Two binding proteins of the ABC transporter that confers growth of Bifidobacterium animalis subsp. lactis ATCC27673 on β‐mannan possess distinct manno‐oligosaccharide‐binding profiles
Summary Human gut bifidobacteria rely on ATP‐binding cassette (ABC) transporters for oligosaccharide uptake. Multiple oligosaccharide‐specific solute‐binding protein (SBP) genes are occasionally associated with a single ABC transporter, but the significance of this multiplicity remains unclear. Here...
Gespeichert in:
| Veröffentlicht in: | Molecular microbiology 2019-07, Vol.112 (1), p.114-130 |
|---|---|
| Hauptverfasser: | , , , , , , , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | 130 |
|---|---|
| container_issue | 1 |
| container_start_page | 114 |
| container_title | Molecular microbiology |
| container_volume | 112 |
| creator | Ejby, M. Guskov, A. Pichler, M. J. Zanten, G. C. Schoof, E. Saburi, W. Slotboom, D. J. Abou Hachem, M. |
| description | Summary
Human gut bifidobacteria rely on ATP‐binding cassette (ABC) transporters for oligosaccharide uptake. Multiple oligosaccharide‐specific solute‐binding protein (SBP) genes are occasionally associated with a single ABC transporter, but the significance of this multiplicity remains unclear. Here, we characterize BlMnBP1 and BlMnBP2, the two SBPs associated to the β‐manno‐oligosaccharide (MnOS) ABC transporter in Bifidobacterium animalis subsp. lactis. Despite similar overall specificity and preference to mannotriose (Kd≈80 nM), affinity of BlMnBP1 is up to 2570‐fold higher for disaccharides than BlMnBP2. Structural analysis revealed a substitution of an asparagine that recognizes the mannosyl at position 2 in BlMnBP1, by a glycine in BlMnBP2, which affects substrate affinity. Both substitution types occur in bifidobacterial SBPs, but BlMnBP1‐like variants prevail in human gut isolates. B. animalis subsp. lactis ATCC27673 showed growth on gluco and galactomannans and was able to outcompete a mannan‐degrading Bacteroides ovatus strain in co‐cultures, attesting the efficiency of this ABC uptake system. By contrast, a strain that lacks this transporter failed to grow on mannan. This study highlights SBP diversification as a possible strategy to modulate oligosaccharide uptake preferences of bifidobacterial ABC‐transporters during adaptation to specific ecological niches. Efficient metabolism of galactomannan by distinct bifidobacteria, merits evaluating this plant glycan as a potential prebiotic.
This study is describes the molecular basis of the competitive growth of a Bifidobacterium on β‐mannans. The efficient growth is mediated by secreted mannanase and a single ABC uptake system with two associated capture proteins that display overlapping manno‐oligosaccharide specificities. The structures, biochemical properties and phylogenetics of the transport proteins that support competition on preferred substrates is presented. |
| doi_str_mv | 10.1111/mmi.14257 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2204685019</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2204685019</sourcerecordid><originalsourceid>FETCH-LOGICAL-c3887-e6e6f42740dd677d06b20cafce4a0e36dfba0adbab5429fe66bd7a159badc3cf3</originalsourceid><addsrcrecordid>eNp1kU9u1DAUxi1ERYfCggsgS2zKIlMnTuxkOY1aqNSKzSCxi_x3xlViB79Eo-44AmfpAXoEDsFJ8DClQkh4Y_l7P33v-X0IvcnJMk_nbBjcMi-Lij9Di5yyKiuaqn6OFqSpSEbr4ssxeglwS0hOCaMv0DElTclpTRboYb0LWDqvnd_gMYbJOA84WDxtDV6dt3iKwsMY4mRi0sSEVfDWRMCbGHbTdo-eO-t0kEIlxs0DFt4NoneAYZYwLnGfKum1WrdtwRmnOHj84_7nt--D8F54PAYAA4C1g8l5NeG9HlI99G4TQCi1FdFpk5S_JrWuN_AKHVnRg3n9eJ-gz5cX6_Zjdv3pw1W7us4UrWueGWaYLQteEq0Z55owWRAlrDKlIIYybaUgQkshq7JorGFMai7yqpFCK6osPUGnB9_U-OtsYOoGB8r0vfAmzNAVBSlZXZG8Sei7f9DbMEefpktURXmZ82pPvT9QKqbfR2O7MaatxbsuJ90-1C6F2v0ONbFvHx1nORj9RP5JMQFnB2CXdnL3f6fu5ubqYPkL-XCz0w</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2253741759</pqid></control><display><type>article</type><title>Two binding proteins of the ABC transporter that confers growth of Bifidobacterium animalis subsp. lactis ATCC27673 on β‐mannan possess distinct manno‐oligosaccharide‐binding profiles</title><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>Wiley Free Content</source><source>Wiley Online Library All Journals</source><creator>Ejby, M. ; Guskov, A. ; Pichler, M. J. ; Zanten, G. C. ; Schoof, E. ; Saburi, W. ; Slotboom, D. J. ; Abou Hachem, M.</creator><creatorcontrib>Ejby, M. ; Guskov, A. ; Pichler, M. J. ; Zanten, G. C. ; Schoof, E. ; Saburi, W. ; Slotboom, D. J. ; Abou Hachem, M.</creatorcontrib><description>Summary
Human gut bifidobacteria rely on ATP‐binding cassette (ABC) transporters for oligosaccharide uptake. Multiple oligosaccharide‐specific solute‐binding protein (SBP) genes are occasionally associated with a single ABC transporter, but the significance of this multiplicity remains unclear. Here, we characterize BlMnBP1 and BlMnBP2, the two SBPs associated to the β‐manno‐oligosaccharide (MnOS) ABC transporter in Bifidobacterium animalis subsp. lactis. Despite similar overall specificity and preference to mannotriose (Kd≈80 nM), affinity of BlMnBP1 is up to 2570‐fold higher for disaccharides than BlMnBP2. Structural analysis revealed a substitution of an asparagine that recognizes the mannosyl at position 2 in BlMnBP1, by a glycine in BlMnBP2, which affects substrate affinity. Both substitution types occur in bifidobacterial SBPs, but BlMnBP1‐like variants prevail in human gut isolates. B. animalis subsp. lactis ATCC27673 showed growth on gluco and galactomannans and was able to outcompete a mannan‐degrading Bacteroides ovatus strain in co‐cultures, attesting the efficiency of this ABC uptake system. By contrast, a strain that lacks this transporter failed to grow on mannan. This study highlights SBP diversification as a possible strategy to modulate oligosaccharide uptake preferences of bifidobacterial ABC‐transporters during adaptation to specific ecological niches. Efficient metabolism of galactomannan by distinct bifidobacteria, merits evaluating this plant glycan as a potential prebiotic.
This study is describes the molecular basis of the competitive growth of a Bifidobacterium on β‐mannans. The efficient growth is mediated by secreted mannanase and a single ABC uptake system with two associated capture proteins that display overlapping manno‐oligosaccharide specificities. The structures, biochemical properties and phylogenetics of the transport proteins that support competition on preferred substrates is presented.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/mmi.14257</identifier><identifier>PMID: 30947380</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>ABC transporter ; ABC transporters ; Affinity ; Asparagine ; Bifidobacterium animalis ; Disaccharides ; Ecological niches ; Glycan ; Glycine ; Mannan ; Metabolism ; Niches ; Oligosaccharides ; Proteins ; Structural analysis ; Substitutes ; Substrate preferences ; Substrates</subject><ispartof>Molecular microbiology, 2019-07, Vol.112 (1), p.114-130</ispartof><rights>2019 John Wiley & Sons Ltd</rights><rights>2019 John Wiley & Sons Ltd.</rights><rights>Copyright © 2019 John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3887-e6e6f42740dd677d06b20cafce4a0e36dfba0adbab5429fe66bd7a159badc3cf3</citedby><cites>FETCH-LOGICAL-c3887-e6e6f42740dd677d06b20cafce4a0e36dfba0adbab5429fe66bd7a159badc3cf3</cites><orcidid>0000-0001-8250-1842 ; 0000-0003-2340-2216</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fmmi.14257$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fmmi.14257$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1416,1432,27923,27924,45573,45574,46408,46832</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30947380$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ejby, M.</creatorcontrib><creatorcontrib>Guskov, A.</creatorcontrib><creatorcontrib>Pichler, M. J.</creatorcontrib><creatorcontrib>Zanten, G. C.</creatorcontrib><creatorcontrib>Schoof, E.</creatorcontrib><creatorcontrib>Saburi, W.</creatorcontrib><creatorcontrib>Slotboom, D. J.</creatorcontrib><creatorcontrib>Abou Hachem, M.</creatorcontrib><title>Two binding proteins of the ABC transporter that confers growth of Bifidobacterium animalis subsp. lactis ATCC27673 on β‐mannan possess distinct manno‐oligosaccharide‐binding profiles</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
Human gut bifidobacteria rely on ATP‐binding cassette (ABC) transporters for oligosaccharide uptake. Multiple oligosaccharide‐specific solute‐binding protein (SBP) genes are occasionally associated with a single ABC transporter, but the significance of this multiplicity remains unclear. Here, we characterize BlMnBP1 and BlMnBP2, the two SBPs associated to the β‐manno‐oligosaccharide (MnOS) ABC transporter in Bifidobacterium animalis subsp. lactis. Despite similar overall specificity and preference to mannotriose (Kd≈80 nM), affinity of BlMnBP1 is up to 2570‐fold higher for disaccharides than BlMnBP2. Structural analysis revealed a substitution of an asparagine that recognizes the mannosyl at position 2 in BlMnBP1, by a glycine in BlMnBP2, which affects substrate affinity. Both substitution types occur in bifidobacterial SBPs, but BlMnBP1‐like variants prevail in human gut isolates. B. animalis subsp. lactis ATCC27673 showed growth on gluco and galactomannans and was able to outcompete a mannan‐degrading Bacteroides ovatus strain in co‐cultures, attesting the efficiency of this ABC uptake system. By contrast, a strain that lacks this transporter failed to grow on mannan. This study highlights SBP diversification as a possible strategy to modulate oligosaccharide uptake preferences of bifidobacterial ABC‐transporters during adaptation to specific ecological niches. Efficient metabolism of galactomannan by distinct bifidobacteria, merits evaluating this plant glycan as a potential prebiotic.
This study is describes the molecular basis of the competitive growth of a Bifidobacterium on β‐mannans. The efficient growth is mediated by secreted mannanase and a single ABC uptake system with two associated capture proteins that display overlapping manno‐oligosaccharide specificities. The structures, biochemical properties and phylogenetics of the transport proteins that support competition on preferred substrates is presented.</description><subject>ABC transporter</subject><subject>ABC transporters</subject><subject>Affinity</subject><subject>Asparagine</subject><subject>Bifidobacterium animalis</subject><subject>Disaccharides</subject><subject>Ecological niches</subject><subject>Glycan</subject><subject>Glycine</subject><subject>Mannan</subject><subject>Metabolism</subject><subject>Niches</subject><subject>Oligosaccharides</subject><subject>Proteins</subject><subject>Structural analysis</subject><subject>Substitutes</subject><subject>Substrate preferences</subject><subject>Substrates</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNp1kU9u1DAUxi1ERYfCggsgS2zKIlMnTuxkOY1aqNSKzSCxi_x3xlViB79Eo-44AmfpAXoEDsFJ8DClQkh4Y_l7P33v-X0IvcnJMk_nbBjcMi-Lij9Di5yyKiuaqn6OFqSpSEbr4ssxeglwS0hOCaMv0DElTclpTRboYb0LWDqvnd_gMYbJOA84WDxtDV6dt3iKwsMY4mRi0sSEVfDWRMCbGHbTdo-eO-t0kEIlxs0DFt4NoneAYZYwLnGfKum1WrdtwRmnOHj84_7nt--D8F54PAYAA4C1g8l5NeG9HlI99G4TQCi1FdFpk5S_JrWuN_AKHVnRg3n9eJ-gz5cX6_Zjdv3pw1W7us4UrWueGWaYLQteEq0Z55owWRAlrDKlIIYybaUgQkshq7JorGFMai7yqpFCK6osPUGnB9_U-OtsYOoGB8r0vfAmzNAVBSlZXZG8Sei7f9DbMEefpktURXmZ82pPvT9QKqbfR2O7MaatxbsuJ90-1C6F2v0ONbFvHx1nORj9RP5JMQFnB2CXdnL3f6fu5ubqYPkL-XCz0w</recordid><startdate>201907</startdate><enddate>201907</enddate><creator>Ejby, M.</creator><creator>Guskov, A.</creator><creator>Pichler, M. J.</creator><creator>Zanten, G. C.</creator><creator>Schoof, E.</creator><creator>Saburi, W.</creator><creator>Slotboom, D. J.</creator><creator>Abou Hachem, M.</creator><general>Blackwell Publishing Ltd</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-8250-1842</orcidid><orcidid>https://orcid.org/0000-0003-2340-2216</orcidid></search><sort><creationdate>201907</creationdate><title>Two binding proteins of the ABC transporter that confers growth of Bifidobacterium animalis subsp. lactis ATCC27673 on β‐mannan possess distinct manno‐oligosaccharide‐binding profiles</title><author>Ejby, M. ; Guskov, A. ; Pichler, M. J. ; Zanten, G. C. ; Schoof, E. ; Saburi, W. ; Slotboom, D. J. ; Abou Hachem, M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3887-e6e6f42740dd677d06b20cafce4a0e36dfba0adbab5429fe66bd7a159badc3cf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>ABC transporter</topic><topic>ABC transporters</topic><topic>Affinity</topic><topic>Asparagine</topic><topic>Bifidobacterium animalis</topic><topic>Disaccharides</topic><topic>Ecological niches</topic><topic>Glycan</topic><topic>Glycine</topic><topic>Mannan</topic><topic>Metabolism</topic><topic>Niches</topic><topic>Oligosaccharides</topic><topic>Proteins</topic><topic>Structural analysis</topic><topic>Substitutes</topic><topic>Substrate preferences</topic><topic>Substrates</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ejby, M.</creatorcontrib><creatorcontrib>Guskov, A.</creatorcontrib><creatorcontrib>Pichler, M. J.</creatorcontrib><creatorcontrib>Zanten, G. C.</creatorcontrib><creatorcontrib>Schoof, E.</creatorcontrib><creatorcontrib>Saburi, W.</creatorcontrib><creatorcontrib>Slotboom, D. J.</creatorcontrib><creatorcontrib>Abou Hachem, M.</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ejby, M.</au><au>Guskov, A.</au><au>Pichler, M. J.</au><au>Zanten, G. C.</au><au>Schoof, E.</au><au>Saburi, W.</au><au>Slotboom, D. J.</au><au>Abou Hachem, M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Two binding proteins of the ABC transporter that confers growth of Bifidobacterium animalis subsp. lactis ATCC27673 on β‐mannan possess distinct manno‐oligosaccharide‐binding profiles</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2019-07</date><risdate>2019</risdate><volume>112</volume><issue>1</issue><spage>114</spage><epage>130</epage><pages>114-130</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Summary
Human gut bifidobacteria rely on ATP‐binding cassette (ABC) transporters for oligosaccharide uptake. Multiple oligosaccharide‐specific solute‐binding protein (SBP) genes are occasionally associated with a single ABC transporter, but the significance of this multiplicity remains unclear. Here, we characterize BlMnBP1 and BlMnBP2, the two SBPs associated to the β‐manno‐oligosaccharide (MnOS) ABC transporter in Bifidobacterium animalis subsp. lactis. Despite similar overall specificity and preference to mannotriose (Kd≈80 nM), affinity of BlMnBP1 is up to 2570‐fold higher for disaccharides than BlMnBP2. Structural analysis revealed a substitution of an asparagine that recognizes the mannosyl at position 2 in BlMnBP1, by a glycine in BlMnBP2, which affects substrate affinity. Both substitution types occur in bifidobacterial SBPs, but BlMnBP1‐like variants prevail in human gut isolates. B. animalis subsp. lactis ATCC27673 showed growth on gluco and galactomannans and was able to outcompete a mannan‐degrading Bacteroides ovatus strain in co‐cultures, attesting the efficiency of this ABC uptake system. By contrast, a strain that lacks this transporter failed to grow on mannan. This study highlights SBP diversification as a possible strategy to modulate oligosaccharide uptake preferences of bifidobacterial ABC‐transporters during adaptation to specific ecological niches. Efficient metabolism of galactomannan by distinct bifidobacteria, merits evaluating this plant glycan as a potential prebiotic.
This study is describes the molecular basis of the competitive growth of a Bifidobacterium on β‐mannans. The efficient growth is mediated by secreted mannanase and a single ABC uptake system with two associated capture proteins that display overlapping manno‐oligosaccharide specificities. The structures, biochemical properties and phylogenetics of the transport proteins that support competition on preferred substrates is presented.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>30947380</pmid><doi>10.1111/mmi.14257</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0001-8250-1842</orcidid><orcidid>https://orcid.org/0000-0003-2340-2216</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0950-382X |
| ispartof | Molecular microbiology, 2019-07, Vol.112 (1), p.114-130 |
| issn | 0950-382X 1365-2958 |
| language | eng |
| recordid | cdi_proquest_miscellaneous_2204685019 |
| source | Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Wiley Free Content; Wiley Online Library All Journals |
| subjects | ABC transporter ABC transporters Affinity Asparagine Bifidobacterium animalis Disaccharides Ecological niches Glycan Glycine Mannan Metabolism Niches Oligosaccharides Proteins Structural analysis Substitutes Substrate preferences Substrates |
| title | Two binding proteins of the ABC transporter that confers growth of Bifidobacterium animalis subsp. lactis ATCC27673 on β‐mannan possess distinct manno‐oligosaccharide‐binding profiles |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-11T17%3A21%3A08IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Two%20binding%20proteins%20of%20the%20ABC%20transporter%20that%20confers%20growth%20of%20Bifidobacterium%20animalis%20subsp.%20lactis%20ATCC27673%20on%20%CE%B2%E2%80%90mannan%20possess%20distinct%20manno%E2%80%90oligosaccharide%E2%80%90binding%20profiles&rft.jtitle=Molecular%20microbiology&rft.au=Ejby,%20M.&rft.date=2019-07&rft.volume=112&rft.issue=1&rft.spage=114&rft.epage=130&rft.pages=114-130&rft.issn=0950-382X&rft.eissn=1365-2958&rft_id=info:doi/10.1111/mmi.14257&rft_dat=%3Cproquest_cross%3E2204685019%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2253741759&rft_id=info:pmid/30947380&rfr_iscdi=true |