Fructan utilization by members of marine Gammaproteobacteria involves SusC/D-like proteins

Fructans are ubiquitous in terrestrial ecosystems, however, these glycans are underexplored in the marine environment. We have discovered that the Antarctic gammaproteobacterium Pseudoalteromonas distincta is highly adapted to the degradation of fructose-containing substrates. This is enabled by proteins encoded in several genomic regions, including a fructan polysaccharide utilization locus (PUL). In addition to a glycoside hydrolase from family 32 (GH32), the fructan PUL encodes two proteins that have been described as specific for the phylum Bacteroidota and were previously unknown for the class Gammaproteobacteria (phylum Pseudomonadota): a glycan-binding SusD-like protein and a SusC-like TonB-dependent transporter (TBDT), which work as a complex in glycan import in Bacteroidota. Proteome, biochemical, sequence, and structural analyses indicate that the SusD-like protein and SusC-like TBDT of P. distincta mediate the uptake of inulin-type fructans, followed by degradation by a periplasmic exo-active GH32. In contrast, P. distincta likely degrades levan-type fructans via an extracellular endo-acting GH32 that is not encoded in the fructan PUL. Comparative genomics identified further SusD-like proteins and SusC-like TBDTs in Gammaproteobacteria, most of which are co-encoded with GH32s, indicative of fructan PULs, and are frequently associated with the marine habitat. Our study thus suggests that SusC/D-like complexes are not exclusive to the phylum Bacteroidota. It further shows that fructans contribute to the marine glycan pool and are targeted by specialized marine communities.