Marine seaweeds increasingly grow into extensive algal blooms, which are detrimental to coastal ecosystems, tourism and aquaculture. However, algal biomass is also emerging as a sustainable raw material for the bioeconomy. The potential exploitation of algae is hindered by our limited knowledge of the microbial pathways—and hence the distinct biochemical functions of the enzymes involved—that convert algal polysaccharides into oligo- and monosaccharides. Understanding these processes would be essential, however, for applications such as the fermentation of algal biomass into bioethanol or other value-added compounds. Here, we describe the metabolic pathway that enables the marine flavobacterium Formosa agariphila to degrade ulvan, the main cell wall polysaccharide of bloom-forming Ulva species. The pathway involves 12 biochemically characterized carbohydrate-active enzymes, including two polysaccharide lyases, three sulfatases and seven glycoside hydrolases that sequentially break down ulvan into fermentable monosaccharides. This way, the enzymes turn a previously unexploited renewable into a valuable and ecologically sustainable bioresource.
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All data that support the findings of this study are available from the corresponding authors upon reasonable request. The protein structures are deposited in the PDB under 6HHM, 6HHN, 6HPD and 6HR5. Mass spectrometry data were deposited to the ProteomeXchange Consortium via the PRIDE partner repository64 with the dataset identifier PXD009299.
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We thank the German Research Foundation (DFG) for funding through the Research Unit FOR2406 ‘Proteogenomics of Marine Polysaccharide Utilization’ (POMPU) (by grant nos. BO 1862/17-1 to U.T.B., HE 7217/2-1 to J.-H.H. and SCHW 595/10-1 to T.S.). J.-H.H. acknowledges funding by the Emmy-Noether Program of the DFG (grant no. HE 7217/1-1). G.M. is grateful to the French National Research Agency (ANR) for its support with regards to the investment expenditure program IDEALG (grant no. ANR-10-BTBR-04) and the Blue Enzymes project (reference ANR-14-CE19-0020-01). M.-K.Z. and F.U. were supported by scholarships from the Institute of Marine Biotechnology e.V. We thank C. Leroux for mass spectrometry analyses and M. Czjzek and A. Boraston for helpful discussions. We are indebted to the local contacts for their support during X-ray data collection at the PROXIMA-1 and PROXIMA-2 beamlines (SOLEIL Synchrotron, Saint Aubin, France) and the P11 beamline (DESY, Hamburg, Germany). We thank A. Otto, S. Junker and T. Sura for help with the metabolic labeling approach and T. Hinzke for support with analyses of the proteome data. We thank F. Lesourd (Agrival, Plouenan, France) for the gift of the ‘Agrival’ ulvan sample.
The authors declare no conflict of interest.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Tables 1–11, Supplementary Figures 1–48 and Supplementary Note
Summary of all proteins covered by the metabolic labeling approach.
Summary of all proteins covered by the subproteome fractionation.
Sequence-based prediction of subcellular protein localization for ulvan PUL-encoded proteins.
Multimodular proteins of ulvan PUL.