Marine bacteria team up to break down one of the ocean’s toughest carbon-storing molecules

Deep in the ocean, brown algae and diatoms produce a complex carbohydrate molecule called fucoidan, which helps form the algae’s protective outer layer. The fucoidan molecule is very difficult for microbes to break down because its chemical structure may include dozens of different linkages and branching patterns that vary from one algae species to another. This resistance to decay is one reason why fucoidan matters; when microbes struggle to break it down, fucoidan can sink deep into the ocean, carrying carbon with it and potentially storing it for long periods. This could make fucoidan an important player in the ocean’s carbon cycle.For many years, scientists knew of individual bacteria that could break down pieces of fucoidan. But one fundamental question remained unanswered: Could a microbial community break it down completely, and if so, how?A new open-access study published in Nature, led by Andreas Sichert, a former MIT postdoc now at ETH Zurich, and Otto X. Cordero, associate professor of civil and environmental engineering at MIT, provides an answer.”No single bacterium can finish the job,” says Cordero. “Instead, fucoidan is degraded through teamwork. Different bacterial strains specialize in different parts of the molecule, and together, their combined efforts get the job done far more efficiently than any one organism could manage alone.”A puzzle with 453 piecesIn order to understand how fucoidan breaks down in nature, the research team enriched a fucoidan-degrading bacterial community from coastal seawater samples. What they found was staggering: more than 453 different genes, each responsible for making an enzyme that can act on fucoidan, spread across eight bacterial strains the researchers isolated. On their own, none of these strains could fully break down the molecule.But when the researchers used a new, rapid mass-spectrometry method, they were able to observe how bacteria consumed individual sugar building blocks — and a clear pattern emerged. All of that genetic complexity could be reduced to two roles. Some bacterial strains specialized in degrading fucoidan’s fucose-rich “backbone,” while others specialized in removing its side branches, which contain less-common sugars such as xylose and galactose.When strains playing both roles were combined, something noteworthy happened: degradation didn’t simply add up. Instead, it became synergistic and exceeded what the bacteria’s individual activities could predict. The more complementary the strains’ preference for sugar were, the stronger the effect became. In some cases, the paired communities came close to completely degrading the complex polysaccharide.”The breakdown of one of the ocean’s most abundant carbon pools rests on a division of labor,” says Cordero, “not between particular strains, but between functional roles.”Turning complexity into predictabilityThe most surprising result was that this division of labor made the system much more predictable than its underlying complexity indicated.The researchers developed a simple model that sorted bacterial activity into two broad categories: fucose, and the rarer sugars found in fucoidan’s side chains. They trained the model using data from small communities containing just one to three bacterial strains.The simplified model was able to predict degradation in communities containing up to seven strains, and its predictions also generalized to nine structurally different fucoidans from other kinds of algae.”A predictive understanding of a complex system need not come from characterizing each of its parts,” adds Cordero, “but from finding the right simplification.” The finding suggests that scientists may be able to predict how efficiently other complex, carbon-rich biological materials are broken down in nature, even when their exact chemistry and the enzymes involved are only partly understood.The researchers also found that bacteria with complementary capabilities often occurred together in samples taken from the natural ocean, suggesting that the division of labor observed in the laboratory may also play a role in the ocean.The consequences extend well beyond the field of microbiology. The researchers propose a concept they call “diversity-limited degradation,” in which the absence of the right combination of complementary bacterial specialists allows fucoidan to persist for longer instead of being broken down. This concept may help explain why some algal carbon stays in the ocean for extended periods, contributing to long-term carbon storage.For biotechnology, the takeaway is more straightforward. Instead of engineering a single “superbug” that can digest tough and complex biomass, a more promising approach may be to bring together teams of microbes that already specialize in complementary tasks. These teams could potentially be used to process brown algal biomass and other complex polysaccharides on a larger scale.Looking aheadThe broader promise, though, may lie in the approach, rather than the molecule. If hundreds of uncharacterized enzymes can be reduced to two measurable traits, the same strategy might work for other biopolymers whose chemistry has so far resisted description — and, more generally, for predicting what microbial communities do. “Here was a system with hundreds of enzymes acting on a molecule we still can’t fully describe, and it turned out to be far more tractable than anyone expected,” says Cordero. “What we found is that there’s a level of organization above the individual enzyme, corresponding to traits we can measure and plug into simple models that predict function from (genomic) composition. When biology looks intractable, it may be that we haven’t found the right level of description yet.”One question the work leaves open is a fundamental one. Fucoidan is abundant, and has been for a very long time, so why has no bacterium evolved to eat it whole? The researchers suggest answers on two levels: constraints within sugar metabolism itself, and evolutionary dynamics in which complementary specialists are continually regenerated rather than merged into one.”Really, this is a question about how life on Earth is organized,” says Cordero. “Why are the biochemical functions that drive the planet’s elemental cycles distributed across many organisms instead of concentrated in a few? Explaining that is, I think, one of the frontiers of the life sciences.”In addition to Cordero and Sichert, the research team included co-authors from ETH Zurich, the University of Vienna, and the Tata Institute of Fundamental Research.The work was supported by Simons Foundation through the Principles of Microbial Ecosystems (PRIME) collaboration.