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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.

Teredinibacter turnerae is a cultivable cellulolytic Gammaproteobacterium (Cellvibrionaceae) that commonly occurs as an intracellular endosymbiont in the gills of wood‐eating bivalves of the family Teredinidae (shipworms). The genome of T. turnerae encodes a broad range of enzymes that deconstruct cellulose, hemicellulose and pectin and contribute to wood (lignocellulose) digestion in the shipworm gut. However, the mechanisms by which T. turnerae secretes lignocellulolytic enzymes are incompletely understood. Here, we show that T. turnerae cultures grown on carboxymethyl cellulose (CMC) produce membrane vesicles (MVs) that include a variety of proteins identified by liquid chromatography–mass spectrometry (LC–MS/MS) as carbohydrate‐active enzymes (CAZymes) with predicted activities against cellulose, hemicellulose and pectin. Reducing sugar assays and zymography confirm that these MVs exhibit cellulolytic activity, as evidenced by the hydrolysis of CMC. Additionally, these MVs were enriched with TonB‐dependent receptors, which are essential to carbohydrate and iron acquisition by free‐living bacteria. These observations indicate a potential role for MVs in lignocellulose utilisation by T. turnerae in the free‐living state, suggest possible mechanisms for host–symbiont interaction and may be informative for commercial applications such as enzyme production and lignocellulosic biomass conversion. When grown in pure culture, Teredinibacter turnerae secretes membrane vesicles (MVs) enriched in carbohydrate‐active enzymes (CAZymes) predicted to be involved in lignocellulose degradation. Activity assays confirm that these MVs retain the ability to hydrolyse cellulose. These findings indicate a potential role for MVs in lignocellulose utilisation and have implications for both symbiosis mechanisms and industrial applications such as enzyme production and biomass conversion.

We define a system in which the major symbionts that are important to host biology and to the production of secondary metabolites can be cultivated. We show that symbiotic bacteria that are critical to host nutrition and lifestyle also have an immense capacity to produce a multitude of diverse and likely novel bioactive secondary metabolites that could lead to the discovery of drugs and that these pathways are found within shipworm gills. We propose that, by shaping associated microbial communities within the host, the compounds support the ability of shipworms to degrade wood in marine environments. Because these symbionts can be cultivated and genetically manipulated, they provide a powerful model for understanding how secondary metabolism impacts microbial symbiosis. Shipworms play critical roles in recycling wood in the sea. Symbiotic bacteria supply enzymes that the organisms need for nutrition and wood degradation. Some of these bacteria have been grown in pure culture and have the capacity to make many secondary metabolites. However, little is known about whether such secondary metabolite pathways are represented in the symbiont communities within their hosts. In addition, little has been reported about the patterns of host-symbiont co-occurrence. Here, we collected shipworms from the United States, the Philippines, and Brazil and cultivated symbiotic bacteria from their gills. We analyzed sequences from 22 shipworm gill metagenomes from seven shipworm species and from 23 cultivated symbiont isolates. Using (meta)genome sequencing, we demonstrate that the cultivated isolates represent all the major bacterial symbiont species and strains in shipworm gills. We show that the bacterial symbionts are distributed among shipworm hosts in consistent, predictable patterns. The symbiotic bacteria harbor many gene cluster families (GCFs) for biosynthesis of bioactive secondary metabolites, only <5% of which match previously described biosynthetic pathways. Because we were able to cultivate the symbionts and to sequence their genomes, we can definitively enumerate the biosynthetic pathways in these symbiont communities, showing that ∼150 of ∼200 total biosynthetic gene clusters (BGCs) present in the animal gill metagenomes are represented in our culture collection. Shipworm symbionts occur in suites that differ predictably across a wide taxonomic and geographic range of host species and collectively constitute an immense resource for the discovery of new biosynthetic pathways corresponding to bioactive secondary metabolites. IMPORTANCE We define a system in which the major symbionts that are important to host biology and to the production of secondary metabolites can be cultivated. We show that symbiotic bacteria that are critical to host nutrition and lifestyle also have an immense capacity to produce a multitude of diverse and likely novel bioactive secondary metabolites that could lead to the discovery of drugs and that these pathways are found within shipworm gills. We propose that, by shaping associated microbial communities within the host, the compounds support the ability of shipworms to degrade wood in marine environments. Because these symbionts can be cultivated and genetically manipulated, they provide a powerful model for understanding how secondary metabolism impacts microbial symbiosis.

Here we describe an anatomically divergent wood-boring bivalve belonging to the family Teredinidae. Specimens were collected off the coast of Mabini, Batangas, Philippines, in February 2018, from sunken driftwood at a depth of less than 2 m. A combination of characteristics differentiates these specimens from members of previously named teredinid genera and species. Most notable among these include: an enlarged cephalic hood which extends across the posterior slope of the shell valves and integrates into the posterior adductor muscle; a unique structure, which we term the ‘cephalic collar’, formed by protruding folds of the mantle immediately ventral to the foot and extending past the posterior margin of the valves; a large globular stomach located entirely posterior to the posterior adductor muscle and extending substantially beyond the posterior gape of the valves; an elongate crystalline style and style sac extending from the base of the foot, past the posterior adductor muscle, to the posteriorly located stomach; calcareous pallets distinct from those of described genera; a prominently flared mantle collar which extends midway along the stalk of the pallets; and, separated siphons that bear a pigmented pinstripe pattern with highly elaborate compound papillae on the incurrent siphon aperture. We used Micro-Computed Tomography (Micro-CT) to build a virtual 3D anatomical model of this organism, confirming the spatial arrangement of the structures described above. Phylogenetic analysis of the small (18S) and large (28S) nuclear rRNA gene sequences, place this bivalve within the Teredindae on a branch well differentiated from previously named genera and species. We propose the new genus and species Tamilokus mabinia to accommodate these organisms, raising the total number of genera in this economically and environmentally important family to 17. This study demonstrates the efficacy of Micro-CT for anatomical description of a systematically challenging group of bivalves whose highly derived body plans are differentiated predominantly by soft tissue adaptations rather than features of calcareous hard-parts.

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 “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.

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.

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.