Marine bacteroidetes use a conserved enzymatic cascade to digest diatom β-mannan

The polysaccharide beta-mannan, which is common in terrestrial plants but unknown in microalgae, was recently detected during diatom blooms. We identified a beta-mannan polysaccharide utilization locus (PUL) in the genome of the marine flavobacterium Muricauda sp. MAR_2010_75. Proteomics showed beta-mannan induced translation of 22 proteins encoded within the PUL. Biochemical and structural analyses deduced the enzymatic cascade for beta-mannan utilization. A conserved GH26 beta-mannanase with endo-activity depolymerized the beta-mannan. Consistent with the biochemistry, X-ray crystallography showed the typical TIM-barrel fold of related enzymes found in terrestrial beta-mannan degraders. Structural and biochemical analyses of a second GH26 allowed the prediction of an exo-activity on shorter manno-gluco oligosaccharides. Further analysis demonstrated exo-alpha-1,6-galactosidase- and endo-beta-1,4-glucanase activity of the PUL-encoded GH27 and GH5_26, respectively, indicating the target substrate is a galactoglucomannan. Epitope deletion assays with mannanases as analytic tools indicate the presence of beta-mannan in the diatoms Coscinodiscus wailesii and Chaetoceros affinis. Mannanases from the PUL were active on diatom beta-mannan and polysaccharide extracts sampled during a microalgal bloom at the North Sea. Together these results demonstrate that marine microorganisms use a conserved enzymatic cascade to degrade beta-mannans of marine and terrestrial origin and that this metabolic pathway plays a role in marine carbon cycling.

Automated summary

The presence of beta-mannan in diatom blooms suggests that marine microorganisms have a conserved enzymatic cascade for degrading beta-mannans from marine and terrestrial sources, highlighting the importance of this metabolic pathway in marine carbon cycling.