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Transport of symbiont-encoded cellulases from the gill to the gut of shipworms via the enigmatic ducts of Deshayes: a 174-year mystery solved.

ABSTRACT: Shipworms (Bivalvia, Teredinidae) are the principal consumers of wood in marine environments. Like most wood-eating organisms, they digest wood with the aid of cellulolytic enzymes supplied by symbiotic bacteria. However, in shipworms the symbiotic bacteria are not found in the digestive system. Instead, they are located intracellularly in the gland of Deshayes, a specialized tissue found within the gills. It has been independently demonstrated that symbiont-encoded cellulolytic enzymes are present in the digestive systems and gills of two shipworm species, Bankia setacea and Lyrodus pedicellatus, confirming that these enzymes are transported from the gills to the lumen of the gut. However, the mechanism of enzyme transport from gill to gut remains incompletely understood. Recently, a mechanism was proposed by which enzymes are transported within bacterial cells that are expelled from the gill and transported to the mouth by ciliary action of the branchial or food grooves. Here we use in situ immunohistochemical methods to provide evidence for a different mechanism in the shipworm B. setacea, in which cellulolytic enzymes are transported via the ducts of Deshayes, enigmatic structures first described 174 years ago, but whose function have remained unexplained.

SUBMITTER: Altamia MA

PROVIDER: S-EPMC9653257 | biostudies-literature | 2022 Nov

REPOSITORIES: biostudies-literature

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Transport of symbiont-encoded cellulases from the gill to the gut of shipworms via the enigmatic ducts of Deshayes: a 174-year mystery solved.

Altamia Marvin A MA Distel Daniel L DL

Proceedings. Biological sciences 20221109 1986

Shipworms (Bivalvia, Teredinidae) are the principal consumers of wood in marine environments. Like most wood-eating organisms, they digest wood with the aid of cellulolytic enzymes supplied by symbiotic bacteria. However, in shipworms the symbiotic bacteria are not found in the digestive system. Instead, they are located intracellularly in the gland of Deshayes, a specialized tissue found within the gills. It has been independently demonstrated that symbiont-encoded cellulolytic enzymes are pres ...[more]

PMID: 36350208

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Project description: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.

Project description:Bacterial symbionts are critical members of many marine sponge holobionts. Some sponge-associated bacterial lineages, such as Poribacteria, sponge-associated unclassified lineage (SAUL), and Tethybacterales, appear to have broad-host ranges and associate with a diversity of sponge species, while others are more species-specific, having adapted to the niche environment of their host. Host-associated spirochete symbionts that are numerically dominant have been documented in several invertebrates including termites, starfish, and corals. However, dominant spirochete populations are rare in marine sponges, having thus far been observed only in Clathrina clathrus and various species within the Latrunculiidae family, where they are co-dominant alongside Tethybacterales symbionts. This study aimed to characterize these spirochetes and their potential role in the host sponge. Analysis of metagenome-assembled genomes from eight latrunculid sponges revealed that these unusual spirochetes are relatively recent symbionts and are phylogenetically distinct from other sponge-associated spirochetes. Functional comparative analysis suggests that the host sponge may have selected for these spirochetes due to their ability to produce terpenoids and/or possible structural contributions.IMPORTANCESouth African latrunculid sponges are host to co-dominant Tethybacterales and Spirochete symbionts. While the Tethybacterales are broad-host range symbionts, the spirochetes have not been reported as abundant in any other marine sponge except Clathrina clathrus. However, spirochetes are regularly the most dominant populations in marine corals and terrestrial invertebrates where they are predicted to serve as beneficial symbionts. Here, we interrogated eight metagenome-assembled genomes of the latrunculid-associated spirochetes and found that these symbionts are phylogenetically distinct from all invertebrate-associated spirochetes. The symbiosis between the spirochetes and their sponge host appears to have been established relatively recently.

Dataset Information

Transport of symbiont-encoded cellulases from the gill to the gut of shipworms via the enigmatic ducts of Deshayes: a 174-year mystery solved.

Publications

Transport of symbiont-encoded cellulases from the gill to the gut of shipworms via the enigmatic ducts of Deshayes: a 174-year mystery solved.

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