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Ipswich, MA, United States

Altamia M.A.,University of the Philippines at Diliman | Wood N.,Ocean Genome Legacy Inc. | Fung J.M.,Ocean Genome Legacy Inc. | Dedrick S.,Ocean Genome Legacy Inc. | And 4 more authors.
Molecular Ecology

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 geographical 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 between all examined isolates (maximum pairwise difference <0.26%), variation between 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 (i) 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 (ii) 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. © 2014 John Wiley & Sons Ltd. Source

Distel D.L.,Ocean Genome Legacy Inc. | Amin M.,University of Maine, United States | Burgoyne A.,University of Maine, United States | Linton E.,Central Michigan University | And 5 more authors.
Molecular Phylogenetics and Evolution

The ability to consume wood as food (xylotrophy) is unusual among animals. In terrestrial environments, termites and other xylotrophic insects are the principle wood consumers while in marine environments wood-boring bivalves fulfill this role. However, the evolutionary origin of wood feeding in bivalves has remained largely unexplored. Here we provide data indicating that xylotrophy has arisen just once in Bivalvia in a single wood-feeding bivalve lineage that subsequently diversified into distinct shallow- and deep-water branches, both of which have been broadly successful in colonizing the world's oceans. These data also suggest that the appearance of this remarkable life habit was approximately coincident with the acquisition of bacterial endosymbionts. Here we generate a robust phylogeny for xylotrophic bivalves and related species based on sequences of small and large subunit nuclear rRNA genes. We then trace the distribution among the modern taxa of morphological characters and character states associated with xylotrophy and xylotrepesis (wood-boring) and use a parsimony-based method to infer their ancestral states. Based on these ancestral state reconstructions we propose a set of plausible hypotheses describing the evolution of symbiotic xylotrophy in Bivalvia. Within this context, we reinterpret one of the most remarkable progressions in bivalve evolution, the transformation of the " typical" myoid body plan to create a unique lineage of worm-like, tube-forming, wood-feeding clams. The well-supported phylogeny presented here is inconsistent with most taxonomic treatments for xylotrophic bivalves, indicating that the bivalve family Pholadidae and the subfamilies Teredininae and Bankiinae of the family Teredinidae are non-monophyletic, and that the principle traits used for their taxonomic diagnosis are phylogenetically misleading. © 2011 Elsevier Inc. Source

Han A.W.,Oregon Health And Science University | Han A.W.,University of California at Berkeley | Sandy M.,University of California at Santa Barbara | Fishman B.,Oregon Health And Science University | And 5 more authors.

Shipworms are marine bivalve mollusks (Family Teredinidae) that use wood for shelter and food. They harbor a group of closely related, yet phylogenetically distinct, bacterial endosymbionts in bacteriocytes located in the gills. This endosymbiotic community is believed to support the host's nutrition in multiple ways, through the production of cellulolytic enzymes and the fixation of nitrogen. The genome of the shipworm endosymbiont Teredinibacter turnerae T7901 was recently sequenced and in addition to the potential for cellulolytic enzymes and diazotrophy, the genome also revealed a rich potential for secondary metabolites. With nine distinct biosynthetic gene clusters, nearly 7% of the genome is dedicated to secondary metabolites. Bioinformatic analyses predict that one of the gene clusters is responsible for the production of a catecholate siderophore. Here we describe this gene cluster in detail and present the siderophore product from this cluster. Genes similar to the entCEBA genes of enterobactin biosynthesis involved in the production and activation of dihydroxybenzoic acid (DHB) are present in this cluster, as well as a two-module non-ribosomal peptide synthetase (NRPS). A novel triscatecholate siderophore, turnerbactin, was isolated from the supernatant of iron-limited T. turnerae T7901 cultures. Turnerbactin is a trimer of N-(2,3-DHB)-L-Orn-L-Ser with the three monomeric units linked by Ser ester linkages. A monomer, dimer, dehydrated dimer, and dehydrated trimer of 2,3-DHB-L-Orn-L-Ser were also found in the supernatant. A link between the gene cluster and siderophore product was made by constructing a NRPS mutant, TtAH03. Siderophores could not be detected in cultures of TtAH03 by HPLC analysis and Fe-binding activity of culture supernatant was significantly reduced. Regulation of the pathway by iron is supported by identification of putative Fur box sequences and observation of increased Fe-binding activity under iron restriction. Evidence of a turnerbactin fragment was found in shipworm extracts, suggesting the production of turnerbactin in the symbiosis. © 2013 Han et al. Source

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