Metabolic flexibility of enigmatic SAR324 revealed through metagenomics and metatranscriptomics
Summary Chemolithotrophy is a pervasive metabolic lifestyle for microorganisms in the dark ocean. The SAR324 group of Deltaproteobacteria is ubiquitous in the ocean and has been implicated in sulfur oxidation and carbon fixation, but also contains genomic signatures of C1 utilization and heterotroph...
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| Veröffentlicht in: | Environmental microbiology 2014-01, Vol.16 (1), p.304-317 |
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| creator | Sheik, Cody S. Jain, Sunit Dick, Gregory J. |
| description | Summary
Chemolithotrophy is a pervasive metabolic lifestyle for microorganisms in the dark ocean. The SAR324 group of Deltaproteobacteria is ubiquitous in the ocean and has been implicated in sulfur oxidation and carbon fixation, but also contains genomic signatures of C1 utilization and heterotrophy. Here, we reconstructed the metagenome and metatranscriptome of a population of SAR324 from a hydrothermal plume and surrounding waters in the deep Gulf of California to gain insight into the genetic capability and transcriptional dynamics of this enigmatic group. SAR324's metabolism is signified by genes that encode a novel particulate hydrocarbon monooxygenase (pHMO), degradation pathways for corresponding alcohols and short‐chain fatty acids, dissimilatory sulfur oxidation, formate dehydrogenase (FDH) and a nitrite reductase (NirK). Transcripts of the pHMO, NirK, FDH and transporters for exogenous carbon and amino acid uptake were highly abundant in plume waters. Sulfur oxidation genes were also abundant in the plume metatranscriptome, indicating SAR324 may also utilize reduced sulfur species in hydrothermal fluids. These results suggest that aspects of SAR324's versatile metabolism (lithotrophy, heterotrophy and alkane oxidation) operate simultaneously, and may explain SAR324's ubiquity in the deep Gulf of California and in the global marine biosphere. |
| doi_str_mv | 10.1111/1462-2920.12165 |
| format | Article |
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Chemolithotrophy is a pervasive metabolic lifestyle for microorganisms in the dark ocean. The SAR324 group of Deltaproteobacteria is ubiquitous in the ocean and has been implicated in sulfur oxidation and carbon fixation, but also contains genomic signatures of C1 utilization and heterotrophy. Here, we reconstructed the metagenome and metatranscriptome of a population of SAR324 from a hydrothermal plume and surrounding waters in the deep Gulf of California to gain insight into the genetic capability and transcriptional dynamics of this enigmatic group. SAR324's metabolism is signified by genes that encode a novel particulate hydrocarbon monooxygenase (pHMO), degradation pathways for corresponding alcohols and short‐chain fatty acids, dissimilatory sulfur oxidation, formate dehydrogenase (FDH) and a nitrite reductase (NirK). Transcripts of the pHMO, NirK, FDH and transporters for exogenous carbon and amino acid uptake were highly abundant in plume waters. Sulfur oxidation genes were also abundant in the plume metatranscriptome, indicating SAR324 may also utilize reduced sulfur species in hydrothermal fluids. These results suggest that aspects of SAR324's versatile metabolism (lithotrophy, heterotrophy and alkane oxidation) operate simultaneously, and may explain SAR324's ubiquity in the deep Gulf of California and in the global marine biosphere.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.12165</identifier><identifier>PMID: 23809230</identifier><language>eng</language><publisher>Oxford: Blackwell Publishing Ltd</publisher><subject>Animal, plant and microbial ecology ; Biological and medical sciences ; Carbon - metabolism ; Carbon Cycle ; Chemoautotrophic Growth ; Deltaproteobacteria - classification ; Deltaproteobacteria - genetics ; Deltaproteobacteria - isolation & purification ; Deltaproteobacteria - metabolism ; Fatty acids ; Fundamental and applied biological sciences. Psychology ; General aspects ; Metagenome ; Microbial ecology ; Microbiology ; Oceans and Seas ; Oxidation-Reduction ; Phylogeny ; Seawater - microbiology ; Sulfur - metabolism ; Transcriptome</subject><ispartof>Environmental microbiology, 2014-01, Vol.16 (1), p.304-317</ispartof><rights>Published 2013. This article is a U.S. Government work and is in the public domain in the USA</rights><rights>2015 INIST-CNRS</rights><rights>Published 2013. This article is a U.S. Government work and is in the public domain in the USA.</rights><rights>Copyright © 2014 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%2F1462-2920.12165$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.12165$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=28282066$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23809230$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sheik, Cody S.</creatorcontrib><creatorcontrib>Jain, Sunit</creatorcontrib><creatorcontrib>Dick, Gregory J.</creatorcontrib><title>Metabolic flexibility of enigmatic SAR324 revealed through metagenomics and metatranscriptomics</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
Chemolithotrophy is a pervasive metabolic lifestyle for microorganisms in the dark ocean. The SAR324 group of Deltaproteobacteria is ubiquitous in the ocean and has been implicated in sulfur oxidation and carbon fixation, but also contains genomic signatures of C1 utilization and heterotrophy. Here, we reconstructed the metagenome and metatranscriptome of a population of SAR324 from a hydrothermal plume and surrounding waters in the deep Gulf of California to gain insight into the genetic capability and transcriptional dynamics of this enigmatic group. SAR324's metabolism is signified by genes that encode a novel particulate hydrocarbon monooxygenase (pHMO), degradation pathways for corresponding alcohols and short‐chain fatty acids, dissimilatory sulfur oxidation, formate dehydrogenase (FDH) and a nitrite reductase (NirK). Transcripts of the pHMO, NirK, FDH and transporters for exogenous carbon and amino acid uptake were highly abundant in plume waters. Sulfur oxidation genes were also abundant in the plume metatranscriptome, indicating SAR324 may also utilize reduced sulfur species in hydrothermal fluids. These results suggest that aspects of SAR324's versatile metabolism (lithotrophy, heterotrophy and alkane oxidation) operate simultaneously, and may explain SAR324's ubiquity in the deep Gulf of California and in the global marine biosphere.</description><subject>Animal, plant and microbial ecology</subject><subject>Biological and medical sciences</subject><subject>Carbon - metabolism</subject><subject>Carbon Cycle</subject><subject>Chemoautotrophic Growth</subject><subject>Deltaproteobacteria - classification</subject><subject>Deltaproteobacteria - genetics</subject><subject>Deltaproteobacteria - isolation & purification</subject><subject>Deltaproteobacteria - metabolism</subject><subject>Fatty acids</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>General aspects</subject><subject>Metagenome</subject><subject>Microbial ecology</subject><subject>Microbiology</subject><subject>Oceans and Seas</subject><subject>Oxidation-Reduction</subject><subject>Phylogeny</subject><subject>Seawater - microbiology</subject><subject>Sulfur - metabolism</subject><subject>Transcriptome</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkU1v1DAQhi1ERUvhzA1FQkhcAv6M42NVtaVSt6zaoh4tJ5lsXZxkayfQ_ffMfrBIXLAPHs88rzWel5B3jH5muL4wWfCcG45Xzgr1ghztMy_3MeOH5HVKj5QyLTR9RQ65KKnhgh4RO4PRVUPwddYGePaVD35cZUObQe8XnRuxcHtyI7jMIvwEF6DJxoc4TIuHrEPpAvqh83XKXN9sEmN0faqjX46b_Bty0LqQ4O3uPCbfz8_uTr_mV98uLk9PrnIvjVC5UgK7ayvRyoY3FS-hkKWRrXFKmwrb5YViiklGi0JqKA0WwFSVYGUrSs3FMfm0fXcZh6cJ0mg7n2oIwfUwTMkyrYTUpVDm_6g0VON4jED0wz_o4zDFHj-ClJasMJoppN7vqKnqoLHL6DsXV_bPlBH4uANcql1ocUS1T3-5Ejd-DDm15X75AKt9nVG7Ntuu7bRra-3GbHs2u9wEqMu3Op9GeN7rXPxhC3Rc2fvrC3su5c39bD63c_EbGZqnWg</recordid><startdate>201401</startdate><enddate>201401</enddate><creator>Sheik, Cody S.</creator><creator>Jain, Sunit</creator><creator>Dick, Gregory J.</creator><general>Blackwell Publishing Ltd</general><general>Blackwell</general><general>Wiley Subscription Services, Inc</general><scope>BSCLL</scope><scope>IQODW</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>201401</creationdate><title>Metabolic flexibility of enigmatic SAR324 revealed through metagenomics and metatranscriptomics</title><author>Sheik, Cody S. ; Jain, Sunit ; Dick, Gregory J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-i4935-553001fb3f4d2db28e64894f9a579b2382651514106647e899a5e9bb318f38723</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animal, plant and microbial ecology</topic><topic>Biological and medical sciences</topic><topic>Carbon - metabolism</topic><topic>Carbon Cycle</topic><topic>Chemoautotrophic Growth</topic><topic>Deltaproteobacteria - classification</topic><topic>Deltaproteobacteria - genetics</topic><topic>Deltaproteobacteria - isolation & purification</topic><topic>Deltaproteobacteria - metabolism</topic><topic>Fatty acids</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>General aspects</topic><topic>Metagenome</topic><topic>Microbial ecology</topic><topic>Microbiology</topic><topic>Oceans and Seas</topic><topic>Oxidation-Reduction</topic><topic>Phylogeny</topic><topic>Seawater - microbiology</topic><topic>Sulfur - metabolism</topic><topic>Transcriptome</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sheik, Cody S.</creatorcontrib><creatorcontrib>Jain, Sunit</creatorcontrib><creatorcontrib>Dick, Gregory J.</creatorcontrib><collection>Istex</collection><collection>Pascal-Francis</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>Sheik, Cody S.</au><au>Jain, Sunit</au><au>Dick, Gregory J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Metabolic flexibility of enigmatic SAR324 revealed through metagenomics and metatranscriptomics</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2014-01</date><risdate>2014</risdate><volume>16</volume><issue>1</issue><spage>304</spage><epage>317</epage><pages>304-317</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
Chemolithotrophy is a pervasive metabolic lifestyle for microorganisms in the dark ocean. The SAR324 group of Deltaproteobacteria is ubiquitous in the ocean and has been implicated in sulfur oxidation and carbon fixation, but also contains genomic signatures of C1 utilization and heterotrophy. Here, we reconstructed the metagenome and metatranscriptome of a population of SAR324 from a hydrothermal plume and surrounding waters in the deep Gulf of California to gain insight into the genetic capability and transcriptional dynamics of this enigmatic group. SAR324's metabolism is signified by genes that encode a novel particulate hydrocarbon monooxygenase (pHMO), degradation pathways for corresponding alcohols and short‐chain fatty acids, dissimilatory sulfur oxidation, formate dehydrogenase (FDH) and a nitrite reductase (NirK). Transcripts of the pHMO, NirK, FDH and transporters for exogenous carbon and amino acid uptake were highly abundant in plume waters. Sulfur oxidation genes were also abundant in the plume metatranscriptome, indicating SAR324 may also utilize reduced sulfur species in hydrothermal fluids. These results suggest that aspects of SAR324's versatile metabolism (lithotrophy, heterotrophy and alkane oxidation) operate simultaneously, and may explain SAR324's ubiquity in the deep Gulf of California and in the global marine biosphere.</abstract><cop>Oxford</cop><pub>Blackwell Publishing Ltd</pub><pmid>23809230</pmid><doi>10.1111/1462-2920.12165</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animal, plant and microbial ecology Biological and medical sciences Carbon - metabolism Carbon Cycle Chemoautotrophic Growth Deltaproteobacteria - classification Deltaproteobacteria - genetics Deltaproteobacteria - isolation & purification Deltaproteobacteria - metabolism Fatty acids Fundamental and applied biological sciences. Psychology General aspects Metagenome Microbial ecology Microbiology Oceans and Seas Oxidation-Reduction Phylogeny Seawater - microbiology Sulfur - metabolism Transcriptome |
| title | Metabolic flexibility of enigmatic SAR324 revealed through metagenomics and metatranscriptomics |
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