How do shipworms eat wood? A non-enzymatic, symbiont-mediated mechanism for the digestion of lignocellulose in teredinids

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Shipworms live in the ocean and are related to clams. They are some of a very few animals in the world that can eat wood. They also play an important role in nature by recycling the carbon in wood. It is estimated that between 2 - 5% of the world’s woody plant material is eaten by shipworms. The goal of this project is to understand how shipworms eat wood. Digesting wood’s complex structure isn’t easy. Scientists know that relatively large enzymes alone cannot break down wood, because wood molecules are packed too tightly together for enzymes to enter. Shipworms farm bacteria in their gills, and these bacteria have recently been found to produce very small compounds that may move into the shipworm gut where the small compounds can make powerful oxygen radicals to digest the wood. Making the oxygen radicals is proposed as the first step needed to break open the wood structure into smaller pieces. Then, in a second step, enzymes can completely digest the wood. Previously, the compounds that can make the oxygen radicals were found only in some types of fungi that also digest wood. Scientists believe that studying this shipworm chemistry may open up new knowledge about how carbon is cycled in our oceans, and may also lead to new discoveries on ways to make biofuels and renewable materials. The researchers involved in this project also believe strongly in supporting young, underrepresented female scientists and will be running educational opportunities for girls in a local town.Shipworms are the principle degraders of lignocellulose across the world’s oceans; they cause billions of dollars of damage to wooden structures (boats, piers and sea-defenses), but they also play a major role in carbon-cycling. The relative simplicity of their symbiotic communities and the unique compartmentalization of their digestive system make shipworm symbiosis a tractable counterpoint to terrestrial xylotrophs (e.g., fungi, termites). The goal of this project is to explore the unknown mechanisms of wood digestion in shipworms by examining how these animals interact with their gill endosymbionts and determining specifically whether a symbiont-mediated chemical degradation mechanism is active in the host gut. There are three approaches to reach this goal. The first approach is to determine how low molecular-weight (LMW) metabolites from shipworm gill symbionts may be activated in the host gut to generate a non-enzymatic system for lignocellulose deconstruction. This involves mapping the location of LMW metabolites in the gill and digestive system. The second approach will examine gut compartmentalization for pH environments that may promote symbiont-mediated iron reduction, redox-cycling and the generation of hydroxyl radicals associated with CMF reactions. It will also assess the spatial arrangement and compartmentalization of shipworm anatomy, and identify and map structures linking the gill endosymbionts with the digestive tract. The third approach will compare and analyze the digestive products and waste material from shipworms grown on isotopically-labelled wood. Understanding the basis of wood digestion may allow discovery of candidate catalytic/enzymatic systems and development of new strategies for bio-based materials and biofuel production.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.