argus ; Pathogens ; Physical Sciences ; Physiological aspects ; Physiology ; Proteins ; Receptor mechanisms ; Receptors ; Receptors, Ionotropic Glutamate - genetics ; Receptors, Ionotropic Glutamate - isolation & purification ; Research and Analysis Methods ; Schistosoma mansoni ; Schistosoma mansoni - genetics ; Schistosoma mansoni - pathogenicity ; Schistosomiasis mansoni - genetics ; Schistosomiasis mansoni - parasitology ; Sensory neurons ; Sequence Alignment ; Shellfish ; Signaling ; Snails ; Spatial distribution ; Trematoda ; Western Hemisphere</subject><ispartof>PloS one, 2016-06, Vol.11 (6), p.e0156380-e0156380</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Liang 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><rights>2016 Liang et al 2016 Liang et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c725t-c380855be61ef1807d9c938576e58fd0b37a02cfede595a857d711cd22cea0123</citedby><cites>FETCH-LOGICAL-c725t-c380855be61ef1807d9c938576e58fd0b37a02cfede595a857d711cd22cea0123</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4890853/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4890853/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27253696$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Knight, Matty</contributor><creatorcontrib>Liang, Di</creatorcontrib><creatorcontrib>Wang, Tianfang</creatorcontrib><creatorcontrib>Rotgans, Bronwyn A</creatorcontrib><creatorcontrib>McManus, Donald P</creatorcontrib><creatorcontrib>Cummins, Scott F</creatorcontrib><title>Ionotropic Receptors Identified within the Tentacle of the Freshwater Snail Biomphalaria glabrata, an Intermediate Host of Schistosoma mansoni</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Biomphalaria glabrata (B. glabrata) is an air-breathing aquatic mollusc found in freshwater habitats across the Western Hemisphere. 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The presence of IR25a within presumptive sensory neurons supports a role for this receptor in olfactory processing, contributing to our understanding of the molecular pathways that are involved in Biomphalaria olfactory processing.</description><subject>Amino Acid Sequence</subject><subject>Animals</subject><subject>Aplysia</subject><subject>Aquatic habitats</subject><subject>Biology and Life Sciences</subject><subject>Biomphalaria</subject><subject>Biomphalaria - genetics</subject><subject>Biomphalaria - parasitology</subject><subject>Biomphalaria glabrata</subject><subject>Breathing</subject><subject>Chemoreception</subject><subject>Chemotherapy</subject><subject>Conserved sequence</subject><subject>Crustaceans</subject><subject>Drosophila melanogaster</subject><subject>Education</subject><subject>Fresh Water</subject><subject>Freshwater environments</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Glutamic acid receptors (ionotropic)</subject><subject>Host-Parasite Interactions - 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pathogenicity</subject><subject>Schistosomiasis mansoni - genetics</subject><subject>Schistosomiasis mansoni - parasitology</subject><subject>Sensory neurons</subject><subject>Sequence Alignment</subject><subject>Shellfish</subject><subject>Signaling</subject><subject>Snails</subject><subject>Spatial distribution</subject><subject>Trematoda</subject><subject>Western Hemisphere</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk2Fv0zAQhiMEYqPwDxBYQkIg0WLHtZN8QRoTY5UmTVoHX62r4zSeEjuzXQZ_gt_Mde2mFk0C5UPi83Nv7l77suwloxPGC_bxyq-Cg24yeGcmlAnJS_ooO2QVz8cyp_zxzvdB9izGK0oFL6V8mh3kRS64rORh9nvmnU_BD1aTC6PNkHyIZFYbl2xjTU1ubGqtI6k15BKDoDtDfHO7PgkmtjeQTCBzB7Yjn63vhxY6CBbIsoNFgAQfCDgyc0j1prZIk1Mf01pjrlsbk4--B9KDi97Z59mTBrpoXmzfo-zbyZfL49Px2fnX2fHR2Vhj5WmssddSiIWRzDSspEVd6YqXopBGlE1NF7wAmuvG1EZUAnCjLhjTdZ5rA5TlfJS93ugOnY9qa2VUrKi4KBhnFInZhqg9XKkh2B7CL-XBqtuAD0sFIVm0Q1EhmaS5FLlYTHWzAF5JKBpm6ikrC1ag1qft31YLNEGjjwG6PdH9HWdbtfQ_1LSssE-OAu-2AsFfr0xMqrdRm64DZ_wK60Y7pCxkLv-NYosVVoxdjrI3f6EPG7GlloC9WtfgdQG9FlVHUzHNUYuuW5w8QOFTm95qvKKNxfhewvu9BGSS-ZmWsIpRzeYX_8-ef99n3-6wrYEutdF3q2S9i_vgdAPq4GMMprk_D0bVesLu3FDrCVPbCcO0V7tneZ90N1L8D6JbIU8</recordid><startdate>20160602</startdate><enddate>20160602</enddate><creator>Liang, Di</creator><creator>Wang, Tianfang</creator><creator>Rotgans, Bronwyn A</creator><creator>McManus, Donald P</creator><creator>Cummins, Scott F</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20160602</creationdate><title>Ionotropic Receptors Identified within the Tentacle of the Freshwater Snail Biomphalaria glabrata, an Intermediate Host of Schistosoma mansoni</title><author>Liang, Di ; Wang, Tianfang ; Rotgans, Bronwyn A ; McManus, Donald P ; Cummins, Scott F</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c725t-c380855be61ef1807d9c938576e58fd0b37a02cfede595a857d711cd22cea0123</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Amino Acid Sequence</topic><topic>Animals</topic><topic>Aplysia</topic><topic>Aquatic habitats</topic><topic>Biology and Life Sciences</topic><topic>Biomphalaria</topic><topic>Biomphalaria - genetics</topic><topic>Biomphalaria - parasitology</topic><topic>Biomphalaria glabrata</topic><topic>Breathing</topic><topic>Chemoreception</topic><topic>Chemotherapy</topic><topic>Conserved sequence</topic><topic>Crustaceans</topic><topic>Drosophila melanogaster</topic><topic>Education</topic><topic>Fresh Water</topic><topic>Freshwater environments</topic><topic>Genetic aspects</topic><topic>Genomes</topic><topic>Glutamic acid receptors (ionotropic)</topic><topic>Host-Parasite Interactions - genetics</topic><topic>Humans</topic><topic>Identification methods</topic><topic>Information processing</topic><topic>Insects</topic><topic>Ion channels (ligand-gated)</topic><topic>Ligands</topic><topic>Medicine and Health Sciences</topic><topic>Mollusca</topic><topic>Neurons</topic><topic>Neurosciences</topic><topic>Nucleotide sequence</topic><topic>Odors</topic><topic>Organs</topic><topic>Panulirus argus</topic><topic>Pathogens</topic><topic>Physical Sciences</topic><topic>Physiological aspects</topic><topic>Physiology</topic><topic>Proteins</topic><topic>Receptor mechanisms</topic><topic>Receptors</topic><topic>Receptors, Ionotropic Glutamate - genetics</topic><topic>Receptors, Ionotropic Glutamate - isolation & purification</topic><topic>Research and Analysis Methods</topic><topic>Schistosoma mansoni</topic><topic>Schistosoma mansoni - genetics</topic><topic>Schistosoma mansoni - pathogenicity</topic><topic>Schistosomiasis mansoni - genetics</topic><topic>Schistosomiasis mansoni - parasitology</topic><topic>Sensory neurons</topic><topic>Sequence Alignment</topic><topic>Shellfish</topic><topic>Signaling</topic><topic>Snails</topic><topic>Spatial distribution</topic><topic>Trematoda</topic><topic>Western Hemisphere</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liang, Di</creatorcontrib><creatorcontrib>Wang, Tianfang</creatorcontrib><creatorcontrib>Rotgans, Bronwyn A</creatorcontrib><creatorcontrib>McManus, Donald P</creatorcontrib><creatorcontrib>Cummins, Scott F</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liang, Di</au><au>Wang, Tianfang</au><au>Rotgans, Bronwyn A</au><au>McManus, Donald P</au><au>Cummins, Scott F</au><au>Knight, Matty</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Ionotropic Receptors Identified within the Tentacle of the Freshwater Snail Biomphalaria glabrata, an Intermediate Host of Schistosoma mansoni</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2016-06-02</date><risdate>2016</risdate><volume>11</volume><issue>6</issue><spage>e0156380</spage><epage>e0156380</epage><pages>e0156380-e0156380</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Biomphalaria glabrata (B. glabrata) is an air-breathing aquatic mollusc found in freshwater habitats across the Western Hemisphere. It is most well-known for its recognized capacity to act as a major intermediate host for Schistosoma mansoni, the human blood fluke parasite. Ionotropic receptors (IRs), a variant family of the ionotropic glutamate receptors (iGluR), have an evolutionary ancient function in detecting odors to initiate chemosensory signaling. In this study, we applied an array of methods towards the goal of identifying IR-like family members in B. glabrata, ultimately revealing two types, the iGluR and IR. Sequence alignment showed that three ligand-binding residues are conserved in most Biomphalaria iGluR sequences, while the IRs did exhibit a variable pattern, lacking some or all known glutamate-interactingresidues, supporting their distinct classification from the iGluRs. We show that B. glabrata contains 7 putative IRs, some of which are expressed within its chemosensory organs. To further investigate a role for the more ancient IR25a type in chemoreception, we tested its spatial distribution pattern within the snail cephalic tentacle by in situ hybridization. The presence of IR25a within presumptive sensory neurons supports a role for this receptor in olfactory processing, contributing to our understanding of the molecular pathways that are involved in Biomphalaria olfactory processing.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27253696</pmid><doi>10.1371/journal.pone.0156380</doi><oa>free_for_read</oa></addata></record> |
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subjects | Amino Acid Sequence Animals Aplysia Aquatic habitats Biology and Life Sciences Biomphalaria Biomphalaria - genetics Biomphalaria - parasitology Biomphalaria glabrata Breathing Chemoreception Chemotherapy Conserved sequence Crustaceans Drosophila melanogaster Education Fresh Water Freshwater environments Genetic aspects Genomes Glutamic acid receptors (ionotropic) Host-Parasite Interactions - genetics Humans Identification methods Information processing Insects Ion channels (ligand-gated) Ligands Medicine and Health Sciences Mollusca Neurons Neurosciences Nucleotide sequence Odors Organs Panulirus argus Pathogens Physical Sciences Physiological aspects Physiology Proteins Receptor mechanisms Receptors Receptors, Ionotropic Glutamate - genetics Receptors, Ionotropic Glutamate - isolation & purification Research and Analysis Methods Schistosoma mansoni Schistosoma mansoni - genetics Schistosoma mansoni - pathogenicity Schistosomiasis mansoni - genetics Schistosomiasis mansoni - parasitology Sensory neurons Sequence Alignment Shellfish Signaling Snails Spatial distribution Trematoda Western Hemisphere |
title | Ionotropic Receptors Identified within the Tentacle of the Freshwater Snail Biomphalaria glabrata, an Intermediate Host of Schistosoma mansoni |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-06T16%3A13%3A51IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Ionotropic%20Receptors%20Identified%20within%20the%20Tentacle%20of%20the%20Freshwater%20Snail%20Biomphalaria%20glabrata,%20an%20Intermediate%20Host%20of%20Schistosoma%20mansoni&rft.jtitle=PloS%20one&rft.au=Liang,%20Di&rft.date=2016-06-02&rft.volume=11&rft.issue=6&rft.spage=e0156380&rft.epage=e0156380&rft.pages=e0156380-e0156380&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0156380&rft_dat=%3Cgale_plos_%3EA454205607%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1793571310&rft_id=info:pmid/27253696&rft_galeid=A454205607&rft_doaj_id=oai_doaj_org_article_05616026525b4cfba396a7f1ed418717&rfr_iscdi=true |