Biochemical Basis of Xylooligosaccharide Utilisation by Gut Bacteria
Xylan is one of the major structural components of the plant cell wall. Xylan present in the human diet reaches the large intestine undigested and becomes a substrate to species of the gut microbiota. Here, we characterised the capacity of and strains to utilise xylan derivatives. We showed that ATC...
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| Veröffentlicht in: | International journal of molecular sciences 2022-03, Vol.23 (6), p.2992 |
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| creator | Singh, Ravindra Pal Bhaiyya, Raja Thakur, Raksha Niharika, Jayashree Singh, Chandrajeet Latousakis, Dimitrios Saalbach, Gerhard Nepogodiev, Sergey A Singh, Praveen Sharma, Sukesh Chander Sengupta, Shantanu Juge, Nathalie Field, Robert A |
| description | Xylan is one of the major structural components of the plant cell wall. Xylan present in the human diet reaches the large intestine undigested and becomes a substrate to species of the gut microbiota. Here, we characterised the capacity of
and
strains to utilise xylan derivatives. We showed that
ATCC 53608 and
ATCC 27340 produced β-D-xylosidases, enabling growth on xylooligosaccharide (XOS). The recombinant enzymes were highly active on artificial (
-nitrophenyl β-D-xylopyranoside) and natural (xylobiose, xylotriose, and xylotetraose) substrates, and showed transxylosylation activity and tolerance to xylose inhibition. The enzymes belong to glycoside hydrolase family 120 with Asp as nucleophile and Glu as proton donor, as shown by homology modelling and confirmed by site-directed mutagenesis. In silico analysis revealed that these enzymes were part of a gene cluster in
but not in
strains, and quantitative proteomics identified other enzymes and transporters involved in
XOS utilisation. Based on these findings, we proposed a model for an XOS metabolism pathway in
and
strains. Together with phylogenetic analyses, the data also revealed the extended xylanolytic potential of the gut microbiota. |
| doi_str_mv | 10.3390/ijms23062992 |
| format | Article |
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and
strains to utilise xylan derivatives. We showed that
ATCC 53608 and
ATCC 27340 produced β-D-xylosidases, enabling growth on xylooligosaccharide (XOS). The recombinant enzymes were highly active on artificial (
-nitrophenyl β-D-xylopyranoside) and natural (xylobiose, xylotriose, and xylotetraose) substrates, and showed transxylosylation activity and tolerance to xylose inhibition. The enzymes belong to glycoside hydrolase family 120 with Asp as nucleophile and Glu as proton donor, as shown by homology modelling and confirmed by site-directed mutagenesis. In silico analysis revealed that these enzymes were part of a gene cluster in
but not in
strains, and quantitative proteomics identified other enzymes and transporters involved in
XOS utilisation. Based on these findings, we proposed a model for an XOS metabolism pathway in
and
strains. Together with phylogenetic analyses, the data also revealed the extended xylanolytic potential of the gut microbiota.</description><identifier>ISSN: 1422-0067</identifier><identifier>ISSN: 1661-6596</identifier><identifier>EISSN: 1422-0067</identifier><identifier>DOI: 10.3390/ijms23062992</identifier><identifier>PMID: 35328413</identifier><language>eng</language><publisher>Switzerland: MDPI AG</publisher><subject>Bacteria ; Bacteria - genetics ; Bacteria - metabolism ; Cell walls ; Digestive system ; Enzymes ; Genes ; Genomes ; Glucuronates ; Glycosidases ; Glycoside hydrolase ; Gram-positive bacteria ; Homology ; Humans ; Hydrolase ; Intestinal microflora ; Intestine ; Large intestine ; Microbiota ; Oligosaccharides ; Phylogeny ; Proteomics ; Site-directed mutagenesis ; Strains (organisms) ; Substrate Specificity ; Xylan ; Xylans - metabolism ; Xylopyranoside ; Xylosidases - metabolism</subject><ispartof>International journal of molecular sciences, 2022-03, Vol.23 (6), p.2992</ispartof><rights>2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2022 by the authors. 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c412t-4126a57c024b86930ec5785f11e3bab92a10f165d87fe152fec9c1e4a63857e33</citedby><cites>FETCH-LOGICAL-c412t-4126a57c024b86930ec5785f11e3bab92a10f165d87fe152fec9c1e4a63857e33</cites><orcidid>0000-0002-2472-9328 ; 0000-0001-7889-7688 ; 0000-0001-8515-1315 ; 0000-0001-9796-4612 ; 0000-0001-8574-0275</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8954004/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8954004/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35328413$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Singh, Ravindra Pal</creatorcontrib><creatorcontrib>Bhaiyya, Raja</creatorcontrib><creatorcontrib>Thakur, Raksha</creatorcontrib><creatorcontrib>Niharika, Jayashree</creatorcontrib><creatorcontrib>Singh, Chandrajeet</creatorcontrib><creatorcontrib>Latousakis, Dimitrios</creatorcontrib><creatorcontrib>Saalbach, Gerhard</creatorcontrib><creatorcontrib>Nepogodiev, Sergey A</creatorcontrib><creatorcontrib>Singh, Praveen</creatorcontrib><creatorcontrib>Sharma, Sukesh Chander</creatorcontrib><creatorcontrib>Sengupta, Shantanu</creatorcontrib><creatorcontrib>Juge, Nathalie</creatorcontrib><creatorcontrib>Field, Robert A</creatorcontrib><title>Biochemical Basis of Xylooligosaccharide Utilisation by Gut Bacteria</title><title>International journal of molecular sciences</title><addtitle>Int J Mol Sci</addtitle><description>Xylan is one of the major structural components of the plant cell wall. Xylan present in the human diet reaches the large intestine undigested and becomes a substrate to species of the gut microbiota. Here, we characterised the capacity of
and
strains to utilise xylan derivatives. We showed that
ATCC 53608 and
ATCC 27340 produced β-D-xylosidases, enabling growth on xylooligosaccharide (XOS). The recombinant enzymes were highly active on artificial (
-nitrophenyl β-D-xylopyranoside) and natural (xylobiose, xylotriose, and xylotetraose) substrates, and showed transxylosylation activity and tolerance to xylose inhibition. The enzymes belong to glycoside hydrolase family 120 with Asp as nucleophile and Glu as proton donor, as shown by homology modelling and confirmed by site-directed mutagenesis. In silico analysis revealed that these enzymes were part of a gene cluster in
but not in
strains, and quantitative proteomics identified other enzymes and transporters involved in
XOS utilisation. Based on these findings, we proposed a model for an XOS metabolism pathway in
and
strains. Together with phylogenetic analyses, the data also revealed the extended xylanolytic potential of the gut microbiota.</description><subject>Bacteria</subject><subject>Bacteria - genetics</subject><subject>Bacteria - metabolism</subject><subject>Cell walls</subject><subject>Digestive system</subject><subject>Enzymes</subject><subject>Genes</subject><subject>Genomes</subject><subject>Glucuronates</subject><subject>Glycosidases</subject><subject>Glycoside hydrolase</subject><subject>Gram-positive bacteria</subject><subject>Homology</subject><subject>Humans</subject><subject>Hydrolase</subject><subject>Intestinal microflora</subject><subject>Intestine</subject><subject>Large intestine</subject><subject>Microbiota</subject><subject>Oligosaccharides</subject><subject>Phylogeny</subject><subject>Proteomics</subject><subject>Site-directed mutagenesis</subject><subject>Strains (organisms)</subject><subject>Substrate Specificity</subject><subject>Xylan</subject><subject>Xylans - metabolism</subject><subject>Xylopyranoside</subject><subject>Xylosidases - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>International journal of molecular sciences</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Singh, Ravindra Pal</au><au>Bhaiyya, Raja</au><au>Thakur, Raksha</au><au>Niharika, Jayashree</au><au>Singh, Chandrajeet</au><au>Latousakis, Dimitrios</au><au>Saalbach, Gerhard</au><au>Nepogodiev, Sergey A</au><au>Singh, Praveen</au><au>Sharma, Sukesh Chander</au><au>Sengupta, Shantanu</au><au>Juge, Nathalie</au><au>Field, Robert A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Biochemical Basis of Xylooligosaccharide Utilisation by Gut Bacteria</atitle><jtitle>International journal of molecular sciences</jtitle><addtitle>Int J Mol Sci</addtitle><date>2022-03-10</date><risdate>2022</risdate><volume>23</volume><issue>6</issue><spage>2992</spage><pages>2992-</pages><issn>1422-0067</issn><issn>1661-6596</issn><eissn>1422-0067</eissn><abstract>Xylan is one of the major structural components of the plant cell wall. Xylan present in the human diet reaches the large intestine undigested and becomes a substrate to species of the gut microbiota. Here, we characterised the capacity of
and
strains to utilise xylan derivatives. We showed that
ATCC 53608 and
ATCC 27340 produced β-D-xylosidases, enabling growth on xylooligosaccharide (XOS). The recombinant enzymes were highly active on artificial (
-nitrophenyl β-D-xylopyranoside) and natural (xylobiose, xylotriose, and xylotetraose) substrates, and showed transxylosylation activity and tolerance to xylose inhibition. The enzymes belong to glycoside hydrolase family 120 with Asp as nucleophile and Glu as proton donor, as shown by homology modelling and confirmed by site-directed mutagenesis. In silico analysis revealed that these enzymes were part of a gene cluster in
but not in
strains, and quantitative proteomics identified other enzymes and transporters involved in
XOS utilisation. Based on these findings, we proposed a model for an XOS metabolism pathway in
and
strains. Together with phylogenetic analyses, the data also revealed the extended xylanolytic potential of the gut microbiota.</abstract><cop>Switzerland</cop><pub>MDPI AG</pub><pmid>35328413</pmid><doi>10.3390/ijms23062992</doi><orcidid>https://orcid.org/0000-0002-2472-9328</orcidid><orcidid>https://orcid.org/0000-0001-7889-7688</orcidid><orcidid>https://orcid.org/0000-0001-8515-1315</orcidid><orcidid>https://orcid.org/0000-0001-9796-4612</orcidid><orcidid>https://orcid.org/0000-0001-8574-0275</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | International journal of molecular sciences, 2022-03, Vol.23 (6), p.2992 |
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| source | MDPI - Multidisciplinary Digital Publishing Institute; MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central |
| subjects | Bacteria Bacteria - genetics Bacteria - metabolism Cell walls Digestive system Enzymes Genes Genomes Glucuronates Glycosidases Glycoside hydrolase Gram-positive bacteria Homology Humans Hydrolase Intestinal microflora Intestine Large intestine Microbiota Oligosaccharides Phylogeny Proteomics Site-directed mutagenesis Strains (organisms) Substrate Specificity Xylan Xylans - metabolism Xylopyranoside Xylosidases - metabolism |
| title | Biochemical Basis of Xylooligosaccharide Utilisation by Gut Bacteria |
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