The Complete Genome of Teredinibacter turnerae T7901: An Intracellular Endosymbiont of Marine Wood-Boring Bivalves (Shipworms)

Abstract

Here we report the complete genome sequence of Teredinibacter turnerae T7901. T. turnerae is a marine gamma proteobacterium that occurs as an intracellular endosymbiont in the gills of wood-boring marine bivalves of the family Teredinidae (shipworms). This species is the sole cultivated member of an endosymbiotic consortium thought to provide the host with enzymes, including cellulases and nitrogenase, critical for digestion of wood and supplementation of the host's nitrogen-deficient diet. T. turnerae is closely related to the free-living marine polysaccharide degrading bacterium Saccharophagus degradans str. 2–40 and to as yet uncultivated endosymbionts with which it coexists in shipworm cells. Like S. degradans, the T. turnerae genome encodes a large number of enzymes predicted to be involved in complex polysaccharide degradation (>100). However, unlike S. degradans, which degrades a broad spectrum (>10 classes) of complex plant, fungal and algal polysaccharides, T. turnerae primarily encodes enzymes associated with deconstruction of terrestrial woody plant material. Also unlike S. degradans and many other eubacteria, T. turnerae dedicates a large proportion of its genome to genes predicted to function in secondary metabolism. Despite its intracellular niche, the T. turnerae genome lacks many features associated with obligate intracellular existence (e.g. reduced genome size, reduced %G+C, loss of genes of core metabolism) and displays evidence of adaptations common to free-living bacteria (e.g. defense against bacteriophage infection). These results suggest that T. turnerae is likely a facultative intracellular ensosymbiont whose niche presently includes, or recently included, free-living existence. As such, the T. turnerae genome provides insights into the range of genomic adaptations associated with intracellular endosymbiosis as well as enzymatic mechanisms relevant to the recycling of plant materials in marine environments and the production of cellulose-derived biofuels.

Genomic versatility and functional variation between two dominant heterotrophic symbionts of deep-sea Osedax worms

“…In general, large genomes are thought to be more ecologically versatile (Konstantinidis and Tiedje, 2004), which would thus be important for an environmentally acquired symbiont that has both free-living and host-associated stages. The estimated genome sizes of the Osedax symbionts, larger than free-living relatives, and similar to the facultative intracellular endosymbiont Teredinibacter turnerae of the marine shipworm bivalve (Table 1; Yang et al, 2009), indirectly suggests a possible retention of genes for both free-living and intracellular existence. Vestimentiferan tubeworms, siboglinid relatives of Osedax, are infected each generation with symbionts from the local environment in which the worm larvae settle (Nussbaumer et al, 2006).…”

“…The Candidatus Poribacteria symbiont in sponges has the genomic potential for both ferric iron and heme uptake (Siegl et al, 2010), Candidatus Endoriftia persephone, the symbiont in tubeworms, can uptake both ferrous and ferric iron (Robidart et al, 2008), whereas Teredinibacter turnerae, the symbiont of wood-feeding bivalves, appears to possess only a single hemin-based mechanism for iron uptake (Yang et al, 2009). Until additional data is available for other beneficial symbionts, it remains unknown whether multiple modes of iron acquisition are an adaptation broadly employed by symbionts.…”

“…Similarly, large genes were identified in both symbionts with homology to those that encode RTX-like toxins, which aid in membrane disruption and host cell invasion by pathogenic and symbiotic bacteria (Fullner et al, 2002;Jeong et al, 2005;Ruby et al, 2005). Both T. teridinibacter and Photorhabdus luminescens, the symbiont of entomopathogenic nematodes, possess many similar secretion systems, adhesins and toxins, suggesting a role in mediating both adverse and beneficial interactions with eukaryotes (Ffrench-Constant et al, 2000;Duchaud et al, 2003;Yang et al, 2009). The Osedax symbionts are not only suspected to infect nascent Osedax larvae, at a time when their immune system and developmental program might be more conducive to infection, but also to repeatedly infect adults, through their root tips, over time (Verna et al, 2010).…”

“…New details have emerged regarding the range of adaptations used by endosymbionts, parallels with pathogens, provisioning from symbiont to host and many ecological aspects, including transmission between host generations and the duality of negotiating between host-associated and free-living lifestages. Recent advances in molecular biology and genomics have enabled this insight for chemosynthetic symbionts, in particular, hosted by the marine oligochaete Olavius algarvensis (Woyke et al, 2006), vesicomyid clam species (Kuwahara et al, 2007;Newton et al, 2007), the siboglinid tubeworm Riftia pachyptila (Robidart et al, 2008) and the heterotrophic symbionts of wood-boring bivalves (Yang et al, 2009). …”

Molecular insight into lignocellulose digestion by a marine isopod in the absence of gut microbes

“…Both of these borers ingest wood, but they have contrasting approaches to lignocellulose digestion. Like termites, teredinid wood borers have mutualistic associations with cellulolytic microbes, thought to play a critical role in lignocellulose digestion (15,17). Similarly, terrestrial isopods appear to require gut microbes to aid in lignocelluloses digestion (18).…”