Sulfur Cycling and Methanogenesis Primarily Drive Microbial Colonization of the Highly Sulfidic Urania Deep Hypersaline Basin
Urania basin in the deep Mediterranean Sea houses a lake that is > 100 m deep, devoid of oxygen, 6 times more saline than seawater, and has very high levels of methane and particularly sulf ide (up to 16 mM), making it among the most sulfidic water bodies on Earth. Along the depth profile there a...
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creator | Borin, Sara Brusetti, Lorenzo Mapelli, Francesca D'Auria, Giuseppe Brusa, Tullio Marzorati, Massimo Rizzi, Aurora Yakimov, Michail Marty, Danielle de Lange, Gert J. van der Wielen, Paul Bolhuis, Henk McGenity, Terry J. Polymenakou, Paraskevi N. Malinverno, Elisa Giuliano, Laura Corselli, Cesare Daffonchio, Daniele Karl, David M. |
description | Urania basin in the deep Mediterranean Sea houses a lake that is > 100 m deep, devoid of oxygen, 6 times more saline than seawater, and has very high levels of methane and particularly sulf ide (up to 16 mM), making it among the most sulfidic water bodies on Earth. Along the depth profile there are 2 chemoclines, a steep one with the overlying oxic seawater, and another between anoxic brines of different density, where gradients of salinity, electron donors and acceptors occur. To identify and differentiate the microbes and processes contributing to the turnover of organic matter and sulfide along the water column, these chemoclines were sampled at a high resolution. Bacterial cell numbers increased up to a hundredfold in the chemoclines as a consequence of elevated nutrient availability, with higher numbers in the upper interface where redox gradient was steeper. Bacterial and archaeal communities, analyzed by DNA fingerprinting, 16S rRNA gene libraries, activity measurements, and cultivation, were highly stratified and metabolically more active along the chemoclines compared with seawater or the uniformly hypersaline brines. Detailed analysis of 16S rRNA gene sequences revealed that in both chemoclines δ-and ε-Proteobacteria, predominantly sulfate reducers and sulfur oxidizers, respectively, were the dominant bacteria. In the deepest layers of the basin MSBL1, putatively responsible for methanogenesis, dominated among archaea. The data suggest that the complex microbial community is adapted to the basin's extreme chemistry, and the elevated biomass is driven largely by sulfur cycling and methanogenesis. |
doi_str_mv | 10.1073/pnas.0811984106 |
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Along the depth profile there are 2 chemoclines, a steep one with the overlying oxic seawater, and another between anoxic brines of different density, where gradients of salinity, electron donors and acceptors occur. To identify and differentiate the microbes and processes contributing to the turnover of organic matter and sulfide along the water column, these chemoclines were sampled at a high resolution. Bacterial cell numbers increased up to a hundredfold in the chemoclines as a consequence of elevated nutrient availability, with higher numbers in the upper interface where redox gradient was steeper. Bacterial and archaeal communities, analyzed by DNA fingerprinting, 16S rRNA gene libraries, activity measurements, and cultivation, were highly stratified and metabolically more active along the chemoclines compared with seawater or the uniformly hypersaline brines. Detailed analysis of 16S rRNA gene sequences revealed that in both chemoclines δ-and ε-Proteobacteria, predominantly sulfate reducers and sulfur oxidizers, respectively, were the dominant bacteria. In the deepest layers of the basin MSBL1, putatively responsible for methanogenesis, dominated among archaea. The data suggest that the complex microbial community is adapted to the basin's extreme chemistry, and the elevated biomass is driven largely by sulfur cycling and methanogenesis.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.0811984106</identifier><identifier>PMID: 19470485</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Archaea ; Archaea - metabolism ; Bacteria ; Bacteria - metabolism ; Basins ; Biomass ; Brine ; Brines ; Cell number ; Cells ; Colonization ; Data processing ; Deoxyribonucleic acid ; DNA ; DNA fingerprinting ; Ecosystem ; Gene libraries ; Houses ; Lakes ; Manganese - metabolism ; Marine environment ; Methane ; Methane production ; Methanogenesis ; Molecular Sequence Data ; Nitrates - metabolism ; Nutrient availability ; Ocean, Atmosphere ; Organic matter ; Oxygen ; Oxygen - metabolism ; Physical Sciences ; Proteobacteria ; rRNA 16S ; rRNA genes ; Salinity ; Salinity effects ; Sciences of the Universe ; Sea water ; Seas ; Seawater ; Seawater - microbiology ; Sulfate ; Sulfates ; Sulfide ; Sulfides ; Sulfur ; Sulfur - metabolism ; Water - metabolism ; Water column</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2009-06, Vol.106 (23), p.9151-9156</ispartof><rights>Copyright National Academy of Sciences Jun 9, 2009</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c562t-aecf4eaf1034187e8503568bc17e15dbfc32187366d071a573d9ef658e3ae9f73</citedby><cites>FETCH-LOGICAL-c562t-aecf4eaf1034187e8503568bc17e15dbfc32187366d071a573d9ef658e3ae9f73</cites><orcidid>0000-0002-2928-6538</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/106/23.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/40483184$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/40483184$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27903,27904,53770,53772,57996,58229</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19470485$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-00412581$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Borin, Sara</creatorcontrib><creatorcontrib>Brusetti, Lorenzo</creatorcontrib><creatorcontrib>Mapelli, Francesca</creatorcontrib><creatorcontrib>D'Auria, Giuseppe</creatorcontrib><creatorcontrib>Brusa, Tullio</creatorcontrib><creatorcontrib>Marzorati, Massimo</creatorcontrib><creatorcontrib>Rizzi, Aurora</creatorcontrib><creatorcontrib>Yakimov, Michail</creatorcontrib><creatorcontrib>Marty, Danielle</creatorcontrib><creatorcontrib>de Lange, Gert J.</creatorcontrib><creatorcontrib>van der Wielen, Paul</creatorcontrib><creatorcontrib>Bolhuis, Henk</creatorcontrib><creatorcontrib>McGenity, Terry J.</creatorcontrib><creatorcontrib>Polymenakou, Paraskevi N.</creatorcontrib><creatorcontrib>Malinverno, Elisa</creatorcontrib><creatorcontrib>Giuliano, Laura</creatorcontrib><creatorcontrib>Corselli, Cesare</creatorcontrib><creatorcontrib>Daffonchio, Daniele</creatorcontrib><creatorcontrib>Karl, David M.</creatorcontrib><title>Sulfur Cycling and Methanogenesis Primarily Drive Microbial Colonization of the Highly Sulfidic Urania Deep Hypersaline Basin</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Urania basin in the deep Mediterranean Sea houses a lake that is > 100 m deep, devoid of oxygen, 6 times more saline than seawater, and has very high levels of methane and particularly sulf ide (up to 16 mM), making it among the most sulfidic water bodies on Earth. Along the depth profile there are 2 chemoclines, a steep one with the overlying oxic seawater, and another between anoxic brines of different density, where gradients of salinity, electron donors and acceptors occur. To identify and differentiate the microbes and processes contributing to the turnover of organic matter and sulfide along the water column, these chemoclines were sampled at a high resolution. Bacterial cell numbers increased up to a hundredfold in the chemoclines as a consequence of elevated nutrient availability, with higher numbers in the upper interface where redox gradient was steeper. Bacterial and archaeal communities, analyzed by DNA fingerprinting, 16S rRNA gene libraries, activity measurements, and cultivation, were highly stratified and metabolically more active along the chemoclines compared with seawater or the uniformly hypersaline brines. Detailed analysis of 16S rRNA gene sequences revealed that in both chemoclines δ-and ε-Proteobacteria, predominantly sulfate reducers and sulfur oxidizers, respectively, were the dominant bacteria. In the deepest layers of the basin MSBL1, putatively responsible for methanogenesis, dominated among archaea. The data suggest that the complex microbial community is adapted to the basin's extreme chemistry, and the elevated biomass is driven largely by sulfur cycling and methanogenesis.</description><subject>Archaea</subject><subject>Archaea - metabolism</subject><subject>Bacteria</subject><subject>Bacteria - metabolism</subject><subject>Basins</subject><subject>Biomass</subject><subject>Brine</subject><subject>Brines</subject><subject>Cell number</subject><subject>Cells</subject><subject>Colonization</subject><subject>Data processing</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA fingerprinting</subject><subject>Ecosystem</subject><subject>Gene libraries</subject><subject>Houses</subject><subject>Lakes</subject><subject>Manganese - metabolism</subject><subject>Marine environment</subject><subject>Methane</subject><subject>Methane production</subject><subject>Methanogenesis</subject><subject>Molecular Sequence Data</subject><subject>Nitrates - metabolism</subject><subject>Nutrient availability</subject><subject>Ocean, Atmosphere</subject><subject>Organic matter</subject><subject>Oxygen</subject><subject>Oxygen - metabolism</subject><subject>Physical Sciences</subject><subject>Proteobacteria</subject><subject>rRNA 16S</subject><subject>rRNA genes</subject><subject>Salinity</subject><subject>Salinity effects</subject><subject>Sciences of the Universe</subject><subject>Sea water</subject><subject>Seas</subject><subject>Seawater</subject><subject>Seawater - microbiology</subject><subject>Sulfate</subject><subject>Sulfates</subject><subject>Sulfide</subject><subject>Sulfides</subject><subject>Sulfur</subject><subject>Sulfur - metabolism</subject><subject>Water - metabolism</subject><subject>Water column</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2009</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFks9v0zAUxyMEYmVw5gRYHBAcuj3HduJckEYHFKkTSLCz5SYvrSvX7uykokj87zi0WmEHOFl6_rzv-_XNsqcUziiU7HzjdDwDSWklOYXiXjaiUNFxwSu4n40A8nIsec5PskcxrgCgEhIeZie04iVwKUbZz6-9bftAJrvaGrcg2jXkCruldn6BDqOJ5Eswax2M3ZHLYLZIrkwd_NxoSybeemd-6M54R3xLuiWSqVksEzrImsbU5DpoZzS5RNyQ6W6DIepUCMk7HY17nD1otY345PCeZtcf3n-bTMezzx8_TS5m41oUeTfWWLccdUuBcSpLlAKYKOS8piVS0czbmuUpzoqigZJqUbKmwrYQEpnGqi3ZafZ2r7vp52tsanRd0FZtfk-2U14b9fePM0u18FuVF1KUHJLAm73A8k7a9GKmhhgAp7mQdEsT--pQLPibHmOn1ibWaK126PuoipIJVkH1XzAHmY5ZDu2_vAOufB9c2lhiKINcyqHF8z2UrhNjwPa2TwpqMIsazKKOZkkZz__cypE_uCMBrw_AkHmUK1TOVEUFVW1vbYffu4S--DeaiGd7YhU7H24RnioxKjn7BUzG3ZQ</recordid><startdate>20090609</startdate><enddate>20090609</enddate><creator>Borin, Sara</creator><creator>Brusetti, Lorenzo</creator><creator>Mapelli, Francesca</creator><creator>D'Auria, Giuseppe</creator><creator>Brusa, Tullio</creator><creator>Marzorati, Massimo</creator><creator>Rizzi, Aurora</creator><creator>Yakimov, Michail</creator><creator>Marty, Danielle</creator><creator>de Lange, Gert J.</creator><creator>van der Wielen, Paul</creator><creator>Bolhuis, Henk</creator><creator>McGenity, Terry J.</creator><creator>Polymenakou, Paraskevi N.</creator><creator>Malinverno, Elisa</creator><creator>Giuliano, Laura</creator><creator>Corselli, Cesare</creator><creator>Daffonchio, Daniele</creator><creator>Karl, David M.</creator><general>National Academy of Sciences</general><general>National Acad Sciences</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7T7</scope><scope>7X8</scope><scope>1XC</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-2928-6538</orcidid></search><sort><creationdate>20090609</creationdate><title>Sulfur Cycling and Methanogenesis Primarily Drive Microbial Colonization of the Highly Sulfidic Urania Deep Hypersaline Basin</title><author>Borin, Sara ; Brusetti, Lorenzo ; Mapelli, Francesca ; D'Auria, Giuseppe ; Brusa, Tullio ; Marzorati, Massimo ; Rizzi, Aurora ; Yakimov, Michail ; Marty, Danielle ; de Lange, Gert J. ; van der Wielen, Paul ; Bolhuis, Henk ; McGenity, Terry J. ; Polymenakou, Paraskevi N. ; Malinverno, Elisa ; Giuliano, Laura ; Corselli, Cesare ; Daffonchio, Daniele ; Karl, David M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c562t-aecf4eaf1034187e8503568bc17e15dbfc32187366d071a573d9ef658e3ae9f73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>Archaea</topic><topic>Archaea - 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PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2009-06-09</date><risdate>2009</risdate><volume>106</volume><issue>23</issue><spage>9151</spage><epage>9156</epage><pages>9151-9156</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Urania basin in the deep Mediterranean Sea houses a lake that is > 100 m deep, devoid of oxygen, 6 times more saline than seawater, and has very high levels of methane and particularly sulf ide (up to 16 mM), making it among the most sulfidic water bodies on Earth. Along the depth profile there are 2 chemoclines, a steep one with the overlying oxic seawater, and another between anoxic brines of different density, where gradients of salinity, electron donors and acceptors occur. To identify and differentiate the microbes and processes contributing to the turnover of organic matter and sulfide along the water column, these chemoclines were sampled at a high resolution. Bacterial cell numbers increased up to a hundredfold in the chemoclines as a consequence of elevated nutrient availability, with higher numbers in the upper interface where redox gradient was steeper. Bacterial and archaeal communities, analyzed by DNA fingerprinting, 16S rRNA gene libraries, activity measurements, and cultivation, were highly stratified and metabolically more active along the chemoclines compared with seawater or the uniformly hypersaline brines. Detailed analysis of 16S rRNA gene sequences revealed that in both chemoclines δ-and ε-Proteobacteria, predominantly sulfate reducers and sulfur oxidizers, respectively, were the dominant bacteria. In the deepest layers of the basin MSBL1, putatively responsible for methanogenesis, dominated among archaea. The data suggest that the complex microbial community is adapted to the basin's extreme chemistry, and the elevated biomass is driven largely by sulfur cycling and methanogenesis.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>19470485</pmid><doi>10.1073/pnas.0811984106</doi><tpages>6</tpages><orcidid>https://orcid.org/0000-0002-2928-6538</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Archaea Archaea - metabolism Bacteria Bacteria - metabolism Basins Biomass Brine Brines Cell number Cells Colonization Data processing Deoxyribonucleic acid DNA DNA fingerprinting Ecosystem Gene libraries Houses Lakes Manganese - metabolism Marine environment Methane Methane production Methanogenesis Molecular Sequence Data Nitrates - metabolism Nutrient availability Ocean, Atmosphere Organic matter Oxygen Oxygen - metabolism Physical Sciences Proteobacteria rRNA 16S rRNA genes Salinity Salinity effects Sciences of the Universe Sea water Seas Seawater Seawater - microbiology Sulfate Sulfates Sulfide Sulfides Sulfur Sulfur - metabolism Water - metabolism Water column |
title | Sulfur Cycling and Methanogenesis Primarily Drive Microbial Colonization of the Highly Sulfidic Urania Deep Hypersaline Basin |
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