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Discovery of chemoautotrophic symbiosis in the giant shipworm Kuphus polythalamia (Bivalvia: Teredinidae) extends wooden-steps theory.

ABSTRACT: The "wooden-steps" hypothesis [Distel DL, et al. (2000) Nature 403:725-726] proposed that large chemosynthetic mussels found at deep-sea hydrothermal vents descend from much smaller species associated with sunken wood and other organic deposits, and that the endosymbionts of these progenitors made use of hydrogen sulfide from biogenic sources (e.g., decaying wood) rather than from vent fluids. Here, we show that wood has served not only as a stepping stone between habitats but also as a bridge between heterotrophic and chemoautotrophic symbiosis for the giant mud-boring bivalve Kuphus polythalamia This rare and enigmatic species, which achieves the greatest length of any extant bivalve, is the only described member of the wood-boring bivalve family Teredinidae (shipworms) that burrows in marine sediments rather than wood. We show that K. polythalamia harbors sulfur-oxidizing chemoautotrophic (thioautotrophic) bacteria instead of the cellulolytic symbionts that allow other shipworm species to consume wood as food. The characteristics of its symbionts, its phylogenetic position within Teredinidae, the reduction of its digestive system by comparison with other family members, and the loss of morphological features associated with wood digestion indicate that K. polythalamia is a chemoautotrophic bivalve descended from wood-feeding (xylotrophic) ancestors. This is an example in which a chemoautotrophic endosymbiosis arose by displacement of an ancestral heterotrophic symbiosis and a report of pure culture of a thioautotrophic endosymbiont.

SUBMITTER: Distel DL

PROVIDER: S-EPMC5422788 | biostudies-literature | 2017 May

REPOSITORIES: biostudies-literature

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Discovery of chemoautotrophic symbiosis in the giant shipworm <i>Kuphus polythalamia</i> (Bivalvia: Teredinidae) extends wooden-steps theory.

Distel Daniel L DL Altamia Marvin A MA Lin Zhenjian Z Shipway J Reuben JR Han Andrew A Forteza Imelda I Antemano Rowena R Limbaco Ma Gwen J Peñaflor MGJP Tebo Alison G AG Dechavez Rande R Albano Julie J Rosenberg Gary G Concepcion Gisela P GP Schmidt Eric W EW Haygood Margo G MG

Proceedings of the National Academy of Sciences of the United States of America 20170417 18

The "wooden-steps" hypothesis [Distel DL, et al. (2000) <i>Nature</i> 403:725-726] proposed that large chemosynthetic mussels found at deep-sea hydrothermal vents descend from much smaller species associated with sunken wood and other organic deposits, and that the endosymbionts of these progenitors made use of hydrogen sulfide from biogenic sources (e.g., decaying wood) rather than from vent fluids. Here, we show that wood has served not only as a stepping stone between habitats but also as a b ...[more]

PMID: 28416684

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Project description:Purpose: we here adress the gene regulation of G.rosea in response to plant signals in the switch from asymbiotic to presymbiotic growth. Methods: -Strigolactone response: Spores of G.rosea were treated with GR24 (a synthetic strigolactone analog) and collected at 2 days after treatment. Control conditions: spores treated with solvent (M medium acetone 0.1%. Assay and control were performed in triplicates. -Root exsudate response: a cellophane membrane allowing molecule exchanges was deposited on in vitro Daucus carotta roots. Spores were spotted on this membrane and collected 10 days later. Control conditions: spores were spotted on cellophane membrane directly deposited on solid M medium. Assay and control were performed in triplicates. -Fungal gene expression were analyzed on mRNA were sequenced by Illumina HiSeq. sequencing Reads were firstly used in the de novo assembly of Gigaspora rosea Non Redundent Virtual Transcript and then mapped on the assembled transcriptome using CLC genomics workbench. Results: while GR24 triggered the regulation of only few genes which includes 32 genes upregulated (fold chang >2; FDR<0,05, experiment difference>10) and 61 downregulated (fold change < -2; FDR<0,05,experiment difference>10) genes, root exudates regulated several times more genes. A total of 390 genes were up-regulated by root exudates and 442 genes were down-regulated. Moreover, a majority of the genes (23 of 32 upregulated and 25 of 61 downregulated genes) regulated by GR24 were also regulated by root exudates. This is in consistant with the fact that strigolactones secreted from plant root are already characterized as a group of plant signals during AM symbiosis. The result that a large part of genes were differentialy expressed in reponse to root exudates but not GR24 suggested the presence of other plant signals than strigolactones. Conclusions: as a key player during the switch from asymbiotic to presymbiotic growth of G.rosea, plant root secreted signals - including but not limited to striglactones - significantly modified the expression of many G.rosea genes. The genes differentially expressed are mainly involved in oxidation-redution and metabolic processes that might contribute to prepare G.rosea for the following steps of symbiotic association with the host plant.

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Dataset Information

Discovery of chemoautotrophic symbiosis in the giant shipworm Kuphus polythalamia (Bivalvia: Teredinidae) extends wooden-steps theory.

Publications

Discovery of chemoautotrophic symbiosis in the giant shipworm <i>Kuphus polythalamia</i> (Bivalvia: Teredinidae) extends wooden-steps theory.

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