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Abstract

Brown algae are important players in the global carbon cycle by fixing
carbon dioxide into 1 Gt of biomass annually, yet the fate of
fucoidan-their major cell wall polysaccharide-remains poorly understood.
Microbial degradation of fucoidans is slower than that of other
polysaccharides, suggesting that fucoidans are more recalcitrant and may
sequester carbon in the ocean. This may be due to the complex, branched
and highly sulfated structure of fucoidans, which also varies among
species of brown algae. Here, we show that 'Lentimonas' sp. CC4,
belonging to the Verrucomicrobia, acquired a remarkably complex
machinery for the degradation of six different fucoidans. The strain
accumulated 284 putative fucoidanases, including glycoside hydrolases,
sulfatases and carbohydrate esterases, which are primarily located on a
0.89-megabase pair plasmid. Proteomics reveals that these enzymes
assemble into substrate-specific pathways requiring about 100 enzymes
per fucoidan from different species of brown algae. These enzymes
depolymerize fucoidan into fucose, which is metabolized in a
proteome-costly bacterial microcompartment that spatially constrains the
metabolism of the toxic intermediate lactaldehyde. Marine metagenomes
and microbial genomes show that Verrucomicrobia including 'Lentimonas'
are abundant and highly specialized degraders of fucoidans and other
complex polysaccharides. Overall, the complexity of the pathways
underscores why fucoidans are probably recalcitrant and more slowly
degraded, since only highly specialized organisms can effectively
degrade them in the ocean.
'Lentimonas'-a marine microorganism from the Verrucomicrobia phylum-has
>200 different glycoside hydrolase and sulfatase enzymes enabling
digestion of the algal polysaccharide fucoidan, which was thought to be
a recalcitrant source of carbon in our oceans.