Functional interactions among filamentous Epsilonproteobacteria and Bacteroidetes in a deep-sea hydrothermal vent biofilm
Summary Little is known about how lithoautotrophic primary production is connected to microbial organotrophic consumption in hydrothermal systems. Using a multifaceted approach, we analysed the structure and metabolic capabilities within a biofilm growing on the surface of a black smoker chimney in...
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| Veröffentlicht in: | Environmental microbiology 2015-10, Vol.17 (10), p.4063-4077 |
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| creator | Stokke, Runar Dahle, Håkon Roalkvam, Irene Wissuwa, Juliane Daae, Frida Lise Tooming-Klunderud, Ave Thorseth, Ingunn H. Pedersen, Rolf B. Steen, Ida Helene |
| description | Summary
Little is known about how lithoautotrophic primary production is connected to microbial organotrophic consumption in hydrothermal systems. Using a multifaceted approach, we analysed the structure and metabolic capabilities within a biofilm growing on the surface of a black smoker chimney in the Loki's Castle vent field. Imaging revealed the presence of rod‐shaped Bacteroidetes growing as ectobionts on long, sheathed microbial filaments (> 100 μm) affiliated with the Sulfurovum genus within Epsilonproteobacteria. The filaments were composed of a thick (> 200 nm) stable polysaccharide, representing a substantial fraction of organic carbon produced by primary production. An integrated –omics approach enabled us to assess the metabolic potential and in situ metabolism of individual taxonomic and morphological groups identified by imaging. Specifically, we provide evidence that organotrophic Bacteroidetes attach to and glide along the surface of Sulfurovum filaments utilizing organic polymers produced by the lithoautotrophic Sulfurovum. Furthermore, in situ expression of acetyl‐CoA synthetase by Sulfurovum suggested the ability to assimilate acetate, indicating recycling of organic matter in the biofilm. This study expands our understanding of the lifestyles of Epsilonproteobacteria in hydrothermal vents, their metabolic properties and co‐operative interactions in deep‐sea hydrothermal vent food webs. |
| doi_str_mv | 10.1111/1462-2920.12970 |
| format | Article |
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Little is known about how lithoautotrophic primary production is connected to microbial organotrophic consumption in hydrothermal systems. Using a multifaceted approach, we analysed the structure and metabolic capabilities within a biofilm growing on the surface of a black smoker chimney in the Loki's Castle vent field. Imaging revealed the presence of rod‐shaped Bacteroidetes growing as ectobionts on long, sheathed microbial filaments (> 100 μm) affiliated with the Sulfurovum genus within Epsilonproteobacteria. The filaments were composed of a thick (> 200 nm) stable polysaccharide, representing a substantial fraction of organic carbon produced by primary production. An integrated –omics approach enabled us to assess the metabolic potential and in situ metabolism of individual taxonomic and morphological groups identified by imaging. Specifically, we provide evidence that organotrophic Bacteroidetes attach to and glide along the surface of Sulfurovum filaments utilizing organic polymers produced by the lithoautotrophic Sulfurovum. Furthermore, in situ expression of acetyl‐CoA synthetase by Sulfurovum suggested the ability to assimilate acetate, indicating recycling of organic matter in the biofilm. This study expands our understanding of the lifestyles of Epsilonproteobacteria in hydrothermal vents, their metabolic properties and co‐operative interactions in deep‐sea hydrothermal vent food webs.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.12970</identifier><identifier>PMID: 26147346</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Acetates - metabolism ; Acetyl Coenzyme A - biosynthesis ; Bacteroidetes - genetics ; Bacteroidetes - physiology ; Biofilms ; Coenzyme A Ligases - biosynthesis ; Coenzyme A Ligases - metabolism ; Epsilonproteobacteria - genetics ; Epsilonproteobacteria - physiology ; Hydrothermal Vents - microbiology ; Microbial Interactions ; Phylogeny ; RNA, Ribosomal, 16S - genetics</subject><ispartof>Environmental microbiology, 2015-10, Vol.17 (10), p.4063-4077</ispartof><rights>2015 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><rights>2015 Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>Copyright © 2015 Society for Applied Microbiology and John Wiley & Sons Ltd</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://onlinelibrary.wiley.com/doi/pdf/10.1111%2F1462-2920.12970$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.12970$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26147346$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Stokke, Runar</creatorcontrib><creatorcontrib>Dahle, Håkon</creatorcontrib><creatorcontrib>Roalkvam, Irene</creatorcontrib><creatorcontrib>Wissuwa, Juliane</creatorcontrib><creatorcontrib>Daae, Frida Lise</creatorcontrib><creatorcontrib>Tooming-Klunderud, Ave</creatorcontrib><creatorcontrib>Thorseth, Ingunn H.</creatorcontrib><creatorcontrib>Pedersen, Rolf B.</creatorcontrib><creatorcontrib>Steen, Ida Helene</creatorcontrib><title>Functional interactions among filamentous Epsilonproteobacteria and Bacteroidetes in a deep-sea hydrothermal vent biofilm</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
Little is known about how lithoautotrophic primary production is connected to microbial organotrophic consumption in hydrothermal systems. Using a multifaceted approach, we analysed the structure and metabolic capabilities within a biofilm growing on the surface of a black smoker chimney in the Loki's Castle vent field. Imaging revealed the presence of rod‐shaped Bacteroidetes growing as ectobionts on long, sheathed microbial filaments (> 100 μm) affiliated with the Sulfurovum genus within Epsilonproteobacteria. The filaments were composed of a thick (> 200 nm) stable polysaccharide, representing a substantial fraction of organic carbon produced by primary production. An integrated –omics approach enabled us to assess the metabolic potential and in situ metabolism of individual taxonomic and morphological groups identified by imaging. Specifically, we provide evidence that organotrophic Bacteroidetes attach to and glide along the surface of Sulfurovum filaments utilizing organic polymers produced by the lithoautotrophic Sulfurovum. Furthermore, in situ expression of acetyl‐CoA synthetase by Sulfurovum suggested the ability to assimilate acetate, indicating recycling of organic matter in the biofilm. This study expands our understanding of the lifestyles of Epsilonproteobacteria in hydrothermal vents, their metabolic properties and co‐operative interactions in deep‐sea hydrothermal vent food webs.</description><subject>Acetates - metabolism</subject><subject>Acetyl Coenzyme A - biosynthesis</subject><subject>Bacteroidetes - genetics</subject><subject>Bacteroidetes - physiology</subject><subject>Biofilms</subject><subject>Coenzyme A Ligases - biosynthesis</subject><subject>Coenzyme A Ligases - metabolism</subject><subject>Epsilonproteobacteria - genetics</subject><subject>Epsilonproteobacteria - physiology</subject><subject>Hydrothermal Vents - microbiology</subject><subject>Microbial Interactions</subject><subject>Phylogeny</subject><subject>RNA, Ribosomal, 16S - genetics</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkT1z1DAQhjUMGRIOajpGMzQ0Bn3rXJLMXcjkgxQw0GlkeU0UbOuwbOD-PXu-cAVN1GhXet7Val9CXnH2juN6z5URhSgFpqK07Ak5OZw8PcRcHJPnOd8zxq207Bk5FoYrK5U5Idv11Icxpt63NPYjDH7OMvVd6r_TJra-g35MU6arTY5t6jdDGiFVyMEQPfV9TU_nJMUaRshYhnpaA2yKDJ7ebWsU3MHQ4Qu_sBStYsKy3Qty1Pg2w8uHfUG-rFefzz4WV5_OL84-XBVRS8mKIANrdFkFVoYKhFFGWSbs0gjrG1bpAFDJMpQSmAhK88paKcsmQLANV9DIBXm7r4uN_5wgj66LOUDb-h7wW44vpcV5KcEfR61YMi01NrYgb_5D79M04BRnSi2NFqVB6vUDNVUd1G4zxM4PW_dv_gjoPfA7trA93HPmdva6nYFuZ6ab7XWr64s5QF2x18U8wp-Dzg8_nEGPtft6c-5ub_np5aX65tbyL7aHpv8</recordid><startdate>201510</startdate><enddate>201510</enddate><creator>Stokke, Runar</creator><creator>Dahle, Håkon</creator><creator>Roalkvam, Irene</creator><creator>Wissuwa, Juliane</creator><creator>Daae, Frida Lise</creator><creator>Tooming-Klunderud, Ave</creator><creator>Thorseth, Ingunn H.</creator><creator>Pedersen, Rolf B.</creator><creator>Steen, Ida Helene</creator><general>Blackwell Publishing Ltd</general><general>Wiley Subscription Services, Inc</general><scope>BSCLL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7QH</scope><scope>7QL</scope><scope>7ST</scope><scope>7T7</scope><scope>7TN</scope><scope>7U9</scope><scope>7UA</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope></search><sort><creationdate>201510</creationdate><title>Functional interactions among filamentous Epsilonproteobacteria and Bacteroidetes in a deep-sea hydrothermal vent biofilm</title><author>Stokke, Runar ; Dahle, Håkon ; Roalkvam, Irene ; Wissuwa, Juliane ; Daae, Frida Lise ; Tooming-Klunderud, Ave ; Thorseth, Ingunn H. ; Pedersen, Rolf B. ; Steen, Ida Helene</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-i5330-c3c0f59bc09cbe2646470278627af0b5ceeb39c93e02c451b77339fcec7f14ef3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Acetates - metabolism</topic><topic>Acetyl Coenzyme A - biosynthesis</topic><topic>Bacteroidetes - genetics</topic><topic>Bacteroidetes - physiology</topic><topic>Biofilms</topic><topic>Coenzyme A Ligases - biosynthesis</topic><topic>Coenzyme A Ligases - metabolism</topic><topic>Epsilonproteobacteria - genetics</topic><topic>Epsilonproteobacteria - physiology</topic><topic>Hydrothermal Vents - microbiology</topic><topic>Microbial Interactions</topic><topic>Phylogeny</topic><topic>RNA, Ribosomal, 16S - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Stokke, Runar</creatorcontrib><creatorcontrib>Dahle, Håkon</creatorcontrib><creatorcontrib>Roalkvam, Irene</creatorcontrib><creatorcontrib>Wissuwa, Juliane</creatorcontrib><creatorcontrib>Daae, Frida Lise</creatorcontrib><creatorcontrib>Tooming-Klunderud, Ave</creatorcontrib><creatorcontrib>Thorseth, Ingunn H.</creatorcontrib><creatorcontrib>Pedersen, Rolf B.</creatorcontrib><creatorcontrib>Steen, Ida Helene</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>Aqualine</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Oceanic Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Water Resources Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Stokke, Runar</au><au>Dahle, Håkon</au><au>Roalkvam, Irene</au><au>Wissuwa, Juliane</au><au>Daae, Frida Lise</au><au>Tooming-Klunderud, Ave</au><au>Thorseth, Ingunn H.</au><au>Pedersen, Rolf B.</au><au>Steen, Ida Helene</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Functional interactions among filamentous Epsilonproteobacteria and Bacteroidetes in a deep-sea hydrothermal vent biofilm</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2015-10</date><risdate>2015</risdate><volume>17</volume><issue>10</issue><spage>4063</spage><epage>4077</epage><pages>4063-4077</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
Little is known about how lithoautotrophic primary production is connected to microbial organotrophic consumption in hydrothermal systems. Using a multifaceted approach, we analysed the structure and metabolic capabilities within a biofilm growing on the surface of a black smoker chimney in the Loki's Castle vent field. Imaging revealed the presence of rod‐shaped Bacteroidetes growing as ectobionts on long, sheathed microbial filaments (> 100 μm) affiliated with the Sulfurovum genus within Epsilonproteobacteria. The filaments were composed of a thick (> 200 nm) stable polysaccharide, representing a substantial fraction of organic carbon produced by primary production. An integrated –omics approach enabled us to assess the metabolic potential and in situ metabolism of individual taxonomic and morphological groups identified by imaging. Specifically, we provide evidence that organotrophic Bacteroidetes attach to and glide along the surface of Sulfurovum filaments utilizing organic polymers produced by the lithoautotrophic Sulfurovum. Furthermore, in situ expression of acetyl‐CoA synthetase by Sulfurovum suggested the ability to assimilate acetate, indicating recycling of organic matter in the biofilm. This study expands our understanding of the lifestyles of Epsilonproteobacteria in hydrothermal vents, their metabolic properties and co‐operative interactions in deep‐sea hydrothermal vent food webs.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>26147346</pmid><doi>10.1111/1462-2920.12970</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Environmental microbiology, 2015-10, Vol.17 (10), p.4063-4077 |
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| language | eng |
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| source | MEDLINE; Wiley Online Library Journals Frontfile Complete |
| subjects | Acetates - metabolism Acetyl Coenzyme A - biosynthesis Bacteroidetes - genetics Bacteroidetes - physiology Biofilms Coenzyme A Ligases - biosynthesis Coenzyme A Ligases - metabolism Epsilonproteobacteria - genetics Epsilonproteobacteria - physiology Hydrothermal Vents - microbiology Microbial Interactions Phylogeny RNA, Ribosomal, 16S - genetics |
| title | Functional interactions among filamentous Epsilonproteobacteria and Bacteroidetes in a deep-sea hydrothermal vent biofilm |
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