A novel membrane-spanning one-component system controls β-glucan utilization in marine Bacteroidota

One of the most prevalent and bioavailable glycans in marine systems is the {beta}-glucan laminarin. Members of the phylum Bacteroidota are particularly well adapted to degrade this and other polysaccharides. Although recent research has provided detailed insights into the enzymatic breakdown of marine glycans by this phylum, the regulatory mechanisms that govern their utilization remain largely unexplored. Here, we describe a novel membrane-spanning one-component system that regulates laminarin utilization in marine Bacteroidota. We analyzed this {beta}-glucan utilization regulator (BguR) type in the marine model bacterium Formosa agariphila KMM3901T. Deletion of the regulator gene abolishes growth on laminarin, whereas the wild type exhibits more than 80-fold induction of the associated genomic gene cluster, indicating the regulators role as a transcriptional activator for laminarin utilization. Structural predictions show that its periplasmic sensor domain resembles those of hybrid two-component systems (HTCSs), although the absence of phosphorylation domains and distinct architecture indicate a completely different, ATP-independent mode-of-action. Comparative genomics show that this regulator is widespread among Bacteroidota, exhibiting lineage-specific distribution patterns similar to hallmark features such as tandem SusCD-like pairs. BguR is frequently found in close proximity to {beta}-glucan-targeting PULs in the genome, implying a defined substrate preference that extends beyond laminarin. These findings suggest a novel regulatory mechanism for glycan sensing in marine bacteria, shedding light on an important facet of the marine carbon cycle.