A methyl esterase from Bifidobacterium longum subsp. longum reshapes the prebiotic properties of apple pectin by triggering differential modulatory capacity in faecal cultures
Pectin structures have received increasing attention as emergent prebiotics due to their capacity to promote beneficial intestinal bacteria. Yet the collective activity of gut bacterial communities to cooperatively metabolize structural variants of this substrate remains largely unknown. Herein, the characterization of a pectin methylesterase, BpeM, from Bifidobacterium longum subsp. longum, is reported. The purified enzyme was able to remove methyl groups from highly methoxylated apple pectin, and the mathematical modelling of its activity enabled to tightly control the reaction conditions to achieve predefined final degrees of methyl-esterification in the resultant pectin. Demethylated pectin, generated by BpeM, exhibited differential fermentation patterns by gut microbial communities in in vitro mixed faecal cultures, promoting a stronger increase of bacterial genera associated with beneficial effects including Lactobacillus, Bifidobacterium and Collinsella. Our findings demonstrate that controlled pectin demethylation by the action of a B. longum esterase selectively modifies its prebiotic fermentation pattern, producing substrates that promote targeted bacterial groups more efficiently. This opens new possibilities to exploit biotechnological applications of enzymes from gut commensals to programme prebiotic properties.
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2024
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Pectin structures have received increasing attention as emergent prebiotics due to their capacity to promote beneficial intestinal bacteria. Yet the collective activity of gut bacterial communities to cooperatively metabolize structural variants of this substrate remains largely unknown. Herein, the characterization of a pectin methylesterase, BpeM, from Bifidobacterium longum subsp. longum, is reported. The purified enzyme was able to remove methyl groups from highly methoxylated apple pectin, and the mathematical modelling of its activity enabled to tightly control the reaction conditions to achieve predefined final degrees of methyl-esterification in the resultant pectin. Demethylated pectin, generated by BpeM, exhibited differential fermentation patterns by gut microbial communities in in vitro mixed faecal cultures, promoting a stronger increase of bacterial genera associated with beneficial effects including Lactobacillus, Bifidobacterium and Collinsella. Our findings demonstrate that controlled pectin demethylation by the action of a B. longum esterase selectively modifies its prebiotic fermentation pattern, producing substrates that promote targeted bacterial groups more efficiently. This opens new possibilities to exploit biotechnological applications of enzymes from gut commensals to programme prebiotic properties. |
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Ministerio de Ciencia, Innovación y Universidades (España) |
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Ministerio de Ciencia, Innovación y Universidades (España) Calvete-Torre, Inés Sabater, Carlos Muñoz-Almagro, Nerea Campelo, Ana B. Moreno, F. Javier Margolles Barros, Abelardo Ruíz García, Lorena |
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Calvete-Torre, Inés Sabater, Carlos Muñoz-Almagro, Nerea Campelo, Ana B. Moreno, F. Javier Margolles Barros, Abelardo Ruíz García, Lorena |
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Calvete-Torre, Inés Sabater, Carlos Muñoz-Almagro, Nerea Campelo, Ana B. Moreno, F. Javier Margolles Barros, Abelardo Ruíz García, Lorena A methyl esterase from Bifidobacterium longum subsp. longum reshapes the prebiotic properties of apple pectin by triggering differential modulatory capacity in faecal cultures |
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Calvete-Torre, Inés |
title |
A methyl esterase from Bifidobacterium longum subsp. longum reshapes the prebiotic properties of apple pectin by triggering differential modulatory capacity in faecal cultures |
title_short |
A methyl esterase from Bifidobacterium longum subsp. longum reshapes the prebiotic properties of apple pectin by triggering differential modulatory capacity in faecal cultures |
title_full |
A methyl esterase from Bifidobacterium longum subsp. longum reshapes the prebiotic properties of apple pectin by triggering differential modulatory capacity in faecal cultures |
title_fullStr |
A methyl esterase from Bifidobacterium longum subsp. longum reshapes the prebiotic properties of apple pectin by triggering differential modulatory capacity in faecal cultures |
title_full_unstemmed |
A methyl esterase from Bifidobacterium longum subsp. longum reshapes the prebiotic properties of apple pectin by triggering differential modulatory capacity in faecal cultures |
title_sort |
methyl esterase from bifidobacterium longum subsp. longum reshapes the prebiotic properties of apple pectin by triggering differential modulatory capacity in faecal cultures |
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Wiley-VCH |
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2024 |
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http://hdl.handle.net/10261/364565 |
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dig-cial-es-10261-3645652024-07-29T10:38:11Z A methyl esterase from Bifidobacterium longum subsp. longum reshapes the prebiotic properties of apple pectin by triggering differential modulatory capacity in faecal cultures Calvete-Torre, Inés Sabater, Carlos Muñoz-Almagro, Nerea Campelo, Ana B. Moreno, F. Javier Margolles Barros, Abelardo Ruíz García, Lorena Ministerio de Ciencia, Innovación y Universidades (España) Ministerio de Ciencia e Innovación (España) European Commission Agencia Estatal de Investigación (España) Fundación para el Fomento en Asturias de la Investigación Científica Aplicada y la Tecnología Principado de Asturias Ministerio de Economía y Competitividad (España) Pectin structures have received increasing attention as emergent prebiotics due to their capacity to promote beneficial intestinal bacteria. Yet the collective activity of gut bacterial communities to cooperatively metabolize structural variants of this substrate remains largely unknown. Herein, the characterization of a pectin methylesterase, BpeM, from Bifidobacterium longum subsp. longum, is reported. The purified enzyme was able to remove methyl groups from highly methoxylated apple pectin, and the mathematical modelling of its activity enabled to tightly control the reaction conditions to achieve predefined final degrees of methyl-esterification in the resultant pectin. Demethylated pectin, generated by BpeM, exhibited differential fermentation patterns by gut microbial communities in in vitro mixed faecal cultures, promoting a stronger increase of bacterial genera associated with beneficial effects including Lactobacillus, Bifidobacterium and Collinsella. Our findings demonstrate that controlled pectin demethylation by the action of a B. longum esterase selectively modifies its prebiotic fermentation pattern, producing substrates that promote targeted bacterial groups more efficiently. This opens new possibilities to exploit biotechnological applications of enzymes from gut commensals to programme prebiotic properties. We thank the projects MICINNAGL2016-78311-R, RTI2018-095021-J-I00, PID2021-123862OB-100 and PID2022-141737OB-I00, funded by MCIN/AEI/ 10.13039/501100011033/ and by ERDF A way of making Europe; and AYUD-2021-50910 from the autonomic Government of Principado de Asturias (FICYT, supported by FEDER). Carlos Sabater was the recipient of a Juan de la Cierva-Formación postdoctoral contract from MICINN, the Spanish Ministry of Science and Innovation (FJC2019-042125-I). Peer reviewed 2024-07-29T10:38:11Z 2024-07-29T10:38:11Z 2024 artículo Microbial Biotechnology 17(5): e14443 (2024) http://hdl.handle.net/10261/364565 10.1111/1751-7915.14443 1751-7915 38722820 en #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/MINECO//AGL2016-78311-R info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-095021-J-I00/ES/REVALORIZACION DE SUBPRODUCTOS DE LA INDUSTRIA AGROALIMENTARIA CON CAPACIDAD PARA MODULAR POBLACIONES DE LA MICROBIOTA INTESTINAL: POTENCIALES IMPLICACIONES BIOTECNOLOGICAS/ info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-123862OB-I00/ES/APROVECHAMIENTO INTEGRAL DE SUBPRODUCTOS AGROALIMENTARIOS VEGETALES DENTRO DEL CONCEPTO DE BIORREFINERIA. PRODUCCION Y CARACTERIZACION DE PECTINA Y OTROS COMPUESTOS RELEVANTES/ info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2022-141737OB-I00/ES/UTILIZACION DE ESTERASAS DE CARBOHIDRATOS DE MICROBIOMAS INTESTINALES PARA ADAPTAR LAS PROPIEDADES FERMENTATIVAS DE PREBIOTICOS DE PRECISION/ info:eu-repo/grantAgreement/AEI//FJC2019-042125-I Publisher's version The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI 10.1111/1751-7915.14443 https://doi.org/10.1111/1751-7915.14443 Sí open application/pdf Wiley-VCH |