Thiosocius teredinicola gen. nov., sp. nov., a sulfur-oxidizing chemolithoautotrophic endosymbiont cultivated from the gills of the giant shipworm, Kuphus polythalamius
A chemolithoautotrophic sulfur-oxidizing, diazotrophic, facultatively heterotrophic, endosymbiotic bacterium, designated as strain 2141T, was isolated from the gills of the giant shipworm Kuphus polythalamius (Teredinidae: Bivalvia). Based on its 16S rRNA sequence, the endosymbiont falls within a clade that includes the as-yet-uncultivated thioautotrophic symbionts of a marine ciliate and hydrothermal vent gastropods, uncultivated marine sediment bacteria, and a free-living sulfur-oxidizing bacterium ODIII6, all of which belong to the Gammaproteobacteria. The endosymbiont is Gram-negative, rod-shaped and has a single polar flagellum when grown in culture. This bacterium can be grown chemolithoautotrophically on a chemically defined medium supplemented with either hydrogen sulfide, thiosulfate, tetrathionate or elemental sulfur. The closed-circular genome has a DNA G+C content of 60.1 mol% and is 4.79 Mbp in size with a large nitrogenase cluster spanning nearly 40 kbp. The diazotrophic capability was confirmed by growing the strain on chemolithoautotrophic thiosulfate-based medium without a combined source of fixed nitrogen. The bacterium is also capable of heterotrophic growth on organic acids such as acetate and propionate. The pH, temperature and salinity optima for chemolithoautotrophic growth on thiosulfate were found to be 8.5, 34 °C and 0.2 M NaCl, respectively. To our knowledge, this is the first report of pure culture of a thioautotrophic animal symbiont. The type strain of Thiosocius teredinicola is PMS-2141T.STBD.0c.01aT (=DSM 108030T).
This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
DubilierN, BerginC, LottC. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol2008; 6:725–740 [View Article][PubMed]
HuberM. Compendium of Bivalves 2. A Full-Color Guide to the Remaining Seven Families. A Systematic Listing of 8,500 Bivalve Species and 10,500 Synonyms Hackenheim, Germany: ConchBooks; 2015
DistelDL, AminM, BurgoyneA, LintonE, MamangkeyG et al. Molecular phylogeny of Pholadoidea Lamarck, 1809 supports a single origin for xylotrophy (wood feeding) and xylotrophic bacterial endosymbiosis in Bivalvia. Mol Phylogenet Evol2011; 61:245–254 [View Article][PubMed]
WaterburyJB, CallowayCB, TurnerRD. A cellulolytic nitrogen-fixing bacterium cultured from the gland of deshayes in shipworms (bivalvia: teredinidae). Science1983; 221:1401–1403 [View Article][PubMed]
DistelDL, MorrillW, Maclaren-ToussaintN, FranksD, WaterburyJ et al.Teredinibacter turnerae gen. nov., sp. nov., a dinitrogen-fixing, cellulolytic, endosymbiotic gamma-proteobacterium isolated from the gills of wood-boring molluscs (Bivalvia: Teredinidae). Int J Syst Evol Microbiol2002; 52:2261–2269 [View Article][PubMed]
ShipwayJR, AltamiaMA, HagaT, VelásquezM, AlbanoJ et al. Observations on the Life History and Geographic Range of the Giant Chemosymbiotic Shipworm Kuphus polythalamius (Bivalvia: Teredinidae). The Biological Bulletin2018; 235: [Epub ahead of print] [View Article]
SuzukiY, KojimaS, SasakiT, SuzukiM, UtsumiT et al. Host-symbiont relationships in hydrothermal vent gastropods of the genus Alviniconcha from the Southwest Pacific. Appl Environ Microbiol2006; 72:1388–1393 [View Article][PubMed]
KueverJ, SievertSM, StevensH, BrinkhoffT, MuyzerG. Microorganisms of the oxidative and reductive part of the sulphur cycle at a shallow-water hydrothermal vent in the Aegean Sea (Milos, Greece). Cah Biol Mar2002; 43:413–416
KuwaharaH, YoshidaT, TakakiY, ShimamuraS, NishiS et al. Reduced genome of the thioautotrophic intracellular symbiont in a deep-sea clam, Calyptogena okutanii. Curr Biol2007; 17:881–886 [View Article][PubMed]
WonYJ, HallamSJ, O'MullanGD, PanIL, BuckKR et al. Environmental acquisition of thiotrophic endosymbionts by deep-sea mussels of the genus bathymodiolus. Appl Environ Microbiol2003; 69:6785–6792 [View Article][PubMed]
FloodBE, JonesDS, BaileyJV. Sedimenticola thiotaurini sp. nov., a sulfur-oxidizing bacterium isolated from salt marsh sediments, and emended descriptions of the genus Sedimenticola and Sedimenticola selenatireducens. Int J Syst Evol Microbiol2015; 65:2522–2530 [View Article][PubMed]
GorisJ, KonstantinidisKT, KlappenbachJA, CoenyeT, VandammeP et al. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol2007; 57:81–91 [View Article][PubMed]
KimM, OhHS, ParkSC, ChunJ. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol2014; 64:346–351 [View Article][PubMed]
QinQL, XieBB, ZhangXY, ChenXL, ZhouBC et al. A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol2014; 196:2210–2215 [View Article][PubMed]
Abdul-RahmanF, PetitE, BlanchardJL. The distribution of polyhedral bacterial microcompartments suggests frequent horizontal transfer and operon reassembly. J Phylogenetics Evol Biol2013; 1:1–7
KruegerDM, DubilierN, CavanaughCM. Chemoautotrophic symbiosis in the tropical clamSolemya occidentalis (Bivalvia: Protobranchia): ultrastructural and phylogenetic analysis. Mar Biol1996; 126:55–64 [View Article]
PetersenJM, KemperA, Gruber-VodickaH, CardiniU, van der GeestM et al. Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation. Nat Microbiol2016; 2:16195 [View Article][PubMed]
KleinerM, WentrupC, LottC, TeelingH, WetzelS et al. Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use. Proc Natl Acad Sci USA2012; 109:E1173E1182 [View Article][PubMed]
Thiosocius teredinicola gen. nov., sp. nov., a sulfur-oxidizing chemolithoautotrophic endosymbiont cultivated from the gills of the giant shipworm, Kuphus polythalamius