Mechanisms of recalcitrant fucoidan breakdown in marine Planctomycetota

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 () and Laura Alonso-Sáez ()
Additional contact information
Carla Pérez-Cruz: Basque Research and Technology Alliance (BRTA)
Alicia Moraleda-Montoya: Biobizkaia Health Research Institute
Raquel Liébana: Basque Research and Technology Alliance (BRTA)
Oihana Terrones: University of the Basque Country
Uxue Arrizabalaga: Basque Research and Technology Alliance (BRTA)
Mikel García-Alija: Biobizkaia Health Research Institute
Maier Lorizate: University of the Basque Country
Ana Martínez Gascueña: Biobizkaia Health Research Institute
Isabel García-Álvarez: Pozuelo de Alarcón
Jon Ander Nieto-Garai: University of the Basque Country
June Olazar-Intxausti: University of the Basque Country
Bárbara Rodríguez-Colinas: Pozuelo de Alarcón
Enrique Mann: Instituto de Química Orgánica General (IQOG-CSIC)
José Luis Chiara: Instituto de Química Orgánica General (IQOG-CSIC)
Francesc-Xabier Contreras: University of the Basque Country
Marcelo E. Guerin: Spanish National Research Council (CSIC)
Beatriz Trastoy: Biobizkaia Health Research Institute
Laura Alonso-Sáez: Basque Research and Technology Alliance (BRTA)

Nature Communications, 2024, vol. 15, issue 1, 1-24

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-55268-w

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