Molecular basis of an agarose metabolic pathway acquired by a human intestinal symbiont

Citation

Pluvinage, B., Grondin, J.M., Amundsen, C., Klassen, L., Moote, P.E., Xiao, Y., Thomas, D., Pudlo, N.A., Anele, A., Martens, E.C., Inglis, G.D., Uwiera, R.E.R., Boraston, A.B., Abbott, D.W. (2018). Molecular basis of an agarose metabolic pathway acquired by a human intestinal symbiont. Nature Communications, [online] 9(1), http://dx.doi.org/10.1038/s41467-018-03366-x

Plain language summary

Seaweeds have been consumed by humans since antiquity. Recently, it has become known that specialized bacteria that colonize the intestines of humans can digest the polysaccharides found in the cell walls of seaweeds. This is interesting because the carbohydrates and the chemical linkages that connect them in the cell walls of seaweed are very different from those seen in land plants. In this study, we have described the molecular basis of how agarose, a prominent polysaccharide in red seaweed, in digested. The pathway involves four major enzymes that work together to release single sugars from agarose.The growing evident that bacteria possess enzymes capable of catalyzing the digestion of seaweed polysaccharides underpin that the intestinal microbiome of animals is highly dynamic and can adapt to the metabolism of rare polysaccharides included in the diet. These principles are important for animal agriculture because they suggest that alternative feedstuffs, such as seaweed, may represent energy sources for livestock.

Abstract

In red algae, the most abundant principal cell wall polysaccharides are mixed galactan agars, of which agarose is a common component. While bioconversion of agarose is predominantly catalyzed by bacteria that live in the oceans, agarases have been discovered in microorganisms that inhabit diverse terrestrial ecosystems, including human intestines. Here we comprehensively define the structure-function relationship of the agarolytic pathway from the human intestinal bacterium Bacteroides uniformis (Bu) NP1. Using recombinant agarases from Bu NP1 to completely depolymerize agarose, we demonstrate that a non-agarolytic Bu strain can grow on GAL released from agarose. This relationship underscores that rare nutrient utilization by intestinal bacteria is facilitated by the acquisition of highly specific enzymes that unlock inaccessible carbohydrate resources contained within unusual polysaccharides. Intriguingly, the agarolytic pathway is differentially distributed throughout geographically distinct human microbiomes, reflecting a complex historical context for agarose consumption by human beings.

Publication date

2018-12-01

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