Genetic differentiation among isolates of Teredinibacter turnerae, a widely occurring intracellular endosymbiont of shipworms

Abstract

Teredinibacter turnerae is a cultivable intracellular endosymbiont of xylotrophic (wood-feeding) bivalves of the Family Teredinidae (shipworms). Although T. turnerae has been isolated from many shipworm taxa collected in many locations, no systematic effort has been made to explore genetic diversity within this symbiont species across the taxonomic and geographic range of its hosts. The mode of symbiont transmission is unknown. Here we examine sequence diversity in fragments of six genes (16S rRNA, gyrB, sseA, recA, rpoB, and celAB) among 25 isolates of T. turnerae cultured from 13 shipworm species collected in 15 locations in the Atlantic, Pacific and Indian Oceans. While 16S rRNA sequences are nearly invariant among all examined isolates (maximum pairwise difference <0.26%) variation among examined protein coding loci is greater (mean pairwise difference 2.2-5.9%). Phylogenetic analyses based on each protein-coding locus differentiate the 25 isolates into two distinct and well-supported clades. With five exceptions, clade assignments for each isolate were supported by analysis of alleles of each of the five protein coding loci. These exceptions include (1) putative recombinant alleles of the celAB and gyrB loci in two isolates (PMS-535T.S.1b.3 and T8510), suggesting homologous recombination between members of the two clades, and (2) evidence for a putative lateral gene transfer event affecting a second locus (recA) in three isolates (T8412, T8503 and T8513). These results demonstrate that T. turnerae isolates do not represent a homogeneous global population. Instead they indicate the emergence of two lineages that, although distinct, likely experience some level of genetic exchange with each other and with other bacterial species.

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

“…DNA was isolated from bacterial cultures using the DNeasy Blood and Tissue Kit (Qiagen) following the manufacturer's directions. The 16S rRNA gene was amplified using 27 forward and 1,492 reverse primers, and sequenced with these primers plus four internal primers (Table S11) as described by Altamia et al (19).…”

“…S1A). These endosymbiont types include Teredinibacter turnerae, a cellulolytic and nitrogen-fixing gammaproteobacterium that has been isolated in pure culture from the gills of many shipworm species from around the world (16,18,19). The metabolic capabilities displayed by T. turnerae when grown in vitro suggest two potential functions for the shipworm gill endosymbionts: (i) fixing nitrogen to supplement the host's nitrogen-deficient diet of wood and (ii) producing hydrolytic enzymes that contribute to wood digestion (1,18).…”

Editorial 2015

“…), as well as studies of the stability and differentiation of microbial symbiotic communities across genetic and geographic distance (Altamia et al . ; Flot et al . ; Goffredi et al .…”

Nature's microbiome: introduction

“…In another study, Altamia et al . (this issue) estimate evolutionary divergence among Teredinibacter turnerae symbionts from wood‐feeding bivalve species in the family Teredinidae (shipworms). These bacteria occur intracellularly in the gills of the shipworms where they produce enzymes, including cellulases and nitrogenase, which may contribute to the host's ability to survive on an indigestible and nitrogen deficient diet of wood.…”