β-glucan utilization in marine Bacteroidota is controlled by a membrane-spanning one-component system

ABSTRACT One of the most prevalent and bioavailable glycans in marine systems is the β-glucan laminarin. Members of the phylum Bacteroidota are particularly well adapted to degrade this and other polysaccharides. Here, we describe a membrane-spanning one-component system that regulates laminarin utilization in marine Bacteroidota . We analyzed this β-glucan utilization regulator (BguR) type in the marine model bacterium Formosa agariphila KMM3901 T . 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 regulator’s 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 β-glucan-targeting PULs in the genome, implying a defined substrate preference that extends beyond laminarin. These findings suggest a previously unrecognized regulatory mechanism for glycan sensing in marine bacteria, shedding light on an important facet of the marine carbon cycle. IMPORTANCE Although recent research has provided detailed insights into the enzymatic breakdown of algal glycans by marine bacteria, the regulatory mechanisms that govern specific carbohydrate utilization strategies remain largely unexplored. This study reveals a novel regulatory mechanism for β-glucan use by marine Bacteroidota . We identified a membrane-embedded one-component regulator that directly links sensing and utilization of laminarin, a major algal polysaccharide in the oceans. Unlike traditional two-component systems, the new regulator operates without phosphorelays. The regulator and its associated laminarin PULs are widely conserved across diverse marine bacteria and even linked to other β-glucan types, indicating a shared regulatory strategy for carbon acquisition from structurally related substrates. These findings advance our understanding of how key ocean microbes coordinate polysaccharide breakdown.