Comparative genomics and mutagenesis analyses of choline metabolism in the marine R oseobacter clade
Choline is ubiquitous in marine eukaryotes and appears to be widely distributed in surface marine waters; however, its metabolism by marine bacteria is poorly understood. Here, using comparative genomics and molecular genetic approaches, we reveal that the capacity for choline catabolism is widespre...
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Veröffentlicht in: | Environmental microbiology 2015-12, Vol.17 (12), p.5048-5062 |
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description | Choline is ubiquitous in marine eukaryotes and appears to be widely distributed in surface marine waters; however, its metabolism by marine bacteria is poorly understood. Here, using comparative genomics and molecular genetic approaches, we reveal that the capacity for choline catabolism is widespread in marine heterotrophs of the marine
Roseobacter
clade (
MRC
). Using the model bacterium
R
uegeria pomeroyi
, we confirm that the
bet
A
,
bet
B
and
bet
C
genes, encoding choline dehydrogenase, betaine aldehyde dehydrogenase and choline sulfatase, respectively, are involved in choline metabolism. The
bet
T
gene, encoding an organic solute transporter, was essential for the rapid uptake of choline but not glycine betaine (
GBT
). Growth of choline and
GBT
as a sole carbon source resulted in the re‐mineralization of these nitrogen‐rich compounds into ammonium. Oxidation of the methyl groups from choline requires formyltetrahydrofolate synthetase encoded by
fhs
in
R
. pomeroyi
, deletion of which resulted in incomplete degradation of
GBT
. We demonstrate that this was due to an imbalance in the supply of reducing equivalents required for choline catabolism, which can be alleviated by the addition of formate. Together, our results demonstrate that choline metabolism is ubiquitous in the
MRC
and reveal the role of Fhs in methyl group oxidation in
R
. pomeroyi
. |
doi_str_mv | 10.1111/1462-2920.12943 |
format | Article |
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Roseobacter
clade (
MRC
). Using the model bacterium
R
uegeria pomeroyi
, we confirm that the
bet
A
,
bet
B
and
bet
C
genes, encoding choline dehydrogenase, betaine aldehyde dehydrogenase and choline sulfatase, respectively, are involved in choline metabolism. The
bet
T
gene, encoding an organic solute transporter, was essential for the rapid uptake of choline but not glycine betaine (
GBT
). Growth of choline and
GBT
as a sole carbon source resulted in the re‐mineralization of these nitrogen‐rich compounds into ammonium. Oxidation of the methyl groups from choline requires formyltetrahydrofolate synthetase encoded by
fhs
in
R
. pomeroyi
, deletion of which resulted in incomplete degradation of
GBT
. We demonstrate that this was due to an imbalance in the supply of reducing equivalents required for choline catabolism, which can be alleviated by the addition of formate. Together, our results demonstrate that choline metabolism is ubiquitous in the
MRC
and reveal the role of Fhs in methyl group oxidation in
R
. pomeroyi
.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.12943</identifier><identifier>PMID: 26058574</identifier><language>eng</language><publisher>Hoboken: John Wiley and Sons Inc</publisher><ispartof>Environmental microbiology, 2015-12, Vol.17 (12), p.5048-5062</ispartof><rights>2015 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c1412-1d4e88b57b4b2a52b28cd0124fcefb836c3ccdacb4b65ea908dc62b91a26ecd23</citedby><cites>FETCH-LOGICAL-c1412-1d4e88b57b4b2a52b28cd0124fcefb836c3ccdacb4b65ea908dc62b91a26ecd23</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids></links><search><creatorcontrib>Lidbury, Ian</creatorcontrib><creatorcontrib>Kimberley, George</creatorcontrib><creatorcontrib>Scanlan, David J.</creatorcontrib><creatorcontrib>Murrell, J. Colin</creatorcontrib><creatorcontrib>Chen, Yin</creatorcontrib><title>Comparative genomics and mutagenesis analyses of choline metabolism in the marine R oseobacter clade</title><title>Environmental microbiology</title><description>Choline is ubiquitous in marine eukaryotes and appears to be widely distributed in surface marine waters; however, its metabolism by marine bacteria is poorly understood. Here, using comparative genomics and molecular genetic approaches, we reveal that the capacity for choline catabolism is widespread in marine heterotrophs of the marine
Roseobacter
clade (
MRC
). Using the model bacterium
R
uegeria pomeroyi
, we confirm that the
bet
A
,
bet
B
and
bet
C
genes, encoding choline dehydrogenase, betaine aldehyde dehydrogenase and choline sulfatase, respectively, are involved in choline metabolism. The
bet
T
gene, encoding an organic solute transporter, was essential for the rapid uptake of choline but not glycine betaine (
GBT
). Growth of choline and
GBT
as a sole carbon source resulted in the re‐mineralization of these nitrogen‐rich compounds into ammonium. Oxidation of the methyl groups from choline requires formyltetrahydrofolate synthetase encoded by
fhs
in
R
. pomeroyi
, deletion of which resulted in incomplete degradation of
GBT
. We demonstrate that this was due to an imbalance in the supply of reducing equivalents required for choline catabolism, which can be alleviated by the addition of formate. Together, our results demonstrate that choline metabolism is ubiquitous in the
MRC
and reveal the role of Fhs in methyl group oxidation in
R
. pomeroyi
.</description><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><recordid>eNpVUNtKAzEQDaJYrT77mh9Ym2SztxdBijcoCKLPYTKZbSO7m7LZFvr37lopOC9zLsxhOIzdSXEvx1lInatEVWqkqtLpGbs6KecnLNWMXcf4LYQs0kJcspnKRVZmhb5ibhnaLfQw-D3xNXWh9Rg5dI63uwFGgaKfODSHSJGHmuMmNL4j3tIAdoSx5b7jw2ZUoJ-MDx4iBQs4UM-xAUc37KKGJtLt356zr-enz-Vrsnp_eVs-rhKUWqpEOk1labPCaqsgU1aV6IRUukaqbZnmmCI6wNHOM4JKlA5zZSsJKid0Kp2zh2Pudmdbckjd0ENjtr0fXzuYAN78dzq_MeuwN7rQOq-mgMUxAPsQY0_16VYKMxVupkrNVK_5LTz9AYFjdRI</recordid><startdate>201512</startdate><enddate>201512</enddate><creator>Lidbury, Ian</creator><creator>Kimberley, George</creator><creator>Scanlan, David J.</creator><creator>Murrell, J. Colin</creator><creator>Chen, Yin</creator><general>John Wiley and Sons Inc</general><scope>AAYXX</scope><scope>CITATION</scope><scope>5PM</scope></search><sort><creationdate>201512</creationdate><title>Comparative genomics and mutagenesis analyses of choline metabolism in the marine R oseobacter clade</title><author>Lidbury, Ian ; Kimberley, George ; Scanlan, David J. ; Murrell, J. Colin ; Chen, Yin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c1412-1d4e88b57b4b2a52b28cd0124fcefb836c3ccdacb4b65ea908dc62b91a26ecd23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lidbury, Ian</creatorcontrib><creatorcontrib>Kimberley, George</creatorcontrib><creatorcontrib>Scanlan, David J.</creatorcontrib><creatorcontrib>Murrell, J. Colin</creatorcontrib><creatorcontrib>Chen, Yin</creatorcontrib><collection>CrossRef</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lidbury, Ian</au><au>Kimberley, George</au><au>Scanlan, David J.</au><au>Murrell, J. Colin</au><au>Chen, Yin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Comparative genomics and mutagenesis analyses of choline metabolism in the marine R oseobacter clade</atitle><jtitle>Environmental microbiology</jtitle><date>2015-12</date><risdate>2015</risdate><volume>17</volume><issue>12</issue><spage>5048</spage><epage>5062</epage><pages>5048-5062</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Choline is ubiquitous in marine eukaryotes and appears to be widely distributed in surface marine waters; however, its metabolism by marine bacteria is poorly understood. Here, using comparative genomics and molecular genetic approaches, we reveal that the capacity for choline catabolism is widespread in marine heterotrophs of the marine
Roseobacter
clade (
MRC
). Using the model bacterium
R
uegeria pomeroyi
, we confirm that the
bet
A
,
bet
B
and
bet
C
genes, encoding choline dehydrogenase, betaine aldehyde dehydrogenase and choline sulfatase, respectively, are involved in choline metabolism. The
bet
T
gene, encoding an organic solute transporter, was essential for the rapid uptake of choline but not glycine betaine (
GBT
). Growth of choline and
GBT
as a sole carbon source resulted in the re‐mineralization of these nitrogen‐rich compounds into ammonium. Oxidation of the methyl groups from choline requires formyltetrahydrofolate synthetase encoded by
fhs
in
R
. pomeroyi
, deletion of which resulted in incomplete degradation of
GBT
. We demonstrate that this was due to an imbalance in the supply of reducing equivalents required for choline catabolism, which can be alleviated by the addition of formate. Together, our results demonstrate that choline metabolism is ubiquitous in the
MRC
and reveal the role of Fhs in methyl group oxidation in
R
. pomeroyi
.</abstract><cop>Hoboken</cop><pub>John Wiley and Sons Inc</pub><pmid>26058574</pmid><doi>10.1111/1462-2920.12943</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
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language | eng |
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source | Wiley Online Library All Journals |
title | Comparative genomics and mutagenesis analyses of choline metabolism in the marine R oseobacter clade |
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