Bacterial associations in the teredo Bankia australis (Lamellibranchia: Mollusca)

Popham, J. D.; Dickson, M. R.

doi:10.1007/bf00348904

Cited by 48 publications

(34 citation statements)

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“…1D) are found in an internal region of the gill referred to as the gland of Deshayes (11)(12)(13)(14)(15). Culture-independent 16S rRNA gene analyses have shown that the gill endosymbiont community of L. pedicellatus is composed of several endosymbiont types that are closely related to the polysaccharide-degrading gammaproteobacterium Saccharophagus degradans (11,12,16,17) (Fig.…”

mentioning

confidence: 99%

Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk

O’Connor

Fung

Sharp

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

130

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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.Teredinidae | endosymbionts | symbiosis | xylotrophy | carbohydrate-active enzymes

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Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk

O’Connor

Fung

Sharp

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

130

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“…These bacteria were first observed by transmission electron microscopy in the shipworm Bankia australis (32) and were proposed to synthesize essential amino acids lacking in the shipworm's wood-based diet (31). However, the axenic cultivation of a cellulolytic, dinitrogen-fixing bacterium from the gills of several shipworm species suggests that the symbionts play a more direct role in wood feeding (41).…”

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confidence: 99%

Coexistence of Multiple Proteobacterial Endosymbionts in the Gills of the Wood-Boring Bivalve Lyrodus pedicellatus (Bivalvia: Teredinidae)

Distel

Beaudoin

Morrill

2002

Appl Environ Microbiol

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Wood-boring bivalves of the family Teredinidae (commonly called shipworms) are known to harbor dense populations of gram-negative bacteria within specialized cells (bacteriocytes) in their gills. These symbionts are thought to provide enzymes, e.g., cellulase and dinitrogenase, which assist the host in utilizing wood as a primary food source. A cellulolytic, dinitrogen-fixing bacterium, Teredinibacter turnerae, has been isolated from the gill tissues of numerous teredinid bivalves and has been proposed to constitute the sole or predominant symbiont of this bivalve family. Here we demonstrate that one teredinid species, Lyrodus pedicellatus, contains at least four distinct bacterial 16S rRNA types within its gill bacteriocytes, one of which is identical to that of T. turnerae. Phylogenetic analyses indicate that the three newly detected ribotypes are derived from gamma proteobacteria that are related to but distinct (>6.5% sequence divergence) from T. turnerae. In situ hybridizations with 16S rRNA-directed probes demonstrated that the pattern of occurrence of symbiont ribotypes within bacteriocytes was predictable and specific, with some bacteriocytes containing two symbiont ribotypes. However, only two of the six possible pairwise combinations of the four ribotypes were observed to cooccur within the same host cells. The results presented here are consistent with the existence of a complex multiple symbiosis in this shipworm species.Lyrodus pedicellatus is a member of the family Teredinidae, a group of worm-like marine bivalves that burrow into and consume floating or submerged wood with the aid of endosymbiotic bacteria. Adult specimens range from a few millimeters to more than 2 m in length and up to several centimeters in diameter. These bivalves, commonly called shipworms, cause severe damage to ships, piers, fishing equipment, and other wooden structures worldwide. Shipworms also play an important ecological role as the principle agents of mineralization of cellulosic plant materials in shallow (Ͻ150 m) marine and brackish environments (6). Wooden substrates serve as both food and shelter for shipworms, which are the only marine animals known to be capable of normal growth and reproduction with wood as a sole food source (14).The mechanism by which shipworms digest wood is thought to involve gram-negative bacterial endosymbionts found within the gills. These bacteria were first observed by transmission electron microscopy in the shipworm Bankia australis (32) and were proposed to synthesize essential amino acids lacking in the shipworm's wood-based diet (31). However, the axenic cultivation of a cellulolytic, dinitrogen-fixing bacterium from the gills of several shipworm species suggests that the symbionts play a more direct role in wood feeding (41). This symbiotic bacterium, recently named Teredinibacter turnerae (10), was shown to reside within specialized epithelial cells (bacteriocytes) in the shipworm L. pedicellatus (9) in a gill region previously referred to as the Gland of Deshayes (36). Enzymes pr...

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“…Electron microscopy has localized the symbionts to the Gland of Deshayes, a specialized region of the host gill corresponding to the interlamellar junction of the right and left demibranches (7,25,28,32). Unlike symbioses of bivalves with chemoautotrophic bacteria, in the shipworm associations the symbionts can be cultured separately from the host.…”

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confidence: 99%

Bacterial Symbiont Transmission in the Wood-Boring Shipworm Bankia setacea (Bivalvia: Teredinidae)

Sipe

Wilbur

Cary

2000

Appl Environ Microbiol

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The Teredinidae (shipworms) are a morphologically diverse group of marine wood-boring bivalves that are responsible each year for millions of dollars of damage to wooden structures in estuarine and marine habitats worldwide. They exist in a symbiosis with cellulolytic nitrogen-fixing bacteria that provide the host with the necessary enzymes for survival on a diet of wood cellulose. These symbiotic bacteria reside in distinct structures lining the interlamellar junctions of the gill. This study investigated the mode by which these nutritionally essential bacterial symbionts are acquired in the teredinid Bankia setacea. Through 16S ribosomal DNA (rDNA) sequencing, the symbiont residing within the B. setacea gill was phylogenetically characterized and shown to be distinct from previously described shipworm symbionts. In situ hybridization using symbiontspecific 16S rRNA-directed probes bound to bacterial ribosome targets located within the host gill coincident with the known location of the gill symbionts. These specific probes were then used as primers in a PCR-based assay which consistently detected bacterial rDNA in host gill (symbiont containing), gonad tissue, and recently spawned eggs, demonstrating the presence of symbiont cells in host ovary and offspring. These results suggest that B. setacea ensures successful inoculation of offspring through a vertical mode of symbiont transmission and thereby enables a broad distribution of larval settlement.

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Bacterial associations in the teredo Bankia australis (Lamellibranchia: Mollusca)

Cited by 48 publications

References 1 publication

Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk

Gill bacteria enable a novel digestive strategy in a wood-feeding mollusk

Coexistence of Multiple Proteobacterial Endosymbionts in the Gills of the Wood-Boring Bivalve Lyrodus pedicellatus (Bivalvia: Teredinidae)

Bacterial Symbiont Transmission in the Wood-Boring Shipworm Bankia setacea (Bivalvia: Teredinidae)

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