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A metaproteomic assessment of winter and summer bacterioplankton from Antarctic Peninsula coastal surface waters
A metaproteomic survey of surface coastal waters near Palmer Station on the Antarctic Peninsula, West Antarctica, was performed, revealing marked differences in the functional capacity of summer and winter communities of bacterioplankton. Proteins from Flavobacteria were more abundant in the summer...
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Published in: | The ISME Journal 2012-10, Vol.6 (10), p.1883-1900 |
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creator | Williams, Timothy J Long, Emilie Evans, Flavia DeMaere, Mathew Z Lauro, Federico M Raftery, Mark J Ducklow, Hugh Grzymski, Joseph J Murray, Alison E Cavicchioli, Ricardo |
description | A metaproteomic survey of surface coastal waters near Palmer Station on the Antarctic Peninsula, West Antarctica, was performed, revealing marked differences in the functional capacity of summer and winter communities of bacterioplankton. Proteins from Flavobacteria were more abundant in the summer metaproteome, whereas winter was characterized by proteins from ammonia-oxidizing Marine Group I Crenarchaeota. Proteins prevalent in both seasons were from SAR11 and Rhodobacterales clades of Alphaproteobacteria, as well as many lineages of Gammaproteobacteria. The metaproteome data were used to elucidate the main metabolic and energy generation pathways and transport processes occurring at the microbial level in each season. In summer, autotrophic carbon assimilation appears to be driven by oxygenic photoautotrophy, consistent with high light availability and intensity. In contrast, during the dark polar winter, the metaproteome supported the occurrence of chemolithoautotrophy via the 3-hydroxypropionate/4-hydroxybutyrate cycle and the reverse tricarboxylic acid cycle of ammonia-oxidizing archaea and nitrite-oxidizing bacteria, respectively. Proteins involved in nitrification were also detected in the metaproteome. Taurine appears to be an important source of carbon and nitrogen for heterotrophs (especially SAR11), with transporters and enzymes for taurine uptake and degradation abundant in the metaproteome. Divergent heterotrophic strategies for Alphaproteobacteria and Flavobacteria were indicated by the metaproteome data, with Alphaproteobacteria capturing (by high-affinity transport) and processing labile solutes, and Flavobacteria expressing outer membrane receptors for particle adhesion to facilitate the exploitation of non-labile substrates. TonB-dependent receptors from Gammaproteobacteria and Flavobacteria (particularly in summer) were abundant, indicating that scavenging of substrates was likely an important strategy for these clades of Southern Ocean bacteria. This study provides the first insight into differences in functional processes occurring between summer and winter microbial communities in coastal Antarctic waters, and particularly highlights the important role that ‘dark’ carbon fixation has in winter. |
doi_str_mv | 10.1038/ismej.2012.28 |
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Taurine appears to be an important source of carbon and nitrogen for heterotrophs (especially SAR11), with transporters and enzymes for taurine uptake and degradation abundant in the metaproteome. Divergent heterotrophic strategies for Alphaproteobacteria and Flavobacteria were indicated by the metaproteome data, with Alphaproteobacteria capturing (by high-affinity transport) and processing labile solutes, and Flavobacteria expressing outer membrane receptors for particle adhesion to facilitate the exploitation of non-labile substrates. TonB-dependent receptors from Gammaproteobacteria and Flavobacteria (particularly in summer) were abundant, indicating that scavenging of substrates was likely an important strategy for these clades of Southern Ocean bacteria. This study provides the first insight into differences in functional processes occurring between summer and winter microbial communities in coastal Antarctic waters, and particularly highlights the important role that ‘dark’ carbon fixation has in winter.</description><identifier>ISSN: 1751-7362</identifier><identifier>EISSN: 1751-7370</identifier><identifier>DOI: 10.1038/ismej.2012.28</identifier><identifier>PMID: 22534610</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/158/2446/2447 ; 631/326/2565/855 ; 631/326/41/2535 ; 631/337/475 ; Adhesion ; Ammonia ; Ammonia - metabolism ; Antarctic Regions ; Archaea ; Bacteria ; Bacteria - classification ; Bacteria - metabolism ; Biomedical and Life Sciences ; Carbon ; Carbon fixation ; Coastal waters ; Crenarchaeota ; Crenarchaeota - classification ; Crenarchaeota - metabolism ; Ecology ; Evolutionary Biology ; Exploitation ; Flavobacteria ; Heterotrophic Processes ; Life Sciences ; Microbial activity ; Microbial Ecology ; Microbial Genetics and Genomics ; Microbiology ; Nitrification ; Nitrogen ; Oceans and Seas ; Original ; original-article ; Phylogeny ; Plankton - classification ; Plankton - metabolism ; Proteins ; Proteome - analysis ; Seasons ; Seawater - microbiology ; Solutes ; Substrates ; Summer ; Surface water ; Transport processes ; Water - metabolism ; Winter</subject><ispartof>The ISME Journal, 2012-10, Vol.6 (10), p.1883-1900</ispartof><rights>International Society for Microbial Ecology 2012</rights><rights>Copyright Nature Publishing Group Oct 2012</rights><rights>Copyright © 2012 International Society for Microbial Ecology 2012 International Society for Microbial Ecology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c487t-afaea89f9acc32aee843b5e78175c8dbfa9eb2707762a1b99df3360da3e8ff593</citedby><cites>FETCH-LOGICAL-c487t-afaea89f9acc32aee843b5e78175c8dbfa9eb2707762a1b99df3360da3e8ff593</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/PMC3446797/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3446797/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22534610$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Williams, Timothy J</creatorcontrib><creatorcontrib>Long, Emilie</creatorcontrib><creatorcontrib>Evans, Flavia</creatorcontrib><creatorcontrib>DeMaere, Mathew Z</creatorcontrib><creatorcontrib>Lauro, Federico M</creatorcontrib><creatorcontrib>Raftery, Mark J</creatorcontrib><creatorcontrib>Ducklow, Hugh</creatorcontrib><creatorcontrib>Grzymski, Joseph J</creatorcontrib><creatorcontrib>Murray, Alison E</creatorcontrib><creatorcontrib>Cavicchioli, Ricardo</creatorcontrib><title>A metaproteomic assessment of winter and summer bacterioplankton from Antarctic Peninsula coastal surface waters</title><title>The ISME Journal</title><addtitle>ISME J</addtitle><addtitle>ISME J</addtitle><description>A metaproteomic survey of surface coastal waters near Palmer Station on the Antarctic Peninsula, West Antarctica, was performed, revealing marked differences in the functional capacity of summer and winter communities of bacterioplankton. Proteins from Flavobacteria were more abundant in the summer metaproteome, whereas winter was characterized by proteins from ammonia-oxidizing Marine Group I Crenarchaeota. Proteins prevalent in both seasons were from SAR11 and Rhodobacterales clades of Alphaproteobacteria, as well as many lineages of Gammaproteobacteria. The metaproteome data were used to elucidate the main metabolic and energy generation pathways and transport processes occurring at the microbial level in each season. In summer, autotrophic carbon assimilation appears to be driven by oxygenic photoautotrophy, consistent with high light availability and intensity. In contrast, during the dark polar winter, the metaproteome supported the occurrence of chemolithoautotrophy via the 3-hydroxypropionate/4-hydroxybutyrate cycle and the reverse tricarboxylic acid cycle of ammonia-oxidizing archaea and nitrite-oxidizing bacteria, respectively. Proteins involved in nitrification were also detected in the metaproteome. Taurine appears to be an important source of carbon and nitrogen for heterotrophs (especially SAR11), with transporters and enzymes for taurine uptake and degradation abundant in the metaproteome. Divergent heterotrophic strategies for Alphaproteobacteria and Flavobacteria were indicated by the metaproteome data, with Alphaproteobacteria capturing (by high-affinity transport) and processing labile solutes, and Flavobacteria expressing outer membrane receptors for particle adhesion to facilitate the exploitation of non-labile substrates. TonB-dependent receptors from Gammaproteobacteria and Flavobacteria (particularly in summer) were abundant, indicating that scavenging of substrates was likely an important strategy for these clades of Southern Ocean bacteria. This study provides the first insight into differences in functional processes occurring between summer and winter microbial communities in coastal Antarctic waters, and particularly highlights the important role that ‘dark’ carbon fixation has in winter.</description><subject>631/158/2446/2447</subject><subject>631/326/2565/855</subject><subject>631/326/41/2535</subject><subject>631/337/475</subject><subject>Adhesion</subject><subject>Ammonia</subject><subject>Ammonia - metabolism</subject><subject>Antarctic Regions</subject><subject>Archaea</subject><subject>Bacteria</subject><subject>Bacteria - classification</subject><subject>Bacteria - metabolism</subject><subject>Biomedical and Life Sciences</subject><subject>Carbon</subject><subject>Carbon fixation</subject><subject>Coastal waters</subject><subject>Crenarchaeota</subject><subject>Crenarchaeota - classification</subject><subject>Crenarchaeota - metabolism</subject><subject>Ecology</subject><subject>Evolutionary Biology</subject><subject>Exploitation</subject><subject>Flavobacteria</subject><subject>Heterotrophic Processes</subject><subject>Life Sciences</subject><subject>Microbial activity</subject><subject>Microbial Ecology</subject><subject>Microbial Genetics and Genomics</subject><subject>Microbiology</subject><subject>Nitrification</subject><subject>Nitrogen</subject><subject>Oceans and Seas</subject><subject>Original</subject><subject>original-article</subject><subject>Phylogeny</subject><subject>Plankton - classification</subject><subject>Plankton - metabolism</subject><subject>Proteins</subject><subject>Proteome - analysis</subject><subject>Seasons</subject><subject>Seawater - microbiology</subject><subject>Solutes</subject><subject>Substrates</subject><subject>Summer</subject><subject>Surface water</subject><subject>Transport processes</subject><subject>Water - metabolism</subject><subject>Winter</subject><issn>1751-7362</issn><issn>1751-7370</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><recordid>eNqFkc1v1DAQxSNERUvhyBVZ4sIli78SOxekVcWXVIke2rM1ccYlS2IH26Hiv8fLllVBSJw88vzmjZ9fVb1gdMOo0G_GNONuwynjG64fVWdMNaxWQtHHx7rlp9XTlHaUNqpt1ZPqlPNGyJbRs2rZkhkzLDFkDPNoCaSEqWj6TIIjd6PPGAn4gaR1nkvZgy03Y1gm8F9z8MTFMJOtzxBtLvNX6Eef1gmIDZAyTGUwOrBI7qAMpmfViYMp4fP787y6ef_u-uJjffn5w6eL7WVtpVa5BgcIunMdWCs4IGop-gaVLp6sHnoHHfZcUaVaDqzvusEJ0dIBBGrnmk6cV28PusvazzjYYijCZJY4zhB_mACj-bPjxy_mNnw3QspWdaoIvL4XiOHbiimbeUwWp-Ibw5oMk6LjXHLd_h-lSqpWCrZXffUXugtr9OUnCiWpFop1ulD1gbIxpBTRHd_NqNnHbn7FbvaxG77nXz40e6R_51yAzQFIpeVvMT5c-y_Fn3VFvKs</recordid><startdate>20121001</startdate><enddate>20121001</enddate><creator>Williams, Timothy J</creator><creator>Long, Emilie</creator><creator>Evans, Flavia</creator><creator>DeMaere, Mathew Z</creator><creator>Lauro, Federico M</creator><creator>Raftery, Mark J</creator><creator>Ducklow, Hugh</creator><creator>Grzymski, Joseph J</creator><creator>Murray, Alison E</creator><creator>Cavicchioli, Ricardo</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</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>3V.</scope><scope>7QL</scope><scope>7SN</scope><scope>7ST</scope><scope>7T7</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PYCSY</scope><scope>SOI</scope><scope>7X8</scope><scope>7TN</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>5PM</scope></search><sort><creationdate>20121001</creationdate><title>A metaproteomic assessment of winter and summer bacterioplankton from Antarctic Peninsula coastal surface waters</title><author>Williams, Timothy J ; Long, Emilie ; Evans, Flavia ; DeMaere, Mathew Z ; Lauro, Federico M ; Raftery, Mark J ; Ducklow, Hugh ; Grzymski, Joseph J ; Murray, Alison E ; Cavicchioli, Ricardo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c487t-afaea89f9acc32aee843b5e78175c8dbfa9eb2707762a1b99df3360da3e8ff593</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>631/158/2446/2447</topic><topic>631/326/2565/855</topic><topic>631/326/41/2535</topic><topic>631/337/475</topic><topic>Adhesion</topic><topic>Ammonia</topic><topic>Ammonia - 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Proteins from Flavobacteria were more abundant in the summer metaproteome, whereas winter was characterized by proteins from ammonia-oxidizing Marine Group I Crenarchaeota. Proteins prevalent in both seasons were from SAR11 and Rhodobacterales clades of Alphaproteobacteria, as well as many lineages of Gammaproteobacteria. The metaproteome data were used to elucidate the main metabolic and energy generation pathways and transport processes occurring at the microbial level in each season. In summer, autotrophic carbon assimilation appears to be driven by oxygenic photoautotrophy, consistent with high light availability and intensity. In contrast, during the dark polar winter, the metaproteome supported the occurrence of chemolithoautotrophy via the 3-hydroxypropionate/4-hydroxybutyrate cycle and the reverse tricarboxylic acid cycle of ammonia-oxidizing archaea and nitrite-oxidizing bacteria, respectively. Proteins involved in nitrification were also detected in the metaproteome. Taurine appears to be an important source of carbon and nitrogen for heterotrophs (especially SAR11), with transporters and enzymes for taurine uptake and degradation abundant in the metaproteome. Divergent heterotrophic strategies for Alphaproteobacteria and Flavobacteria were indicated by the metaproteome data, with Alphaproteobacteria capturing (by high-affinity transport) and processing labile solutes, and Flavobacteria expressing outer membrane receptors for particle adhesion to facilitate the exploitation of non-labile substrates. TonB-dependent receptors from Gammaproteobacteria and Flavobacteria (particularly in summer) were abundant, indicating that scavenging of substrates was likely an important strategy for these clades of Southern Ocean bacteria. This study provides the first insight into differences in functional processes occurring between summer and winter microbial communities in coastal Antarctic waters, and particularly highlights the important role that ‘dark’ carbon fixation has in winter.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>22534610</pmid><doi>10.1038/ismej.2012.28</doi><tpages>18</tpages><oa>free_for_read</oa></addata></record> |
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subjects | 631/158/2446/2447 631/326/2565/855 631/326/41/2535 631/337/475 Adhesion Ammonia Ammonia - metabolism Antarctic Regions Archaea Bacteria Bacteria - classification Bacteria - metabolism Biomedical and Life Sciences Carbon Carbon fixation Coastal waters Crenarchaeota Crenarchaeota - classification Crenarchaeota - metabolism Ecology Evolutionary Biology Exploitation Flavobacteria Heterotrophic Processes Life Sciences Microbial activity Microbial Ecology Microbial Genetics and Genomics Microbiology Nitrification Nitrogen Oceans and Seas Original original-article Phylogeny Plankton - classification Plankton - metabolism Proteins Proteome - analysis Seasons Seawater - microbiology Solutes Substrates Summer Surface water Transport processes Water - metabolism Winter |
title | A metaproteomic assessment of winter and summer bacterioplankton from Antarctic Peninsula coastal surface waters |
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