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Chlamydomonas reinhardtii thermal tolerance enhancement mediated by a mutualistic interaction with vitamin B12-producing bacteria
Temperature is one of the most important environmental factors affecting the growth and survival of microorganisms and in light of current global patterns is of particular interest. Here, we highlight studies revealing how vitamin B 12 (cobalamin)-producing bacteria increase the fitness of the unice...
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Published in: | The ISME Journal 2013-08, Vol.7 (8), p.1544-1555 |
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creator | Xie, Bo Bishop, Shawn Stessman, Dan Wright, David Spalding, Martin H Halverson, Larry J |
description | Temperature is one of the most important environmental factors affecting the growth and survival of microorganisms and in light of current global patterns is of particular interest. Here, we highlight studies revealing how vitamin B
12
(cobalamin)-producing bacteria increase the fitness of the unicellular alga
Chlamydomonas reinhardtii
following an increase in environmental temperature. Heat stress represses
C. reinhardtii
cobalamin-independent methionine synthase (
METE)
gene expression coinciding with a reduction in METE-mediated methionine synthase activity, chlorosis and cell death during heat stress. However, in the presence of cobalamin-producing bacteria or exogenous cobalamin amendments
C. reinhardtii
cobalamin-dependent methionine synthase METH-mediated methionine biosynthesis is functional at temperatures that result in
C. reinhardtii
death in the absence of cobalamin. Artificial microRNA silencing of
C. reinhardtii METH
expression leads to nearly complete loss of cobalamin-mediated enhancement of thermal tolerance. This suggests that methionine biosynthesis is an essential cellular mechanism for adaptation by
C. reinhardtii
to thermal stress. Increased fitness advantage of METH under environmentally stressful conditions could explain the selective pressure for retaining the
METH
gene in algae and the apparent independent loss of the
METE
gene in various algal species. Our results show that how an organism acclimates to a change in its abiotic environment depends critically on co-occurring species, the nature of that interaction, and how those species interactions evolve. |
doi_str_mv | 10.1038/ismej.2013.43 |
format | article |
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12
(cobalamin)-producing bacteria increase the fitness of the unicellular alga
Chlamydomonas reinhardtii
following an increase in environmental temperature. Heat stress represses
C. reinhardtii
cobalamin-independent methionine synthase (
METE)
gene expression coinciding with a reduction in METE-mediated methionine synthase activity, chlorosis and cell death during heat stress. However, in the presence of cobalamin-producing bacteria or exogenous cobalamin amendments
C. reinhardtii
cobalamin-dependent methionine synthase METH-mediated methionine biosynthesis is functional at temperatures that result in
C. reinhardtii
death in the absence of cobalamin. Artificial microRNA silencing of
C. reinhardtii METH
expression leads to nearly complete loss of cobalamin-mediated enhancement of thermal tolerance. This suggests that methionine biosynthesis is an essential cellular mechanism for adaptation by
C. reinhardtii
to thermal stress. Increased fitness advantage of METH under environmentally stressful conditions could explain the selective pressure for retaining the
METH
gene in algae and the apparent independent loss of the
METE
gene in various algal species. Our results show that how an organism acclimates to a change in its abiotic environment depends critically on co-occurring species, the nature of that interaction, and how those species interactions evolve.</description><identifier>ISSN: 1751-7362</identifier><identifier>EISSN: 1751-7370</identifier><identifier>DOI: 10.1038/ismej.2013.43</identifier><identifier>PMID: 23486253</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>5-Methyltetrahydrofolate-Homocysteine S-Methyltransferase - genetics ; 5-Methyltetrahydrofolate-Homocysteine S-Methyltransferase - metabolism ; 631/326/41 ; 631/326/41/1969 ; 704/158/853 ; Algae ; Bacteria ; Bacteria - genetics ; Bacteria - metabolism ; Bacterial Physiological Phenomena ; Biomedical and Life Sciences ; Biosynthesis ; Chlamydomonas reinhardtii - drug effects ; Chlamydomonas reinhardtii - enzymology ; Chlamydomonas reinhardtii - genetics ; Chlamydomonas reinhardtii - microbiology ; Chlamydomonas reinhardtii - physiology ; Ecology ; Environmental factors ; Evolutionary Biology ; Gene Expression Regulation, Plant ; Heat tolerance ; Life Sciences ; Methionine - genetics ; Methionine - metabolism ; Methionine - pharmacology ; Microbial Ecology ; Microbial Genetics and Genomics ; Microbiology ; Microorganisms ; Mortality ; Original ; original-article ; Sinorhizobium meliloti - genetics ; Sinorhizobium meliloti - metabolism ; Sinorhizobium meliloti - physiology ; Stress, Physiological ; Symbiosis ; Temperature ; Thermal stress ; Vitamin B 12 - genetics ; Vitamin B 12 - metabolism ; Vitamin B 12 - pharmacology ; Vitamin B Complex - pharmacology</subject><ispartof>The ISME Journal, 2013-08, Vol.7 (8), p.1544-1555</ispartof><rights>International Society for Microbial Ecology 2013</rights><rights>Copyright Nature Publishing Group Aug 2013</rights><rights>Copyright © 2013 International Society for Microbial Ecology 2013 International Society for Microbial Ecology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3693-964806b4eccbf92e97f381c819b7b1f01217cad2a07bc871fbeff370ba24ea343</citedby><cites>FETCH-LOGICAL-c3693-964806b4eccbf92e97f381c819b7b1f01217cad2a07bc871fbeff370ba24ea343</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/PMC3721113/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3721113/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27903,27904,53770,53772</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23486253$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Xie, Bo</creatorcontrib><creatorcontrib>Bishop, Shawn</creatorcontrib><creatorcontrib>Stessman, Dan</creatorcontrib><creatorcontrib>Wright, David</creatorcontrib><creatorcontrib>Spalding, Martin H</creatorcontrib><creatorcontrib>Halverson, Larry J</creatorcontrib><title>Chlamydomonas reinhardtii thermal tolerance enhancement mediated by a mutualistic interaction with vitamin B12-producing bacteria</title><title>The ISME Journal</title><addtitle>ISME J</addtitle><addtitle>ISME J</addtitle><description>Temperature is one of the most important environmental factors affecting the growth and survival of microorganisms and in light of current global patterns is of particular interest. Here, we highlight studies revealing how vitamin B
12
(cobalamin)-producing bacteria increase the fitness of the unicellular alga
Chlamydomonas reinhardtii
following an increase in environmental temperature. Heat stress represses
C. reinhardtii
cobalamin-independent methionine synthase (
METE)
gene expression coinciding with a reduction in METE-mediated methionine synthase activity, chlorosis and cell death during heat stress. However, in the presence of cobalamin-producing bacteria or exogenous cobalamin amendments
C. reinhardtii
cobalamin-dependent methionine synthase METH-mediated methionine biosynthesis is functional at temperatures that result in
C. reinhardtii
death in the absence of cobalamin. Artificial microRNA silencing of
C. reinhardtii METH
expression leads to nearly complete loss of cobalamin-mediated enhancement of thermal tolerance. This suggests that methionine biosynthesis is an essential cellular mechanism for adaptation by
C. reinhardtii
to thermal stress. Increased fitness advantage of METH under environmentally stressful conditions could explain the selective pressure for retaining the
METH
gene in algae and the apparent independent loss of the
METE
gene in various algal species. Our results show that how an organism acclimates to a change in its abiotic environment depends critically on co-occurring species, the nature of that interaction, and how those species interactions evolve.</description><subject>5-Methyltetrahydrofolate-Homocysteine S-Methyltransferase - genetics</subject><subject>5-Methyltetrahydrofolate-Homocysteine S-Methyltransferase - metabolism</subject><subject>631/326/41</subject><subject>631/326/41/1969</subject><subject>704/158/853</subject><subject>Algae</subject><subject>Bacteria</subject><subject>Bacteria - genetics</subject><subject>Bacteria - metabolism</subject><subject>Bacterial Physiological Phenomena</subject><subject>Biomedical and Life Sciences</subject><subject>Biosynthesis</subject><subject>Chlamydomonas reinhardtii - drug effects</subject><subject>Chlamydomonas reinhardtii - enzymology</subject><subject>Chlamydomonas reinhardtii - genetics</subject><subject>Chlamydomonas reinhardtii - microbiology</subject><subject>Chlamydomonas reinhardtii - physiology</subject><subject>Ecology</subject><subject>Environmental factors</subject><subject>Evolutionary Biology</subject><subject>Gene Expression Regulation, Plant</subject><subject>Heat tolerance</subject><subject>Life Sciences</subject><subject>Methionine - genetics</subject><subject>Methionine - metabolism</subject><subject>Methionine - pharmacology</subject><subject>Microbial Ecology</subject><subject>Microbial Genetics and Genomics</subject><subject>Microbiology</subject><subject>Microorganisms</subject><subject>Mortality</subject><subject>Original</subject><subject>original-article</subject><subject>Sinorhizobium meliloti - genetics</subject><subject>Sinorhizobium meliloti - metabolism</subject><subject>Sinorhizobium meliloti - physiology</subject><subject>Stress, Physiological</subject><subject>Symbiosis</subject><subject>Temperature</subject><subject>Thermal stress</subject><subject>Vitamin B 12 - genetics</subject><subject>Vitamin B 12 - metabolism</subject><subject>Vitamin B 12 - pharmacology</subject><subject>Vitamin B Complex - pharmacology</subject><issn>1751-7362</issn><issn>1751-7370</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><recordid>eNptkc1v1DAQxSNERUvhyBVZ4pzFY2fj5IIEK76kSr2Us2U7k41Xsb3YTtEe-c_xsmVVpJ7G0vvpzRu_qnoDdAWUd-9tcrhbMQp81fBn1RWINdSCC_r8_G7ZZfUypR2la9G24kV1yXjTtWzNr6rfm2lW7jAEF7xKJKL1k4pDtpbkCaNTM8lhxqi8QYJFK9Ohz8ThYFXGgegDUcQteVGzTdkaYn0uvMk2ePLL5onc26yc9eQTsHofw7AY67dEFwSjVa-qi1HNCV8_zOvqx5fPd5tv9c3t1--bjze14W3P675tOtrqBo3RY8-wFyPvwHTQa6FhpMBAGDUwRYU2nYBR4ziWb9CKNah4w6-rDyff_aJLeFOOiGqW-2idigcZlJX_K95OchvuJRcMAHgxePdgEMPPBVOWu7BEXzJLaABoD5T2hapPlIkhpYjjeQNQeWxM_m1MHhuTzdH17eNYZ_pfRQVYnYBUJL_F-Gjtk45_AC88pl0</recordid><startdate>201308</startdate><enddate>201308</enddate><creator>Xie, Bo</creator><creator>Bishop, Shawn</creator><creator>Stessman, Dan</creator><creator>Wright, David</creator><creator>Spalding, Martin H</creator><creator>Halverson, Larry J</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>AEUYN</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>5PM</scope></search><sort><creationdate>201308</creationdate><title>Chlamydomonas reinhardtii thermal tolerance enhancement mediated by a mutualistic interaction with vitamin B12-producing bacteria</title><author>Xie, Bo ; Bishop, Shawn ; Stessman, Dan ; Wright, David ; Spalding, Martin H ; Halverson, Larry J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3693-964806b4eccbf92e97f381c819b7b1f01217cad2a07bc871fbeff370ba24ea343</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>5-Methyltetrahydrofolate-Homocysteine S-Methyltransferase - genetics</topic><topic>5-Methyltetrahydrofolate-Homocysteine S-Methyltransferase - metabolism</topic><topic>631/326/41</topic><topic>631/326/41/1969</topic><topic>704/158/853</topic><topic>Algae</topic><topic>Bacteria</topic><topic>Bacteria - genetics</topic><topic>Bacteria - metabolism</topic><topic>Bacterial Physiological Phenomena</topic><topic>Biomedical and Life Sciences</topic><topic>Biosynthesis</topic><topic>Chlamydomonas reinhardtii - drug effects</topic><topic>Chlamydomonas reinhardtii - enzymology</topic><topic>Chlamydomonas reinhardtii - genetics</topic><topic>Chlamydomonas reinhardtii - microbiology</topic><topic>Chlamydomonas reinhardtii - physiology</topic><topic>Ecology</topic><topic>Environmental factors</topic><topic>Evolutionary Biology</topic><topic>Gene Expression Regulation, Plant</topic><topic>Heat tolerance</topic><topic>Life Sciences</topic><topic>Methionine - genetics</topic><topic>Methionine - metabolism</topic><topic>Methionine - pharmacology</topic><topic>Microbial Ecology</topic><topic>Microbial Genetics and Genomics</topic><topic>Microbiology</topic><topic>Microorganisms</topic><topic>Mortality</topic><topic>Original</topic><topic>original-article</topic><topic>Sinorhizobium meliloti - genetics</topic><topic>Sinorhizobium meliloti - metabolism</topic><topic>Sinorhizobium meliloti - physiology</topic><topic>Stress, Physiological</topic><topic>Symbiosis</topic><topic>Temperature</topic><topic>Thermal stress</topic><topic>Vitamin B 12 - genetics</topic><topic>Vitamin B 12 - metabolism</topic><topic>Vitamin B 12 - pharmacology</topic><topic>Vitamin B Complex - pharmacology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Xie, Bo</creatorcontrib><creatorcontrib>Bishop, Shawn</creatorcontrib><creatorcontrib>Stessman, Dan</creatorcontrib><creatorcontrib>Wright, David</creatorcontrib><creatorcontrib>Spalding, Martin H</creatorcontrib><creatorcontrib>Halverson, Larry J</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>ProQuest Health and Medical</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>ProQuest Biological Science Journals</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Environmental Science Collection</collection><collection>Environment Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The ISME Journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xie, Bo</au><au>Bishop, Shawn</au><au>Stessman, Dan</au><au>Wright, David</au><au>Spalding, Martin H</au><au>Halverson, Larry J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Chlamydomonas reinhardtii thermal tolerance enhancement mediated by a mutualistic interaction with vitamin B12-producing bacteria</atitle><jtitle>The ISME Journal</jtitle><stitle>ISME J</stitle><addtitle>ISME J</addtitle><date>2013-08</date><risdate>2013</risdate><volume>7</volume><issue>8</issue><spage>1544</spage><epage>1555</epage><pages>1544-1555</pages><issn>1751-7362</issn><eissn>1751-7370</eissn><abstract>Temperature is one of the most important environmental factors affecting the growth and survival of microorganisms and in light of current global patterns is of particular interest. Here, we highlight studies revealing how vitamin B
12
(cobalamin)-producing bacteria increase the fitness of the unicellular alga
Chlamydomonas reinhardtii
following an increase in environmental temperature. Heat stress represses
C. reinhardtii
cobalamin-independent methionine synthase (
METE)
gene expression coinciding with a reduction in METE-mediated methionine synthase activity, chlorosis and cell death during heat stress. However, in the presence of cobalamin-producing bacteria or exogenous cobalamin amendments
C. reinhardtii
cobalamin-dependent methionine synthase METH-mediated methionine biosynthesis is functional at temperatures that result in
C. reinhardtii
death in the absence of cobalamin. Artificial microRNA silencing of
C. reinhardtii METH
expression leads to nearly complete loss of cobalamin-mediated enhancement of thermal tolerance. This suggests that methionine biosynthesis is an essential cellular mechanism for adaptation by
C. reinhardtii
to thermal stress. Increased fitness advantage of METH under environmentally stressful conditions could explain the selective pressure for retaining the
METH
gene in algae and the apparent independent loss of the
METE
gene in various algal species. Our results show that how an organism acclimates to a change in its abiotic environment depends critically on co-occurring species, the nature of that interaction, and how those species interactions evolve.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>23486253</pmid><doi>10.1038/ismej.2013.43</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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subjects | 5-Methyltetrahydrofolate-Homocysteine S-Methyltransferase - genetics 5-Methyltetrahydrofolate-Homocysteine S-Methyltransferase - metabolism 631/326/41 631/326/41/1969 704/158/853 Algae Bacteria Bacteria - genetics Bacteria - metabolism Bacterial Physiological Phenomena Biomedical and Life Sciences Biosynthesis Chlamydomonas reinhardtii - drug effects Chlamydomonas reinhardtii - enzymology Chlamydomonas reinhardtii - genetics Chlamydomonas reinhardtii - microbiology Chlamydomonas reinhardtii - physiology Ecology Environmental factors Evolutionary Biology Gene Expression Regulation, Plant Heat tolerance Life Sciences Methionine - genetics Methionine - metabolism Methionine - pharmacology Microbial Ecology Microbial Genetics and Genomics Microbiology Microorganisms Mortality Original original-article Sinorhizobium meliloti - genetics Sinorhizobium meliloti - metabolism Sinorhizobium meliloti - physiology Stress, Physiological Symbiosis Temperature Thermal stress Vitamin B 12 - genetics Vitamin B 12 - metabolism Vitamin B 12 - pharmacology Vitamin B Complex - pharmacology |
title | Chlamydomonas reinhardtii thermal tolerance enhancement mediated by a mutualistic interaction with vitamin B12-producing bacteria |
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