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

Abstract

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...

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

“…A probe broadly targeting the domain bacteria (21) (EUB338 ; Table S11) was labeled at the 5′ end with Alexa Fluor 594. Tissues were fixed in 4% (wt/vol) paraformaldehyde in seawater, embedded in paraffin, and sectioned as previously described (12). Optimal hybridization conditions were predicted using the mathFISH program (mathfish.cee.wisc.…”

“…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.…”

Nitrogen fixation in a chemoautotrophic lucinid symbiosis

“…Prokaryotic nitrogen fixers are associated with a diversity of eukaryotic hosts in a wide range of habitats, including the well-studied Rhizobium and Bradyrhizobium genera that form root-nodule symbioses with legumes 17 and the actinomycetal Frankia species associated with woody plants 18 . In marine environments, symbiotic nitrogen-fixers are known to be associated with a variety of invertebrates, such as wood-boring bivalves (shipworms) 19 , corals, sponges and sea urchins 20 .…”

Predominance of Trichoderma and Penicillium in cellulolytic aerobic filamentous fungi from subtropical and tropical forests in China, and their use in finding highly efficient β-glucosidase

“…However, natural cellulose is difficult to be degraded to glucose owing to its structure and the fact that it is often found in combination with lignin and hemicellulose [3]. Cellulose degradation and utilization are part of the global carbon cycle, with the major degradation power of cellulose in nature derived from cellulases produced by microorganisms [4][5][6][7].…”