Cell-surface protein YwfG of Lactococcus lactis binds to α-1,2-linked mannose
Lactococcus lactis strains are used as starter cultures in the production of fermented dairy and vegetable foods, but the species also occurs in other niches such as plant material. Lactococcus lactis subsp. lactis G50 (G50) is a plant-derived strain and potential candidate probiotics. Western blott...
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| Veröffentlicht in: | PloS one 2023-01, Vol.18 (1), p.e0273955-e0273955 |
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| description | Lactococcus lactis strains are used as starter cultures in the production of fermented dairy and vegetable foods, but the species also occurs in other niches such as plant material. Lactococcus lactis subsp. lactis G50 (G50) is a plant-derived strain and potential candidate probiotics. Western blotting of cell-wall proteins using antibodies generated against whole G50 cells detected a 120-kDa protein. MALDI-TOF MS analysis identified it as YwfG, a Leu-Pro-any-Thr-Gly cell-wall-anchor-domain-containing protein. Based on a predicted domain structure, a recombinant YwfG variant covering the N-terminal half (aa 28-511) of YwfG (YwfG28-511) was crystallized and the crystal structure was determined. The structure consisted of an L-type lectin domain, a mucin-binding protein domain, and a mucus-binding protein repeat. Recombinant YwfG variants containing combinations of these domains (YwfG28-270, YwfG28-336, YwfG28-511, MubR4) were prepared and their interactions with monosaccharides were examined by isothermal titration calorimetry; the only interaction observed was between YwfG28-270, which contained the L-type lectin domain, and d-mannose. Among four mannobioses, α-1,2-mannobiose had the highest affinity for YwfG28-270 (dissociation constant = 34 μM). YwfG28-270 also interacted with yeast mannoproteins and yeast mannan. Soaking of the crystals of YwfG28-511 with mannose or α-1,2-mannobiose revealed that both sugars bound to the L-type lectin domain in a similar manner, although the presence of the mucin-binding protein domain and the mucus-binding protein repeat within the recombinant protein inhibited the interaction between the L-type lectin domain and mannose residues. Three of the YwfG variants (except MubR4) induced aggregation of yeast cells. Strain G50 also induced aggregation of yeast cells, which was abolished by deletion of ywfG from G50, suggesting that surface YwfG contributes to the interaction with yeast cells. These findings provide new structural and functional insights into the interaction between L. lactis and its ecological niche via binding of the cell-surface protein YwfG with mannose. |
| doi_str_mv | 10.1371/journal.pone.0273955 |
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Lactococcus lactis subsp. lactis G50 (G50) is a plant-derived strain and potential candidate probiotics. Western blotting of cell-wall proteins using antibodies generated against whole G50 cells detected a 120-kDa protein. MALDI-TOF MS analysis identified it as YwfG, a Leu-Pro-any-Thr-Gly cell-wall-anchor-domain-containing protein. Based on a predicted domain structure, a recombinant YwfG variant covering the N-terminal half (aa 28-511) of YwfG (YwfG28-511) was crystallized and the crystal structure was determined. The structure consisted of an L-type lectin domain, a mucin-binding protein domain, and a mucus-binding protein repeat. Recombinant YwfG variants containing combinations of these domains (YwfG28-270, YwfG28-336, YwfG28-511, MubR4) were prepared and their interactions with monosaccharides were examined by isothermal titration calorimetry; the only interaction observed was between YwfG28-270, which contained the L-type lectin domain, and d-mannose. Among four mannobioses, α-1,2-mannobiose had the highest affinity for YwfG28-270 (dissociation constant = 34 μM). YwfG28-270 also interacted with yeast mannoproteins and yeast mannan. Soaking of the crystals of YwfG28-511 with mannose or α-1,2-mannobiose revealed that both sugars bound to the L-type lectin domain in a similar manner, although the presence of the mucin-binding protein domain and the mucus-binding protein repeat within the recombinant protein inhibited the interaction between the L-type lectin domain and mannose residues. Three of the YwfG variants (except MubR4) induced aggregation of yeast cells. Strain G50 also induced aggregation of yeast cells, which was abolished by deletion of ywfG from G50, suggesting that surface YwfG contributes to the interaction with yeast cells. These findings provide new structural and functional insights into the interaction between L. lactis and its ecological niche via binding of the cell-surface protein YwfG with mannose.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0273955</identifier><identifier>PMID: 36602978</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Agglomeration ; Antibodies ; Bacteria ; Biology and Life Sciences ; Calorimetry ; Cell surface ; Crystal structure ; Crystallization ; Crystals ; Dissociation ; Ecological niches ; Fermentation ; Fermented milk products ; Glucose ; Gram-positive bacteria ; Lactococcus lactis ; Lactococcus lactis - genetics ; Lactococcus lactis - metabolism ; Lectins - metabolism ; Mannan ; Mannoproteins ; Mannose ; Mannose - metabolism ; Medicine and Health Sciences ; Membrane Proteins - metabolism ; Monosaccharides ; Mucin ; Mucins - metabolism ; Mucus ; Niches ; Physical Sciences ; Plants ; Probiotics ; Proteins ; Research and Analysis Methods ; Saccharomyces cerevisiae ; Starter cultures ; Structure-function relationships ; Sugar ; Titration ; Titration calorimetry ; Western blotting ; Yeast ; Yeasts</subject><ispartof>PloS one, 2023-01, Vol.18 (1), p.e0273955-e0273955</ispartof><rights>Copyright: © 2023 Tsuchiya et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>2023 Tsuchiya et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2023 Tsuchiya et al 2023 Tsuchiya et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-1ed537f8b482e96572ef683bf5e0539aefe07abf88ebf5a24d268f172300e4f73</citedby><cites>FETCH-LOGICAL-c526t-1ed537f8b482e96572ef683bf5e0539aefe07abf88ebf5a24d268f172300e4f73</cites><orcidid>0000-0002-3551-6854 ; 0000-0001-7148-8101</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/PMC9815576/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9815576/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2095,2914,23846,27903,27904,53770,53772,79347,79348</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36602978$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Balogun, Emmanuel Oluwadare</contributor><creatorcontrib>Tsuchiya, Wataru</creatorcontrib><creatorcontrib>Fujimoto, Zui</creatorcontrib><creatorcontrib>Inagaki, Noritoshi</creatorcontrib><creatorcontrib>Nakagawa, Hiroyuki</creatorcontrib><creatorcontrib>Tanaka, Miwa</creatorcontrib><creatorcontrib>Kimoto-Nira, Hiromi</creatorcontrib><creatorcontrib>Yamazaki, Toshimasa</creatorcontrib><creatorcontrib>Suzuki, Chise</creatorcontrib><title>Cell-surface protein YwfG of Lactococcus lactis binds to α-1,2-linked mannose</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Lactococcus lactis strains are used as starter cultures in the production of fermented dairy and vegetable foods, but the species also occurs in other niches such as plant material. Lactococcus lactis subsp. lactis G50 (G50) is a plant-derived strain and potential candidate probiotics. Western blotting of cell-wall proteins using antibodies generated against whole G50 cells detected a 120-kDa protein. MALDI-TOF MS analysis identified it as YwfG, a Leu-Pro-any-Thr-Gly cell-wall-anchor-domain-containing protein. Based on a predicted domain structure, a recombinant YwfG variant covering the N-terminal half (aa 28-511) of YwfG (YwfG28-511) was crystallized and the crystal structure was determined. The structure consisted of an L-type lectin domain, a mucin-binding protein domain, and a mucus-binding protein repeat. Recombinant YwfG variants containing combinations of these domains (YwfG28-270, YwfG28-336, YwfG28-511, MubR4) were prepared and their interactions with monosaccharides were examined by isothermal titration calorimetry; the only interaction observed was between YwfG28-270, which contained the L-type lectin domain, and d-mannose. Among four mannobioses, α-1,2-mannobiose had the highest affinity for YwfG28-270 (dissociation constant = 34 μM). YwfG28-270 also interacted with yeast mannoproteins and yeast mannan. Soaking of the crystals of YwfG28-511 with mannose or α-1,2-mannobiose revealed that both sugars bound to the L-type lectin domain in a similar manner, although the presence of the mucin-binding protein domain and the mucus-binding protein repeat within the recombinant protein inhibited the interaction between the L-type lectin domain and mannose residues. Three of the YwfG variants (except MubR4) induced aggregation of yeast cells. Strain G50 also induced aggregation of yeast cells, which was abolished by deletion of ywfG from G50, suggesting that surface YwfG contributes to the interaction with yeast cells. These findings provide new structural and functional insights into the interaction between L. lactis and its ecological niche via binding of the cell-surface protein YwfG with mannose.</description><subject>Agglomeration</subject><subject>Antibodies</subject><subject>Bacteria</subject><subject>Biology and Life Sciences</subject><subject>Calorimetry</subject><subject>Cell surface</subject><subject>Crystal structure</subject><subject>Crystallization</subject><subject>Crystals</subject><subject>Dissociation</subject><subject>Ecological niches</subject><subject>Fermentation</subject><subject>Fermented milk products</subject><subject>Glucose</subject><subject>Gram-positive bacteria</subject><subject>Lactococcus lactis</subject><subject>Lactococcus lactis - genetics</subject><subject>Lactococcus lactis - metabolism</subject><subject>Lectins - metabolism</subject><subject>Mannan</subject><subject>Mannoproteins</subject><subject>Mannose</subject><subject>Mannose - metabolism</subject><subject>Medicine and Health Sciences</subject><subject>Membrane Proteins - 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genetics</topic><topic>Lactococcus lactis - metabolism</topic><topic>Lectins - metabolism</topic><topic>Mannan</topic><topic>Mannoproteins</topic><topic>Mannose</topic><topic>Mannose - metabolism</topic><topic>Medicine and Health Sciences</topic><topic>Membrane Proteins - metabolism</topic><topic>Monosaccharides</topic><topic>Mucin</topic><topic>Mucins - metabolism</topic><topic>Mucus</topic><topic>Niches</topic><topic>Physical Sciences</topic><topic>Plants</topic><topic>Probiotics</topic><topic>Proteins</topic><topic>Research and Analysis Methods</topic><topic>Saccharomyces cerevisiae</topic><topic>Starter cultures</topic><topic>Structure-function relationships</topic><topic>Sugar</topic><topic>Titration</topic><topic>Titration calorimetry</topic><topic>Western blotting</topic><topic>Yeast</topic><topic>Yeasts</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Tsuchiya, Wataru</creatorcontrib><creatorcontrib>Fujimoto, Zui</creatorcontrib><creatorcontrib>Inagaki, Noritoshi</creatorcontrib><creatorcontrib>Nakagawa, Hiroyuki</creatorcontrib><creatorcontrib>Tanaka, Miwa</creatorcontrib><creatorcontrib>Kimoto-Nira, Hiromi</creatorcontrib><creatorcontrib>Yamazaki, Toshimasa</creatorcontrib><creatorcontrib>Suzuki, Chise</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>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology 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>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</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>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tsuchiya, Wataru</au><au>Fujimoto, Zui</au><au>Inagaki, Noritoshi</au><au>Nakagawa, Hiroyuki</au><au>Tanaka, Miwa</au><au>Kimoto-Nira, Hiromi</au><au>Yamazaki, Toshimasa</au><au>Suzuki, Chise</au><au>Balogun, Emmanuel Oluwadare</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cell-surface protein YwfG of Lactococcus lactis binds to α-1,2-linked mannose</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2023-01-01</date><risdate>2023</risdate><volume>18</volume><issue>1</issue><spage>e0273955</spage><epage>e0273955</epage><pages>e0273955-e0273955</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Lactococcus lactis strains are used as starter cultures in the production of fermented dairy and vegetable foods, but the species also occurs in other niches such as plant material. Lactococcus lactis subsp. lactis G50 (G50) is a plant-derived strain and potential candidate probiotics. Western blotting of cell-wall proteins using antibodies generated against whole G50 cells detected a 120-kDa protein. MALDI-TOF MS analysis identified it as YwfG, a Leu-Pro-any-Thr-Gly cell-wall-anchor-domain-containing protein. Based on a predicted domain structure, a recombinant YwfG variant covering the N-terminal half (aa 28-511) of YwfG (YwfG28-511) was crystallized and the crystal structure was determined. The structure consisted of an L-type lectin domain, a mucin-binding protein domain, and a mucus-binding protein repeat. Recombinant YwfG variants containing combinations of these domains (YwfG28-270, YwfG28-336, YwfG28-511, MubR4) were prepared and their interactions with monosaccharides were examined by isothermal titration calorimetry; the only interaction observed was between YwfG28-270, which contained the L-type lectin domain, and d-mannose. Among four mannobioses, α-1,2-mannobiose had the highest affinity for YwfG28-270 (dissociation constant = 34 μM). YwfG28-270 also interacted with yeast mannoproteins and yeast mannan. Soaking of the crystals of YwfG28-511 with mannose or α-1,2-mannobiose revealed that both sugars bound to the L-type lectin domain in a similar manner, although the presence of the mucin-binding protein domain and the mucus-binding protein repeat within the recombinant protein inhibited the interaction between the L-type lectin domain and mannose residues. Three of the YwfG variants (except MubR4) induced aggregation of yeast cells. Strain G50 also induced aggregation of yeast cells, which was abolished by deletion of ywfG from G50, suggesting that surface YwfG contributes to the interaction with yeast cells. These findings provide new structural and functional insights into the interaction between L. lactis and its ecological niche via binding of the cell-surface protein YwfG with mannose.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>36602978</pmid><doi>10.1371/journal.pone.0273955</doi><orcidid>https://orcid.org/0000-0002-3551-6854</orcidid><orcidid>https://orcid.org/0000-0001-7148-8101</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2023-01, Vol.18 (1), p.e0273955-e0273955 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_2761138051 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS); PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Agglomeration Antibodies Bacteria Biology and Life Sciences Calorimetry Cell surface Crystal structure Crystallization Crystals Dissociation Ecological niches Fermentation Fermented milk products Glucose Gram-positive bacteria Lactococcus lactis Lactococcus lactis - genetics Lactococcus lactis - metabolism Lectins - metabolism Mannan Mannoproteins Mannose Mannose - metabolism Medicine and Health Sciences Membrane Proteins - metabolism Monosaccharides Mucin Mucins - metabolism Mucus Niches Physical Sciences Plants Probiotics Proteins Research and Analysis Methods Saccharomyces cerevisiae Starter cultures Structure-function relationships Sugar Titration Titration calorimetry Western blotting Yeast Yeasts |
| title | Cell-surface protein YwfG of Lactococcus lactis binds to α-1,2-linked mannose |
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