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Kuphus polythalamius (Teredinidae) is one of the world's largest, most rarely observed, and least understood bivalves. Kuphus polythalamius is also among the few shallow-water marine species and the only teredinid species determined to harbor sulfur-oxidizing chemoautotrophic (thioautotrophic) symbionts. Until the recent discovery of living specimens in the Philippines, this species was known only from calcareous hard parts, fossils, and the preserved soft tissues of a single large specimen. As a result, the anatomy, biology, life history, and geographic range of K. polythalamius remain obscure. Here we report the collection and description of the smallest living specimens of K. polythalamius yet discovered and confirm the species identity of these individuals by using sequences of three genetic markers. Unlike previously collected specimens, all of which have been reported to occur in marine sediments, these specimens were observed burrowing in wood, the same substrate utilized by all other members of the family. These observations suggest that K. polythalamius initially settles on wood and subsequently transitions into sediment, where this species may grow to enormous sizes. This discovery led us to search for and find previously unidentified and misidentified wood-boring specimens of this species within museum collections, and it allowed us to show that the recent geographic range (since 1933) of this species extends across a 3000-mile span from the Philippines to Papua New Guinea and the Solomon Islands.

Shipworms are a group of wood-boring and wood-feeding bivalves of extraordinary economic, ecological and historical importance. Known in the literature since the fourth century BC, shipworms are both destructive pests and critical providers of ecosystem services. All previously described shipworms are obligate wood-borers, completing all or part of their life cycle in wood and most are thought to use wood as a primary source of nutrition. Here, we report and describe a new anatomically and morphologically divergent species of shipworm that bores in carbonate limestone rather than in woody substrates and lacks adaptations associated with wood-boring and wood digestion. The species is highly unusual in that it bores by ingesting rock and is among the very few known freshwater rock-boring macrobioeroders. The calcareous burrow linings of this species resemble fossil borings normally associated with bivalve bioerosion of wood substrates (ichnospecies Teredolites longissimus ) in marginal and fully marine settings. The occurrence of this newly recognized shipworm in a lithic substrate has implications for teredinid phylogeny and evolution, and interpreting palaeoenvironmental conditions based on fossil bioerosion features.

The life cycle of many sessile marine invertebrates includes a dispersive planktonic larval stage whose ability to find a suitable habitat in which to settle and transform into benthic adults is crucial to maximize fitness. To facilitate this process, invertebrate larvae commonly respond to habitat-related chemical cues to guide the search for an appropriate environment. Furthermore, small-scale hydrodynamic conditions affect dispersal of chemical cues, as well as swimming behavior of invertebrate larvae and encounter with potential habitats. Shipworms within the family Teredinidae are dependent on terrestrially derived wood in order to complete their life cycle, but very little is known about the cues and processes that promote settlement. We investigated the potential for remote detection of settling substrate via waterborne chemical cues in teredinid larvae through a combination of empirical field and laboratory flume experiments. Natural populations of teredinid larvae were significantly more abundant close to wooden structures enclosed in plankton net compared to empty control nets, clearly showing that shipworm larvae can sense and respond to chemical cues associated with suitable settling substrate in the field. However, the flume experiments, using ecologically relevant flow velocities, showed that the boundary layer around experimental wooden panels was thin and that the mean flow velocity exceeded larval swimming velocity approximately 5 mm ( approximately 25 larval body lengths) from the panel surface. Therefore, we conclude that the scope for remote detection of waterborne cues is limited and that the likely explanation for the higher abundance of shipworm larvae associated with the wooden panels in the field is a response to a cue during or after attachment on, or very near, the substrate. Waterborne cues probably guide the larva in its decision to remain attached and settle, or to detach and continue swimming and drifting until the next encounter with a solid substrate.

Quantifying biodiversity is challenging when morphology is conserved in taxa with extensive geographic distributions generated in part by human activities. Shipworms, xylophagous wood-boring clams, have been dispersed throughout the world’s oceans by wooden vessels, aquaculture equipment, and in ballast water. Consequently, many species are considered cosmopolitan, with their geographic origin obscured by their extensive distribution. Several cryptic species pairs possessing different reproductive modes are known in the Teredinidae. However, the genetic, ecological, and geographic relationships within these pairs remain unexplored. Members of the Lyrodus pedicellatus complex, both long- and short-term brooders, are found on coastlines of five continents. Phylogenetic, anatomical, ecological, and geographic data were collected on shipworms extracted from test panels, fixed submerged natural wood and driftwood, from multiple locations, primarily in the Hawaiian Archipelago, a center of wooden vessel traffic since the 1400s. Phylogenetic analysis, using multiple loci of L. pedicellatus from Hawaiʻi, Europe, the Mediterranean, Japan, Florida (USA), and California (USA), revealed seven genetically distinct cryptic species comprised of short- and long-term brooders. Reproductive mode was determined to be an inherited trait within the species in this study. Herein we discuss these findings and describe a new member of this complex, Lyrodus reginae sp. nov., from Hawaiʻi. Historically, L. pedicellatus was considered a cosmopolitan species. Our integrative approach reveals a more complicated story, indicating the evolution of multiple cryptic species with different reproductive strategies.

The “wooden-steps” hypothesis [Distel DL, et al. (2000) Nature 403:725–726] proposed that large chemosynthetic mussels found at deep-sea hydrothermal vents descend from much smaller species associated with sunken wood and other organic deposits, and that the endosymbionts of these progenitors made use of hydrogen sulfide from biogenic sources (e.g., decaying wood) rather than from vent fluids. Here, we show that wood has served not only as a stepping stone between habitats but also as a bridge between heterotrophic and chemoautotrophic symbiosis for the giant mud-boring bivalve Kuphus polythalamia. This rare and enigmatic species, which achieves the greatest length of any extant bivalve, is the only described member of the wood-boring bivalve family Teredinidae (shipworms) that burrows in marine sediments rather than wood. We show that K. polythalamia harbors sulfur-oxidizing chemoautotrophic (thioautotrophic) bacteria instead of the cellulolytic symbionts that allow other shipworm species to consume wood as food. The characteristics of its symbionts, its phylogenetic position within Teredinidae, the reduction of its digestive system by comparison with other family members, and the loss of morphological features associated with wood digestion indicate that K. polythalamia is a chemoautotrophic bivalve descended from wood-feeding (xylotrophic) ancestors. This is an example inwhich a chemoautotrophic endosymbiosis arose by displacement of an ancestral heterotrophic symbiosis and a report of pure culture of a thioautotrophic endosymbiont.

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.

Wood is a major carbon input into aquatic ecosystems and is thought to decay slowly, yet surprisingly little terrestrial carbon accumulates in marine sediments. A better mechanistic understanding of how habitat conditions and decomposer communities influence wood decay processes along the river–estuary–ocean continuum can address this seeming paradox. We measured mass loss, wood element, and polymer concentrations, quantified invertebrate-induced decay, and sequenced fungal communities associated with replicate sections of Guazuma branch wood submerged in freshwater, estuarine, and near-shore marine habitats and placed on the soil surface in nearby terrestrial habitats in three watersheds in the tropical eastern Pacific. Over 15 months, we found that wood decayed at similar rates in estuarine, marine, and terrestrial sites, reflecting the combined activity of invertebrate and microbial decomposers. In contrast, in the absence of shipworms (Teredinidae), which accounted for ~40% of wood mass loss in the estuarine habitats, decay proceeded more slowly in freshwater. Over the experiment, wood element chemistry diverged among freshwater, estuarine, and marine habitats, due to differences in both nutrient losses (e.g., potassium and phosphorus) and gains (e.g., calcium and aluminum) through decay. Similarly, we observed changes in wood polymer content, with the highest losses of cellulose, hemicellulose, and lignin moieties in the marine habitat. Aquatic fungal communities were strongly dominated by ascomycetes (88–99% of taxa), compared to terrestrial communities (55% ascomycetes). Large differences in fungal diversity were also observed across habitats with threefold higher richness in terrestrial than freshwater habitats and twofold higher diversity in freshwater than estuarine/marine habitats. Divergent decay trajectories across habitats were associated with widespread order-level differences in fungal composition, with distinct communities found in freshwater, estuarine and marine habitats. However, few individual taxa that were significantly associated with mass loss were broadly distributed, suggesting a high level of functional redundancy. The rapid processing of wood entering tropical rivers by microbes and invertebrates, comparable to that on land, indicates that estuaries and coastal oceans are hotspots not just for the processing of particulate and dissolved organic carbon, but also for woody debris and for the breakdown of lignin, the most recalcitrant polymer in plant tissue.

Shipworms are marine wood-boring bivalve mollusks (family Teredinidae) that harbor a community of closely related Gammaproteobacteria as intracellular endosymbionts in their gills. These symbionts have been proposed to assist the shipworm host in cellulose digestion and have been shown to play a role in nitrogen fixation. The genome of one strain of Teredinibacter turnerae , the first shipworm symbiont to be cultivated, was sequenced, revealing potential as a rich source of polyketides and nonribosomal peptides. Bioassay-guided fractionation led to the isolation and identification of two macrodioloide polyketides belonging to the tartrolon class. Both compounds were found to possess antibacterial properties, and the major compound was found to inhibit other shipworm symbiont strains and various pathogenic bacteria. The gene cluster responsible for the synthesis of these compounds was identified and characterized, and the ketosynthase domains were analyzed phylogenetically. Reverse-transcription PCR in addition to liquid chromatography and high-resolution mass spectrometry and tandem mass spectrometry revealed the transcription of these genes and the presence of the compounds in the shipworm, suggesting that the gene cluster is expressed in vivo and that the compounds may fulfill a specific function for the shipworm host. This study reports tartrolon polyketides from a shipworm symbiont and unveils the biosynthetic gene cluster of a member of this class of compounds, which might reveal the mechanism by which these bioactive metabolites are biosynthesized.

Furfurylation is a modification technique that improves many wood properties. The wood is first impregnated with furfuryl alcohol (FA) diluted in a solvent, and afterward the impregnated wood is cured, during which time a FA derived polymer is formed within the wood cell wall and to some extent also within the cell lumina. In this study, the effect of the solvent used during the impregnation step of the process on the distribution of the FA polymer within the wood structure was investigated for Radiata pine ( Pinus radiata ). It was found that impregnation carried out using isopropanol rather than water as solvent resulted in more filled earlywood tracheid lumina, albeit this result may be confounded by a concomitant difference in weight percent gain. It was hypothesized that the degree of earlywood lumen filling affects the durability of furufrylated wood in marine settings via an effect on the hardness on the microscale as perceived by gribble ( Limnoriidae ) and by shipworm ( Teredinidae ) larvae when they settle on wood.

Wood-boring activities by various invertebrates control the availability of food and space in marine sunken wood communities. We investigated the individual stages of wood fragmentation through a 4 yr colonization experiment. We placed Japanese cedar logs on the sea bed ~2 m below the surface of Tanabe Bay, Japan. A cluster analysis showed 6 successive stages (plus 1 alternative second stage) in the development of the wood borer’s assemblage. Individuals of the bivalve families Teredinidae and Pholadidae and the isopod family Limnoriidae settled on the logs within 2 mo (Stage 1). After rapidly fragmenting the inside of the logs (Stage 2), most of the teredinids died during the first year, leaving numerous empty tunnels reinforced by calcium carbonate linings (Stage 3). Because of this reinforcement, as well as due to the fact that the tunnels never crossed each other, the resulting honeycombed structure remained stable for about 3 yr, allowing for the ongoing development of the sunken wood community. Large-scale fragmentation finally continued with the limnoriids intensively disintegrating the logs from the surface (Stage 4). As the fragmentation process drew to a close, the pholadids disappeared from the assemblage before the limnoriids (Stage 5), the latter persisting until the log had been turned entirely into small particles (Stage 6). This rapid and dynamic fragmentation process is not universal in the sea, but serves as a useful framework for comparing the wood-boring activities across various conditions. Those comparisons will help to evaluate the role of coarse woody debris in marine ecosystems.