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Significance In animals, gut microbes are essential for digestion. Here, we show that bacteria outside the gut can also play a critical role in digestion. In shipworms, wood-eating marine bivalves, endosymbiotic bacteria are found within specialized cells in the gills. We show that these endosymbionts produce wood-degrading enzymes that are selectively transported to the shipworm’s bacteria-free gut, where wood digestion occurs. Because only selected wood-degrading enzymes are transported, the shipworm system naturally identifies those endosymbiont enzymes most relevant to lignocellulose deconstruction without interference from other microbial proteins. Thus, this work expands the known biological repertoire of bacterial endosymbionts to include digestion of food and identifies previously undescribed enzymes and enzyme combinations of potential value to biomass-based industries, such as cellulosic biofuel production. Bacteria play many important roles in animal digestive systems, including the provision of enzymes critical to digestion. Typically, complex communities of bacteria reside in the gut lumen in direct contact with the ingested materials they help to digest. Here, we demonstrate a previously undescribed digestive strategy in the wood-eating marine bivalve Bankia setacea , wherein digestive bacteria are housed in a location remote from the gut. These bivalves, commonly known as shipworms, lack a resident microbiota in the gut compartment where wood is digested but harbor endosymbiotic bacteria within specialized cells in their gills. We show that this comparatively simple bacterial community produces wood-degrading enzymes that are selectively translocated from gill to gut. These enzymes, which include just a small subset of the predicted wood-degrading enzymes encoded in the endosymbiont genomes, accumulate in the gut to the near exclusion of other endosymbiont-made proteins. This strategy of remote enzyme production provides the shipworm with a mechanism to capture liberated sugars from wood without competition from an endogenous gut microbiota. Because only those proteins required for wood digestion are translocated to the gut, this newly described system reveals which of many possible enzymes and enzyme combinations are minimally required for wood degradation. Thus, although it has historically had negative impacts on human welfare, the shipworm digestive process now has the potential to have a positive impact on industries that convert wood and other plant biomass to renewable fuels, fine chemicals, food, feeds, textiles, and paper products.

Marine bivalves of the family Teredinidae (shipworms) are voracious consumers of wood in marine environments. In several shipworm species, dense communities of intracellular bacterial endosymbionts have been observed within specialized cells (bacteriocytes) of the gills (ctenidia). These bacteria are proposed to contribute to digestion of wood by the host. While the microbes of shipworm gills have been studied extensively in several species, the abundance and distribution of microbes in the digestive system have not been adequately addressed. Here we use Fluorescence In-Situ Hybridization (FISH) and laser scanning confocal microscopy with 16S rRNA directed oligonucleotide probes targeting all domains, domains Bacteria and Archaea, and other taxonomic groups to examine the digestive microbiota of 17 specimens from 5 shipworm species (Bankia setacea, Lyrodus pedicellatus, Lyrodus massa, Lyrodus sp. and Teredo aff. triangularis). These data reveal that the caecum, a large sac-like appendage of the stomach that typically contains large quantities of wood particles and is considered the primary site of wood digestion, harbors only very sparse microbial populations. However, a significant number of bacterial cells were observed in fecal pellets within the intestines. These results suggest that due to low abundance, bacteria in the caecum may contribute little to lignocellulose degradation. In contrast, the comparatively high population density of bacteria in the intestine suggests a possible role for intestinal bacteria in the degradation of lignocellulose.

Marine wood-borers and burrowers can substantially alter habitats and human-created structures in the marine environment. While many marine borers and burrowers occur only in a few substrata, burrowing sphaeromatid isopods can damage a variety of substrata. On the Pacific coast of North America, burrowing by the non-native isopod, Sphaeroma quoianum, accelerates shoreline erosion and damages marine structures. We conducted a lab experiment to quantify the per capita burrowing effect of S. quoianum on four common estuarine substrata. After two months, isopods created longer and more voluminous burrows and removed the most material (per capita) in marsh banks and Styrofoam followed by sandstone and non-decayed wood. We also examined the burrow morphology (length, diameter, volume) of burrows of S. quoianum from those four substrata collected in the field. We observed longer and more voluminous burrows in marsh bank and Styrofoam substrata, although we only detected a significant difference in length between substrata. Based on our lab results, we estimate a population of 100 000 adult isopods burrowing for two months could remove approximately 176 liters of marsh bank, 103 1 of Styrofoam, 72 1 of sandstone, or 29 1 of non-decayed wood. While the per capita bioerosion effects are lower than some bioeroders, e.g., the shipworm Bankia setacea, the pholad Penitella penita, high densities and wide distributions of S. quoianum suggest it is a substantial bioeroder within the intertidal and shallow subtidal in temperate Coos Bay, Oregon, and perhaps the other estuaries it has invaded.

Studies were performed at the Port of Everett, Washington, and the associated Snohomish River Estuary, to establish settlement patterns of veliger of the shipworm, Bankia setecea. Estuarine waters at the Port of Tacoma also were sampled for shipworm activity. Veliger settlement patterns at the Port of Everett indicated settlement took place all year, with major activity during August-October. This also was a period of reduced Snohomish River flow; therefore, logs stored in the estuary during 1989 at 1.9-3.0 km up river from the river's mouth were attacked by B. setacea as the salinity of these log-storage sites increased. In contrast, major movement of veligers at the Port of Tacoma was in early summer; high water temperatures were thought to prevent midsummer settlement. The upper side of wooden samplers were significantly more infested by shipworms than the under side. Veliger settlement increased evenly with depth down to the mudline discontinuity. Veligers attacked fresh wooden samplers at a significantly higher rate when these samplers were placed next to wood that had been exposed previously to shipworm attack for over 8 wk. There was proportionally less attack on fresh wooden samplers when these samplers were placed next to material exposed to attack for 4 wk; the least attack on fresh wooden samplers occurred when they were placed adjacent to unnattacked wood that had been exposed to marine water for a month (screening prevented this material from being infested). These results suggested that there were waterborne cues emanating from previously-attacked material that attracted veligers. There were significantly more B. setacea attacks on wooden samplers that were half-covered with Douglas-fir bark as compared with samplers half-covered with foam plastic. These data confirmed observations that shipworms severely attack Douglas-fir logs at sites where the bark has been peeled off, an indication that settling veliger larvae may respond to host-mediated chemical cues.