Marine Gammaproteobacteria use SusC/D-like proteins in fructan utilization

Abstract

Fructans are ubiquitous in terrestrial ecosystems, however, these glycans are unexplored 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 Bacteroidota and were previously unknown for Gammaproteobacteria: a glycan-binding SusD-like protein and a SusC-like TonB-dependent transporter (TBDT), which work as a complex in glycan import. Proteome analyses and biochemistry results suggest that the SusC/D-like proteins of P. distincta shuttle small-sized inulin-type fructans directly into the cell, where they are degraded by a periplasmic exo-active GH32. A SusD-like protein could provide a competitive adavantage in the absence of extracelluar endo-active inulinases. Comparative genomics identified further SusC/D-like proteins 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 shows the first known exception to the paradigm that only Bacteroidota use SusC/D-like proteins. It further suggests that fructans contribute to the marine glycan pool.