Study of the biosynthesis and functionality of polyphosphate in Bifidobacterium longum KABP042

Abstract Polyphosphate (poly-P) biosynthesis in bacteria has been linked to many physiological processes and has been characterized as an interesting functional molecule involved in intestinal homeostasis. We determined the capacity for poly-P production of 18 probiotic strains mainly belonging to B...

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Main Authors: Cristina Alcántara, Marta Perez, Pol Huedo, Tatiana Altadill, Jordi Espadaler-Mazo, Juan Luis Arqués, Manuel Zúñiga, Vicente Monedero
Format: Article
Language:English
Published: Nature Portfolio 2023-07-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-023-38082-0
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author Cristina Alcántara
Marta Perez
Pol Huedo
Tatiana Altadill
Jordi Espadaler-Mazo
Juan Luis Arqués
Manuel Zúñiga
Vicente Monedero
author_facet Cristina Alcántara
Marta Perez
Pol Huedo
Tatiana Altadill
Jordi Espadaler-Mazo
Juan Luis Arqués
Manuel Zúñiga
Vicente Monedero
author_sort Cristina Alcántara
collection DOAJ
description Abstract Polyphosphate (poly-P) biosynthesis in bacteria has been linked to many physiological processes and has been characterized as an interesting functional molecule involved in intestinal homeostasis. We determined the capacity for poly-P production of 18 probiotic strains mainly belonging to Bifidobacterium and former Lactobacillus genera, showing that poly-P synthesis varied widely between strains and is dependent on the availability of phosphate and the growth phase. Bifidobacteria were especially capable of poly-P synthesis and poly-P kinase (ppk) genes were identified in their genomes together with a repertoire of genes involved in phosphate transport and metabolism. In Bifidobacterium longum KABP042, the strain we found with highest poly-P production, variations in ppk expression were linked to growth conditions and presence of phosphate in the medium. Moreover, the strain produced poly-P in presence of breast milk and lacto-N-tetraose increased the amount of poly-P synthesized. Compared to KABP042 supernatants low in poly-P, exposure of Caco-2 cells to KABP042 supernatants rich in poly-P resulted in decreased epithelial permeability and increased barrier resistance, induction of epithelial protecting factors such as HSP27 and enhanced expression of tight junction protein genes. These results highlight the role of bifidobacteria-derived poly-P as a strain-dependent functional factor acting on epithelial integrity.
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spelling doaj.art-083205394a6741748c2d7eed2fd0fd362023-07-09T11:10:32ZengNature PortfolioScientific Reports2045-23222023-07-0113111310.1038/s41598-023-38082-0Study of the biosynthesis and functionality of polyphosphate in Bifidobacterium longum KABP042Cristina Alcántara0Marta Perez1Pol Huedo2Tatiana Altadill3Jordi Espadaler-Mazo4Juan Luis Arqués5Manuel Zúñiga6Vicente Monedero7Laboratorio de Bacterias Lácticas y Probióticos, Instituto de Agroquímica y Tecnología de Alimentos (IATA-CSIC)R&D Department, AB-Biotics S.A. (Part of Kaneka Corporation)R&D Department, AB-Biotics S.A. (Part of Kaneka Corporation)R&D Department, AB-Biotics S.A. (Part of Kaneka Corporation)R&D Department, AB-Biotics S.A. (Part of Kaneka Corporation)Departamento de Tecnología de Alimentos, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA-CSIC)Laboratorio de Bacterias Lácticas y Probióticos, Instituto de Agroquímica y Tecnología de Alimentos (IATA-CSIC)Laboratorio de Bacterias Lácticas y Probióticos, Instituto de Agroquímica y Tecnología de Alimentos (IATA-CSIC)Abstract Polyphosphate (poly-P) biosynthesis in bacteria has been linked to many physiological processes and has been characterized as an interesting functional molecule involved in intestinal homeostasis. We determined the capacity for poly-P production of 18 probiotic strains mainly belonging to Bifidobacterium and former Lactobacillus genera, showing that poly-P synthesis varied widely between strains and is dependent on the availability of phosphate and the growth phase. Bifidobacteria were especially capable of poly-P synthesis and poly-P kinase (ppk) genes were identified in their genomes together with a repertoire of genes involved in phosphate transport and metabolism. In Bifidobacterium longum KABP042, the strain we found with highest poly-P production, variations in ppk expression were linked to growth conditions and presence of phosphate in the medium. Moreover, the strain produced poly-P in presence of breast milk and lacto-N-tetraose increased the amount of poly-P synthesized. Compared to KABP042 supernatants low in poly-P, exposure of Caco-2 cells to KABP042 supernatants rich in poly-P resulted in decreased epithelial permeability and increased barrier resistance, induction of epithelial protecting factors such as HSP27 and enhanced expression of tight junction protein genes. These results highlight the role of bifidobacteria-derived poly-P as a strain-dependent functional factor acting on epithelial integrity.https://doi.org/10.1038/s41598-023-38082-0
spellingShingle Cristina Alcántara
Marta Perez
Pol Huedo
Tatiana Altadill
Jordi Espadaler-Mazo
Juan Luis Arqués
Manuel Zúñiga
Vicente Monedero
Study of the biosynthesis and functionality of polyphosphate in Bifidobacterium longum KABP042
Scientific Reports
title Study of the biosynthesis and functionality of polyphosphate in Bifidobacterium longum KABP042
title_full Study of the biosynthesis and functionality of polyphosphate in Bifidobacterium longum KABP042
title_fullStr Study of the biosynthesis and functionality of polyphosphate in Bifidobacterium longum KABP042
title_full_unstemmed Study of the biosynthesis and functionality of polyphosphate in Bifidobacterium longum KABP042
title_short Study of the biosynthesis and functionality of polyphosphate in Bifidobacterium longum KABP042
title_sort study of the biosynthesis and functionality of polyphosphate in bifidobacterium longum kabp042
url https://doi.org/10.1038/s41598-023-38082-0
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