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

Abstract

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.

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

“…The sequence most similar to ribotypes LP1 through LP4 (93.3 to 95.3%) is that reported for an uncultivated symbiont from the shipworm Bankia setacea (37). Ribotypes LP5 and LP6 were distantly related to those detected in tissue, the former showing the greatest similarity (ϳ90%) to epsilon proteobacteria, while the latter was weakly associated with alpha proteobacteria.…”

“…In these analyses, the T. turnerae sequence (identical to ribotype LP4) and ribotypes LP1, LP2, and LP3 were nested within a single clade that also included the 16S rRNA genes of an uncultivated symbiont from the shipworm B. setacea (37); an uncultivated bacterium, environmental sample BD2-13 (GenBank accession no. AB015541), from deep-sea sediments (1,521 m) in Sugura Bay, Japan (1,521 m; 34°55ЈN, 138°39ЈE) (25); and an undescribed marine heterotrophic bacterium cultivated from seawater collected along the coast of La Jolla, Calif. (SCB11, GenBank accession no.…”

“…As in most intracellular bacterial endosymbioses, the symbiont population L. pedicellatus has been presumed to be a monoculture (9,37,41). However, in a few cases, multiple intracellular endosymbiont species have been observed within a single host.…”

“…Enzymes produced by this symbiont were proposed to facilitate the digestion of wood and to provide an internal source of combined nitrogen to supplement the host's protein-deficient diet (16,41). Phylogenetic analysis, based on 16S rRNA sequences, showed T. turnerae to be a member of the gamma subdivision of the proteobacteria (9, 10).As in most intracellular bacterial endosymbioses, the symbiont population L. pedicellatus has been presumed to be a monoculture (9,37,41). However, in a few cases, multiple intracellular endosymbiont species have been observed within a single host.…”

Vertical Transmission of a Phylogenetically Complex Microbial Consortium in the Viviparous SpongeIrcinia felix

“…Vertical transmission has been documented in terrestrial insects such as ants (42) and aphids (2) as well as in marine invertebrates such as bryozoans (29) and bivalves (4,47). Since the passage of symbionts via the reproductive stages is highly selective, this process frequently leads to cospeciation between the host and symbiotic lineages, resulting in congruent phylogenetic trees (36).…”