Widespread Family of NAD+‑Dependent Sulfoquinovosidases at the Gateway to Sulfoquinovose Catabolism
The sulfosugar sulfoquinovose (SQ) is produced by photosynthetic plants, algae, and cyanobacteria on a scale of 10 billion tons per annum. Its degradation, which is essential to allow cycling of its constituent carbon and sulfur, involves specialized glycosidases termed sulfoquinovosidases (SQases),...
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| Veröffentlicht in: | Journal of the American Chemical Society 2023-12, Vol.145 (51), p.28216-28223 |
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| container_title | Journal of the American Chemical Society |
| container_volume | 145 |
| creator | Kaur, Arashdeep Pickles, Isabelle B. Sharma, Mahima Madeido Soler, Niccolay Scott, Nichollas E. Pidot, Sacha J. Goddard-Borger, Ethan D. Davies, Gideon J. Williams, Spencer J. |
| description | The sulfosugar sulfoquinovose (SQ) is produced by photosynthetic plants, algae, and cyanobacteria on a scale of 10 billion tons per annum. Its degradation, which is essential to allow cycling of its constituent carbon and sulfur, involves specialized glycosidases termed sulfoquinovosidases (SQases), which release SQ from sulfolipid glycoconjugates, so SQ can enter catabolism pathways. However, many SQ catabolic gene clusters lack a gene encoding a classical SQase. Here, we report the discovery of a new family of SQases that use an atypical oxidoreductive mechanism involving NAD+ as a catalytic cofactor. Three-dimensional X-ray structures of complexes with SQ and NAD+ provide insight into the catalytic mechanism, which involves transient oxidation at C3. Bioinformatic survey reveals this new family of NAD+-dependent SQases occurs within sulfoglycolytic and sulfolytic gene clusters that lack classical SQases and is distributed widely including within Roseobacter clade bacteria, suggesting an important contribution to marine sulfur cycling. |
| doi_str_mv | 10.1021/jacs.3c11126 |
| format | Article |
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Its degradation, which is essential to allow cycling of its constituent carbon and sulfur, involves specialized glycosidases termed sulfoquinovosidases (SQases), which release SQ from sulfolipid glycoconjugates, so SQ can enter catabolism pathways. However, many SQ catabolic gene clusters lack a gene encoding a classical SQase. Here, we report the discovery of a new family of SQases that use an atypical oxidoreductive mechanism involving NAD+ as a catalytic cofactor. Three-dimensional X-ray structures of complexes with SQ and NAD+ provide insight into the catalytic mechanism, which involves transient oxidation at C3. Bioinformatic survey reveals this new family of NAD+-dependent SQases occurs within sulfoglycolytic and sulfolytic gene clusters that lack classical SQases and is distributed widely including within Roseobacter clade bacteria, suggesting an important contribution to marine sulfur cycling.</description><identifier>ISSN: 0002-7863</identifier><identifier>EISSN: 1520-5126</identifier><identifier>DOI: 10.1021/jacs.3c11126</identifier><identifier>PMID: 38100472</identifier><language>eng</language><publisher>United States: American Chemical Society</publisher><subject>Metabolic Networks and Pathways ; Methylglucosides - chemistry ; Methylglucosides - metabolism ; NAD - metabolism ; Plants ; Sulfur - metabolism</subject><ispartof>Journal of the American Chemical Society, 2023-12, Vol.145 (51), p.28216-28223</ispartof><rights>2023 The Authors. 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Bioinformatic survey reveals this new family of NAD+-dependent SQases occurs within sulfoglycolytic and sulfolytic gene clusters that lack classical SQases and is distributed widely including within Roseobacter clade bacteria, suggesting an important contribution to marine sulfur cycling.</description><subject>Metabolic Networks and Pathways</subject><subject>Methylglucosides - chemistry</subject><subject>Methylglucosides - metabolism</subject><subject>NAD - metabolism</subject><subject>Plants</subject><subject>Sulfur - metabolism</subject><issn>0002-7863</issn><issn>1520-5126</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNptkE1Lw0AQhhdRbK3ePMseBY3uVzbJsbS2CkUPKh7DJDvBlCQbs4nSm3_Bv-gvMaVVEbzMBzzzzsxLyDFnF5wJfrmE1F3IlHMu9A4Zcl8wz-_rXTJkjAkvCLUckAPnln2rRMj3yUCGvK8DMST4lBt0dYNg6AzKvFhRm9Hb8fTs8_1jijVWBquW3ndFZl-6vLKv1uUGHDoKLW2fkc6hxTdY0db-pZBOoIXEFrkrD8leBoXDo20ekcfZ1cPk2lvczW8m44UHUovWUzpkSYIykhCEXCvDDIbM96UP0hitIpAq6KMCnQTAIQWV8kAJHmCkVCTkiJxudOumvwNdG5e5S7EooELbuVhETEQ69BXv0fMNmjbWuQazuG7yEppVzFm8NjZeGxtvje3xk61yl5RofuBvJ39Xr6eWtmuq_tH_tb4A7dWCHw</recordid><startdate>20231227</startdate><enddate>20231227</enddate><creator>Kaur, Arashdeep</creator><creator>Pickles, Isabelle B.</creator><creator>Sharma, Mahima</creator><creator>Madeido Soler, Niccolay</creator><creator>Scott, Nichollas E.</creator><creator>Pidot, Sacha J.</creator><creator>Goddard-Borger, Ethan D.</creator><creator>Davies, Gideon J.</creator><creator>Williams, Spencer J.</creator><general>American Chemical Society</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>7X8</scope><orcidid>https://orcid.org/0000-0003-1202-6614</orcidid><orcidid>https://orcid.org/0000-0002-8181-9733</orcidid><orcidid>https://orcid.org/0000-0001-6341-4364</orcidid><orcidid>https://orcid.org/0000-0003-2556-8316</orcidid><orcidid>https://orcid.org/0000-0002-7343-776X</orcidid><orcidid>https://orcid.org/0000-0003-3960-2212</orcidid></search><sort><creationdate>20231227</creationdate><title>Widespread Family of NAD+‑Dependent Sulfoquinovosidases at the Gateway to Sulfoquinovose Catabolism</title><author>Kaur, Arashdeep ; Pickles, Isabelle B. ; Sharma, Mahima ; Madeido Soler, Niccolay ; Scott, Nichollas E. ; Pidot, Sacha J. ; Goddard-Borger, Ethan D. ; Davies, Gideon J. ; Williams, Spencer J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a362t-4680bbe393a78164d0de805535a3dd649a34749a4a6b7a1aca4c174217e944923</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Metabolic Networks and Pathways</topic><topic>Methylglucosides - chemistry</topic><topic>Methylglucosides - metabolism</topic><topic>NAD - metabolism</topic><topic>Plants</topic><topic>Sulfur - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kaur, Arashdeep</creatorcontrib><creatorcontrib>Pickles, Isabelle B.</creatorcontrib><creatorcontrib>Sharma, Mahima</creatorcontrib><creatorcontrib>Madeido Soler, Niccolay</creatorcontrib><creatorcontrib>Scott, Nichollas E.</creatorcontrib><creatorcontrib>Pidot, Sacha J.</creatorcontrib><creatorcontrib>Goddard-Borger, Ethan D.</creatorcontrib><creatorcontrib>Davies, Gideon J.</creatorcontrib><creatorcontrib>Williams, Spencer 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>MEDLINE - Academic</collection><jtitle>Journal of the American Chemical Society</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kaur, Arashdeep</au><au>Pickles, Isabelle B.</au><au>Sharma, Mahima</au><au>Madeido Soler, Niccolay</au><au>Scott, Nichollas E.</au><au>Pidot, Sacha J.</au><au>Goddard-Borger, Ethan D.</au><au>Davies, Gideon J.</au><au>Williams, Spencer J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Widespread Family of NAD+‑Dependent Sulfoquinovosidases at the Gateway to Sulfoquinovose Catabolism</atitle><jtitle>Journal of the American Chemical Society</jtitle><addtitle>J. Am. Chem. Soc</addtitle><date>2023-12-27</date><risdate>2023</risdate><volume>145</volume><issue>51</issue><spage>28216</spage><epage>28223</epage><pages>28216-28223</pages><issn>0002-7863</issn><eissn>1520-5126</eissn><abstract>The sulfosugar sulfoquinovose (SQ) is produced by photosynthetic plants, algae, and cyanobacteria on a scale of 10 billion tons per annum. Its degradation, which is essential to allow cycling of its constituent carbon and sulfur, involves specialized glycosidases termed sulfoquinovosidases (SQases), which release SQ from sulfolipid glycoconjugates, so SQ can enter catabolism pathways. However, many SQ catabolic gene clusters lack a gene encoding a classical SQase. Here, we report the discovery of a new family of SQases that use an atypical oxidoreductive mechanism involving NAD+ as a catalytic cofactor. Three-dimensional X-ray structures of complexes with SQ and NAD+ provide insight into the catalytic mechanism, which involves transient oxidation at C3. 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| subjects | Metabolic Networks and Pathways Methylglucosides - chemistry Methylglucosides - metabolism NAD - metabolism Plants Sulfur - metabolism |
| title | Widespread Family of NAD+‑Dependent Sulfoquinovosidases at the Gateway to Sulfoquinovose Catabolism |
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