The fingerprint of chemosymbiosis: origin and preservation of isotopic biosignatures in the nonseep bivalve Loripes lacteus compared with Venerupis aurea
Abstract Endosymbionts in marine bivalves leave characteristic biosignatures in their host organisms. Two nonseep bivalve species collected in Mediterranean lagoons, thiotrophic symbiotic Loripes lacteus and filter-feeding nonsymbiotic Venerupis aurea, were studied in detail with respect to generati...
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| Veröffentlicht in: | FEMS microbiology ecology 2012-08, Vol.81 (2), p.480-493 |
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| creator | Dreier, Anne Stannek, Lorena Blumenberg, Martin Taviani, Marco Sigovini, Marco Wrede, Christoph Thiel, Volker Hoppert, Michael |
| description | Abstract
Endosymbionts in marine bivalves leave characteristic biosignatures in their host organisms. Two nonseep bivalve species collected in Mediterranean lagoons, thiotrophic symbiotic Loripes lacteus and filter-feeding nonsymbiotic Venerupis aurea, were studied in detail with respect to generation and presence of such signatures in living animals, and the preservation of these signals in subfossil (late Pleistocene) sedimentary shells. Three key enzymes from sulfur oxidation (APS-reductase), CO2 fixation (RubisCO) and assimilation of nitrogen [glutamine synthetase (GS)] were detected by immunofluorescence in the bacterial symbionts of Loripes. In Loripes, major activity was derived from GS of the symbionts whereas in Venerupis the host GS is active. In search of geologically stable biosignatures for thiotrophic chemosymbiosis that might be suitable to detect such associations in ancient bivalves, we analyzed the isotopic composition of shell lipids (δ 13C) and the bulk organic matrix of the shell (δ 13C, δ 15N, δ 34S). In the thiotrophic Loripes, δ 13C values were depleted compared with the filter-feeding Venerupis by as much as 8.5‰ for individual fatty acids, and 4.4‰ for bulk organic carbon. Likewise, bulk δ 15N and δ 34S values were more depleted in recent thiotrophic Loripes. Whereas δ 34S values were found to be unstable over time, the combined δ 15N and δ 13C values in organic shell extracts revealed a specific signature for chemosymbiosis in recent and subfossil specimens. |
| doi_str_mv | 10.1111/j.1574-6941.2012.01374.x |
| format | Article |
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Endosymbionts in marine bivalves leave characteristic biosignatures in their host organisms. Two nonseep bivalve species collected in Mediterranean lagoons, thiotrophic symbiotic Loripes lacteus and filter-feeding nonsymbiotic Venerupis aurea, were studied in detail with respect to generation and presence of such signatures in living animals, and the preservation of these signals in subfossil (late Pleistocene) sedimentary shells. Three key enzymes from sulfur oxidation (APS-reductase), CO2 fixation (RubisCO) and assimilation of nitrogen [glutamine synthetase (GS)] were detected by immunofluorescence in the bacterial symbionts of Loripes. In Loripes, major activity was derived from GS of the symbionts whereas in Venerupis the host GS is active. In search of geologically stable biosignatures for thiotrophic chemosymbiosis that might be suitable to detect such associations in ancient bivalves, we analyzed the isotopic composition of shell lipids (δ 13C) and the bulk organic matrix of the shell (δ 13C, δ 15N, δ 34S). In the thiotrophic Loripes, δ 13C values were depleted compared with the filter-feeding Venerupis by as much as 8.5‰ for individual fatty acids, and 4.4‰ for bulk organic carbon. Likewise, bulk δ 15N and δ 34S values were more depleted in recent thiotrophic Loripes. Whereas δ 34S values were found to be unstable over time, the combined δ 15N and δ 13C values in organic shell extracts revealed a specific signature for chemosymbiosis in recent and subfossil specimens.</description><identifier>ISSN: 0168-6496</identifier><identifier>EISSN: 1574-6941</identifier><identifier>DOI: 10.1111/j.1574-6941.2012.01374.x</identifier><identifier>PMID: 22458451</identifier><identifier>CODEN: FMECEZ</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Animal Shells - chemistry ; Animal, plant and microbial ecology ; Animals ; Bacteria - enzymology ; Bacteria - genetics ; Biological and medical sciences ; biosignatures ; Bivalvia ; Bivalvia - chemistry ; Bivalvia - microbiology ; Carbon Cycle ; Carbon dioxide fixation ; Carbon Isotopes - analysis ; Ecology ; endosymbiosis ; Fossils ; Fundamental and applied biological sciences. Psychology ; Glutamate-Ammonia Ligase - analysis ; Lagoons ; Lipids ; Loripes ; Loripes lacteus ; Marine ; Microbial ecology ; Microbiology ; Mollusks ; Nitrogen - chemistry ; Nitrogen Isotopes - analysis ; Organic carbon ; Oxidation-Reduction ; Oxidoreductases Acting on Sulfur Group Donors - analysis ; Pleistocene ; Preservation ; Ribulose-Bisphosphate Carboxylase - analysis ; RNA, Ribosomal, 16S - genetics ; Shellfish ; Shells ; stable isotope ratios ; Sulfur ; Sulfur - analysis ; Sulfur Isotopes - analysis ; Symbiosis ; thiotrophic bivalves ; Various environments (extraatmospheric space, air, water) ; Venerupis ; Venerupis aurea</subject><ispartof>FEMS microbiology ecology, 2012-08, Vol.81 (2), p.480-493</ispartof><rights>2012 Federation of European Microbiological Societies 2012</rights><rights>2012 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved</rights><rights>2015 INIST-CNRS</rights><rights>2012 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved.</rights><rights>Copyright © 2012 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5544-9062f4a727a57d1743bc6f5a8c97e25545df8cd033ba0290b5348c64be0375863</citedby><cites>FETCH-LOGICAL-c5544-9062f4a727a57d1743bc6f5a8c97e25545df8cd033ba0290b5348c64be0375863</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fj.1574-6941.2012.01374.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fj.1574-6941.2012.01374.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,778,782,1414,27911,27912,45561,45562</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=26122466$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22458451$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Dreier, Anne</creatorcontrib><creatorcontrib>Stannek, Lorena</creatorcontrib><creatorcontrib>Blumenberg, Martin</creatorcontrib><creatorcontrib>Taviani, Marco</creatorcontrib><creatorcontrib>Sigovini, Marco</creatorcontrib><creatorcontrib>Wrede, Christoph</creatorcontrib><creatorcontrib>Thiel, Volker</creatorcontrib><creatorcontrib>Hoppert, Michael</creatorcontrib><title>The fingerprint of chemosymbiosis: origin and preservation of isotopic biosignatures in the nonseep bivalve Loripes lacteus compared with Venerupis aurea</title><title>FEMS microbiology ecology</title><addtitle>FEMS Microbiol Ecol</addtitle><description>Abstract
Endosymbionts in marine bivalves leave characteristic biosignatures in their host organisms. Two nonseep bivalve species collected in Mediterranean lagoons, thiotrophic symbiotic Loripes lacteus and filter-feeding nonsymbiotic Venerupis aurea, were studied in detail with respect to generation and presence of such signatures in living animals, and the preservation of these signals in subfossil (late Pleistocene) sedimentary shells. Three key enzymes from sulfur oxidation (APS-reductase), CO2 fixation (RubisCO) and assimilation of nitrogen [glutamine synthetase (GS)] were detected by immunofluorescence in the bacterial symbionts of Loripes. In Loripes, major activity was derived from GS of the symbionts whereas in Venerupis the host GS is active. In search of geologically stable biosignatures for thiotrophic chemosymbiosis that might be suitable to detect such associations in ancient bivalves, we analyzed the isotopic composition of shell lipids (δ 13C) and the bulk organic matrix of the shell (δ 13C, δ 15N, δ 34S). In the thiotrophic Loripes, δ 13C values were depleted compared with the filter-feeding Venerupis by as much as 8.5‰ for individual fatty acids, and 4.4‰ for bulk organic carbon. Likewise, bulk δ 15N and δ 34S values were more depleted in recent thiotrophic Loripes. Whereas δ 34S values were found to be unstable over time, the combined δ 15N and δ 13C values in organic shell extracts revealed a specific signature for chemosymbiosis in recent and subfossil specimens.</description><subject>Animal Shells - chemistry</subject><subject>Animal, plant and microbial ecology</subject><subject>Animals</subject><subject>Bacteria - enzymology</subject><subject>Bacteria - genetics</subject><subject>Biological and medical sciences</subject><subject>biosignatures</subject><subject>Bivalvia</subject><subject>Bivalvia - chemistry</subject><subject>Bivalvia - microbiology</subject><subject>Carbon Cycle</subject><subject>Carbon dioxide fixation</subject><subject>Carbon Isotopes - analysis</subject><subject>Ecology</subject><subject>endosymbiosis</subject><subject>Fossils</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Glutamate-Ammonia Ligase - analysis</subject><subject>Lagoons</subject><subject>Lipids</subject><subject>Loripes</subject><subject>Loripes lacteus</subject><subject>Marine</subject><subject>Microbial ecology</subject><subject>Microbiology</subject><subject>Mollusks</subject><subject>Nitrogen - chemistry</subject><subject>Nitrogen Isotopes - analysis</subject><subject>Organic carbon</subject><subject>Oxidation-Reduction</subject><subject>Oxidoreductases Acting on Sulfur Group Donors - analysis</subject><subject>Pleistocene</subject><subject>Preservation</subject><subject>Ribulose-Bisphosphate Carboxylase - analysis</subject><subject>RNA, Ribosomal, 16S - genetics</subject><subject>Shellfish</subject><subject>Shells</subject><subject>stable isotope ratios</subject><subject>Sulfur</subject><subject>Sulfur - analysis</subject><subject>Sulfur Isotopes - analysis</subject><subject>Symbiosis</subject><subject>thiotrophic bivalves</subject><subject>Various environments (extraatmospheric space, air, water)</subject><subject>Venerupis</subject><subject>Venerupis aurea</subject><issn>0168-6496</issn><issn>1574-6941</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkdGK1DAUhoso7rj6ChIQwZvWpE2aVvBCll0VRrxZvQ1pejqToU1q0s7uPIpv6-nOuIIibG4SON__n3PyJwlhNGN43u4yJiRPy5qzLKcszygrJM9uHyWr-8LjZEVZWaUlr8uz5FmMO0qZKDh9mpzlORcVF2yV_LzeAums20AYg3UT8R0xWxh8PAyN9dHGd8QHu7GOaNeSMUCEsNeT9W5BbfSTH60hd-zG6WlGgiA9oa_zLgKMWNzrfg9kjU4jlnttJpgjMX4YdYCW3NhpS76DgzCPNhKNJvp58qTTfYQXp_s8-XZ1eX3xKV1__fj54sM6NUJwnta0zDuuZS61kC2TvGhM2QldmVpCjohou8q0tCgaTfOaNvgFlSl5A7SQoiqL8-TN0XcM_scMcVKDjQb6Xjvwc1SM5hWqK8EegnIuZVFJRF_9he78HBwuophgssBBWY1UdaRM8DEG6BSGMOhwQCu1JK12aglULYGqJWl1l7S6RenLU4O5GaC9F_6OFoHXJ0BHo_suaGds_MOVDNFy2f_9kbuxPRwePIC6uvyyvFBfHPV-Hv-jTv8d_xd9utSa</recordid><startdate>201208</startdate><enddate>201208</enddate><creator>Dreier, Anne</creator><creator>Stannek, Lorena</creator><creator>Blumenberg, Martin</creator><creator>Taviani, Marco</creator><creator>Sigovini, Marco</creator><creator>Wrede, Christoph</creator><creator>Thiel, Volker</creator><creator>Hoppert, Michael</creator><general>Blackwell Publishing Ltd</general><general>Blackwell</general><general>Oxford University Press</general><scope>IQODW</scope><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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7T7</scope><scope>7TK</scope><scope>7TM</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>7TN</scope><scope>7UA</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope></search><sort><creationdate>201208</creationdate><title>The fingerprint of chemosymbiosis: origin and preservation of isotopic biosignatures in the nonseep bivalve Loripes lacteus compared with Venerupis aurea</title><author>Dreier, Anne ; Stannek, Lorena ; Blumenberg, Martin ; Taviani, Marco ; Sigovini, Marco ; Wrede, Christoph ; Thiel, Volker ; Hoppert, Michael</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5544-9062f4a727a57d1743bc6f5a8c97e25545df8cd033ba0290b5348c64be0375863</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Animal Shells - chemistry</topic><topic>Animal, plant and microbial ecology</topic><topic>Animals</topic><topic>Bacteria - enzymology</topic><topic>Bacteria - genetics</topic><topic>Biological and medical sciences</topic><topic>biosignatures</topic><topic>Bivalvia</topic><topic>Bivalvia - chemistry</topic><topic>Bivalvia - microbiology</topic><topic>Carbon Cycle</topic><topic>Carbon dioxide fixation</topic><topic>Carbon Isotopes - analysis</topic><topic>Ecology</topic><topic>endosymbiosis</topic><topic>Fossils</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Glutamate-Ammonia Ligase - analysis</topic><topic>Lagoons</topic><topic>Lipids</topic><topic>Loripes</topic><topic>Loripes lacteus</topic><topic>Marine</topic><topic>Microbial ecology</topic><topic>Microbiology</topic><topic>Mollusks</topic><topic>Nitrogen - chemistry</topic><topic>Nitrogen Isotopes - analysis</topic><topic>Organic carbon</topic><topic>Oxidation-Reduction</topic><topic>Oxidoreductases Acting on Sulfur Group Donors - analysis</topic><topic>Pleistocene</topic><topic>Preservation</topic><topic>Ribulose-Bisphosphate Carboxylase - analysis</topic><topic>RNA, Ribosomal, 16S - genetics</topic><topic>Shellfish</topic><topic>Shells</topic><topic>stable isotope ratios</topic><topic>Sulfur</topic><topic>Sulfur - analysis</topic><topic>Sulfur Isotopes - analysis</topic><topic>Symbiosis</topic><topic>thiotrophic bivalves</topic><topic>Various environments (extraatmospheric space, air, water)</topic><topic>Venerupis</topic><topic>Venerupis aurea</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Dreier, Anne</creatorcontrib><creatorcontrib>Stannek, Lorena</creatorcontrib><creatorcontrib>Blumenberg, Martin</creatorcontrib><creatorcontrib>Taviani, Marco</creatorcontrib><creatorcontrib>Sigovini, Marco</creatorcontrib><creatorcontrib>Wrede, Christoph</creatorcontrib><creatorcontrib>Thiel, Volker</creatorcontrib><creatorcontrib>Hoppert, Michael</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Oceanic Abstracts</collection><collection>Water Resources Abstracts</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><jtitle>FEMS microbiology ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Dreier, Anne</au><au>Stannek, Lorena</au><au>Blumenberg, Martin</au><au>Taviani, Marco</au><au>Sigovini, Marco</au><au>Wrede, Christoph</au><au>Thiel, Volker</au><au>Hoppert, Michael</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The fingerprint of chemosymbiosis: origin and preservation of isotopic biosignatures in the nonseep bivalve Loripes lacteus compared with Venerupis aurea</atitle><jtitle>FEMS microbiology ecology</jtitle><addtitle>FEMS Microbiol Ecol</addtitle><date>2012-08</date><risdate>2012</risdate><volume>81</volume><issue>2</issue><spage>480</spage><epage>493</epage><pages>480-493</pages><issn>0168-6496</issn><eissn>1574-6941</eissn><coden>FMECEZ</coden><abstract>Abstract
Endosymbionts in marine bivalves leave characteristic biosignatures in their host organisms. Two nonseep bivalve species collected in Mediterranean lagoons, thiotrophic symbiotic Loripes lacteus and filter-feeding nonsymbiotic Venerupis aurea, were studied in detail with respect to generation and presence of such signatures in living animals, and the preservation of these signals in subfossil (late Pleistocene) sedimentary shells. Three key enzymes from sulfur oxidation (APS-reductase), CO2 fixation (RubisCO) and assimilation of nitrogen [glutamine synthetase (GS)] were detected by immunofluorescence in the bacterial symbionts of Loripes. In Loripes, major activity was derived from GS of the symbionts whereas in Venerupis the host GS is active. In search of geologically stable biosignatures for thiotrophic chemosymbiosis that might be suitable to detect such associations in ancient bivalves, we analyzed the isotopic composition of shell lipids (δ 13C) and the bulk organic matrix of the shell (δ 13C, δ 15N, δ 34S). In the thiotrophic Loripes, δ 13C values were depleted compared with the filter-feeding Venerupis by as much as 8.5‰ for individual fatty acids, and 4.4‰ for bulk organic carbon. Likewise, bulk δ 15N and δ 34S values were more depleted in recent thiotrophic Loripes. Whereas δ 34S values were found to be unstable over time, the combined δ 15N and δ 13C values in organic shell extracts revealed a specific signature for chemosymbiosis in recent and subfossil specimens.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>22458451</pmid><doi>10.1111/j.1574-6941.2012.01374.x</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | FEMS microbiology ecology, 2012-08, Vol.81 (2), p.480-493 |
| issn | 0168-6496 1574-6941 |
| language | eng |
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| source | MEDLINE; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Oxford Journals Open Access Collection |
| subjects | Animal Shells - chemistry Animal, plant and microbial ecology Animals Bacteria - enzymology Bacteria - genetics Biological and medical sciences biosignatures Bivalvia Bivalvia - chemistry Bivalvia - microbiology Carbon Cycle Carbon dioxide fixation Carbon Isotopes - analysis Ecology endosymbiosis Fossils Fundamental and applied biological sciences. Psychology Glutamate-Ammonia Ligase - analysis Lagoons Lipids Loripes Loripes lacteus Marine Microbial ecology Microbiology Mollusks Nitrogen - chemistry Nitrogen Isotopes - analysis Organic carbon Oxidation-Reduction Oxidoreductases Acting on Sulfur Group Donors - analysis Pleistocene Preservation Ribulose-Bisphosphate Carboxylase - analysis RNA, Ribosomal, 16S - genetics Shellfish Shells stable isotope ratios Sulfur Sulfur - analysis Sulfur Isotopes - analysis Symbiosis thiotrophic bivalves Various environments (extraatmospheric space, air, water) Venerupis Venerupis aurea |
| title | The fingerprint of chemosymbiosis: origin and preservation of isotopic biosignatures in the nonseep bivalve Loripes lacteus compared with Venerupis aurea |
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