Mechanisms of recalcitrant fucoidan breakdown in marine Planctomycetota
Abstract Marine brown algae produce the highly recalcitrant polysaccharide fucoidan, contributing to long-term oceanic carbon storage and climate regulation. Fucoidan is degraded by specialized heterotrophic bacteria, which promote ecosystem function and global carbon turnover using largely uncharac...
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Nature Portfolio
2024-12-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-55268-w |
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| author | Carla Pérez-Cruz Alicia Moraleda-Montoya Raquel Liébana Oihana Terrones Uxue Arrizabalaga Mikel García-Alija Maier Lorizate Ana Martínez Gascueña Isabel García-Álvarez Jon Ander Nieto-Garai June Olazar-Intxausti Bárbara Rodríguez-Colinas Enrique Mann José Luis Chiara Francesc-Xabier Contreras Marcelo E. Guerin Beatriz Trastoy Laura Alonso-Sáez |
| author_facet | Carla Pérez-Cruz Alicia Moraleda-Montoya Raquel Liébana Oihana Terrones Uxue Arrizabalaga Mikel García-Alija Maier Lorizate Ana Martínez Gascueña Isabel García-Álvarez Jon Ander Nieto-Garai June Olazar-Intxausti Bárbara Rodríguez-Colinas Enrique Mann José Luis Chiara Francesc-Xabier Contreras Marcelo E. Guerin Beatriz Trastoy Laura Alonso-Sáez |
| author_sort | Carla Pérez-Cruz |
| collection | DOAJ |
| description | Abstract Marine brown algae produce the highly recalcitrant polysaccharide fucoidan, contributing to long-term oceanic carbon storage and climate regulation. Fucoidan is degraded by specialized heterotrophic bacteria, which promote ecosystem function and global carbon turnover using largely uncharacterized mechanisms. Here, we isolate and study two Planctomycetota strains from the microbiome associated with the alga Fucus spiralis, which grow efficiently on chemically diverse fucoidans. One of the strains appears to internalize the polymer, while the other strain degrades it extracellularly. Multi-omic approaches show that fucoidan breakdown is mediated by the expression of divergent polysaccharide utilization loci, and endo-fucanases of family GH168 are strongly upregulated during fucoidan digestion. Enzymatic assays and structural biology studies reveal how GH168 endo-fucanases degrade various fucoidan cores from brown algae, assisted by auxiliary hydrolytic enzymes. Overall, our results provide insights into fucoidan processing mechanisms in macroalgal-associated bacteria. |
| format | Article |
| id | doaj-art-875b5428f31445849fa2f36ff8c7f961 |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-875b5428f31445849fa2f36ff8c7f9612025-01-05T12:35:23ZengNature PortfolioNature Communications2041-17232024-12-0115112410.1038/s41467-024-55268-wMechanisms of recalcitrant fucoidan breakdown in marine PlanctomycetotaCarla Pérez-Cruz0Alicia Moraleda-Montoya1Raquel Liébana2Oihana Terrones3Uxue Arrizabalaga4Mikel García-Alija5Maier Lorizate6Ana Martínez Gascueña7Isabel García-Álvarez8Jon Ander Nieto-Garai9June Olazar-Intxausti10Bárbara Rodríguez-Colinas11Enrique Mann12José Luis Chiara13Francesc-Xabier Contreras14Marcelo E. Guerin15Beatriz Trastoy16Laura Alonso-Sáez17AZTI, Marine Research, Basque Research and Technology Alliance (BRTA)Structural Glycoimmunology Laboratory, Biobizkaia Health Research InstituteAZTI, Marine Research, Basque Research and Technology Alliance (BRTA)Department of Biochemistry and Molecular Biology, Faculty of Science and Technology, University of the Basque CountryAZTI, Marine Research, Basque Research and Technology Alliance (BRTA)Structural Glycoimmunology Laboratory, Biobizkaia Health Research InstituteDepartment of Biochemistry and Molecular Biology, Faculty of Science and Technology, University of the Basque CountryStructural Glycoimmunology Laboratory, Biobizkaia Health Research InstituteFacultad de Ciencias Experimentales, Universidad Francisco de Vitoria, Pozuelo de AlarcónDepartment of Biochemistry and Molecular Biology, Faculty of Science and Technology, University of the Basque CountryDepartment of Biochemistry and Molecular Biology, Faculty of Science and Technology, University of the Basque CountryFacultad de Ciencias Experimentales, Universidad Francisco de Vitoria, Pozuelo de AlarcónInstituto de Química Orgánica General (IQOG-CSIC)Instituto de Química Orgánica General (IQOG-CSIC)Department of Biochemistry and Molecular Biology, Faculty of Science and Technology, University of the Basque CountryStructural Glycobiology Laboratory, Department of Structural and Molecular Biology; Molecular Biology Institute of Barcelona (IBMB), Spanish National Research Council (CSIC)Structural Glycoimmunology Laboratory, Biobizkaia Health Research InstituteAZTI, Marine Research, Basque Research and Technology Alliance (BRTA)Abstract Marine brown algae produce the highly recalcitrant polysaccharide fucoidan, contributing to long-term oceanic carbon storage and climate regulation. Fucoidan is degraded by specialized heterotrophic bacteria, which promote ecosystem function and global carbon turnover using largely uncharacterized mechanisms. Here, we isolate and study two Planctomycetota strains from the microbiome associated with the alga Fucus spiralis, which grow efficiently on chemically diverse fucoidans. One of the strains appears to internalize the polymer, while the other strain degrades it extracellularly. Multi-omic approaches show that fucoidan breakdown is mediated by the expression of divergent polysaccharide utilization loci, and endo-fucanases of family GH168 are strongly upregulated during fucoidan digestion. Enzymatic assays and structural biology studies reveal how GH168 endo-fucanases degrade various fucoidan cores from brown algae, assisted by auxiliary hydrolytic enzymes. Overall, our results provide insights into fucoidan processing mechanisms in macroalgal-associated bacteria.https://doi.org/10.1038/s41467-024-55268-w |
| spellingShingle | Carla Pérez-Cruz Alicia Moraleda-Montoya Raquel Liébana Oihana Terrones Uxue Arrizabalaga Mikel García-Alija Maier Lorizate Ana Martínez Gascueña Isabel García-Álvarez Jon Ander Nieto-Garai June Olazar-Intxausti Bárbara Rodríguez-Colinas Enrique Mann José Luis Chiara Francesc-Xabier Contreras Marcelo E. Guerin Beatriz Trastoy Laura Alonso-Sáez Mechanisms of recalcitrant fucoidan breakdown in marine Planctomycetota Nature Communications |
| title | Mechanisms of recalcitrant fucoidan breakdown in marine Planctomycetota |
| title_full | Mechanisms of recalcitrant fucoidan breakdown in marine Planctomycetota |
| title_fullStr | Mechanisms of recalcitrant fucoidan breakdown in marine Planctomycetota |
| title_full_unstemmed | Mechanisms of recalcitrant fucoidan breakdown in marine Planctomycetota |
| title_short | Mechanisms of recalcitrant fucoidan breakdown in marine Planctomycetota |
| title_sort | mechanisms of recalcitrant fucoidan breakdown in marine planctomycetota |
| url | https://doi.org/10.1038/s41467-024-55268-w |
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