Solanki, V. | Search bioRxiv

bioRxiv2024

SusC/D-like proteins in Gammaproteobacteria that utilize fructans

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.

molecular biology↗

bioRxiv2024

Polyelectrolyte mannan from diatoms reshapes sunlit ocean microbiome

Diatoms are a keystone phylum in Earths ecosystems, specializing in oxygen production and carbohydrate fixation that fuels global food webs. Diatoms host a microbiome, but how they preferentially collect bacteria with complementary traits remains unknown. Here we show that diatoms exude a C6-sulfated -1,3-mannan that serves as a selective carbon source for adapted bacteria. Its structure was resolved by NMR spectroscopy, chromatography, chemical synthesis, and enzymatic dissection. Biochemical, physiological, and structural analyses revealed that specialized Bacteroidota employ a four-enzyme pathway to metabolize this mannan. Metagenomic and transcriptomic data indicate that the mannan globally selects for bacteria carrying these enzymes and associated traits. Because the mannan provides only carbon, oxygen, sulfur, and hydrogen, bacteria must obtain other essential elements from alternative sources, reinforcing metabolic interdependence. We propose that diatoms use sulfated mannans to attract beneficial partners and exclude competitors, thereby engineering a microbiome that enhances their productivity and underpins carbon cycling. Significance statementEukaryotes host microbial partners that shape their health, yet how they selectively assemble beneficial microbes remains unclear. Using diatom microalgae as a model, we show they exude a sulfated mannan that nourishes highly adapted bacteria tracking them across the global ocean. Our findings suggest that single-celled eukaryotes can "domesticate" prokaryotes--analogous to how humans have domesticated animals--albeit on a microscopic scale. Dominating much of Earths aquatic surface, diatoms drive [~]20% of global photosynthesis. We propose that sulfated mannan contributes to this success by helping diatoms shape microbial partnerships that underpin planetary energy balance and atmospheric chemistry.

ecology↗