in

A regulatory hydrogenase gene cluster observed in the thioautotrophic symbiont of Bathymodiolus mussel in the East Pacific Rise

  • Sogin, E. M., Leisch, N. & Dubilier, N. Chemosynthetic symbioses. Curr. Biol. 30, R1137–R1142 (2020).

    Article 
    CAS 

    Google Scholar 

  • Dubilier, N., Bergin, C. & Lott, C. Symbiotic diversity in marine animals: The art of harnessing chemosynthesis. Nat. Rev. Microbiol. 6, 725–740 (2008).

    Article 
    CAS 

    Google Scholar 

  • Barry, J. P. et al. Methane-based symbiosis in a mussel, Bathymodiolus platifrons, from cold seeps in Sagami Bay Japan. Invertebr. Biol. 121, 47–54 (2002).

    Article 

    Google Scholar 

  • Le Pennec, M., Donval, A. & Herry, A. Nutritional strategies of the hydrothermal ecosystem bivalves. Prog. Oceanogr. 24, 71–80 (1990).

    Article 
    ADS 

    Google Scholar 

  • Rau, G. H. & Hedges, J. I. Carbon-13 depletion in a hydrothermal vent mussel: Suggestion of a chemosynthetic food source. Science 203, 648–649 (1979).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Wentrup, C., Wendeberg, A., Schimak, M., Borowski, C. & Dubilier, N. Forever competent: Deep-sea bivalves are colonized by their chemosynthetic symbionts throughout their lifetime. Environ. Microbiol. 16, 3699–3713 (2014).

    Article 

    Google Scholar 

  • Dattagupta, S., Bergquist, D., Szalai, E., Macko, S. & Fisher, C. Tissue carbon, nitrogen, and sulfur stable isotope turnover in transplanted Bathymodiolus childressi mussels: Relation to growth and physiological condition. Limnol. Oceanogr. 49, 1144–1151 (2004).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Ikuta, T. et al. Heterogeneous composition of key metabolic gene clusters in a vent mussel symbiont population. ISME J. 10, 990–1001 (2016).

    Article 

    Google Scholar 

  • Takishita, K. et al. Genomic evidence that methanotrophic endosymbionts likely provide deep-sea Bathymodiolus mussels with a sterol intermediate in cholesterol biosynthesis. Genome Biol. Evol. 9, 1148–1160 (2017).

    Article 

    Google Scholar 

  • Sayavedra, L. et al. Horizontal acquisition followed by expansion and diversification of toxin-related genes in deep-sea bivalve symbionts. BioRxiv 110, 330 (2019).

    Google Scholar 

  • Ponnudurai, R. et al. Metabolic and physiological interdependencies in the Bathymodiolus azoricus symbiosis. ISME J. 11, 463–477 (2017).

    Article 
    CAS 

    Google Scholar 

  • Ponnudurai, R. et al. Genome sequence of the sulfur-oxidizing Bathymodiolus thermophilus gill endosymbiont. Stand Genom. Sci. 12, 1–9 (2017).

    Google Scholar 

  • Kiel, S. The Vent and Seep Biota: Aspects from Microbes to Ecosystems Vol. 33 (Springer Science & Business Media, 2010).

    Google Scholar 

  • Lorion, J. et al. Adaptive radiation of chemosymbiotic deep-sea mussels. Proc. R. Soc. B 280, 20131243 (2013).

    Article 

    Google Scholar 

  • Nussbaumer, A. D., Fisher, C. R. & Bright, M. Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature 441, 345–348 (2006).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Gros, O., Liberge, M., Heddi, A., Khatchadourian, C. & Felbeck, H. Detection of the free-living forms of sulfide-oxidizing gill endosymbionts in the lucinid habitat (Thalassia testudinum environment). Appl. Environ. Microbiol. 69, 6264–6267 (2003).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Won, Y.-J. et al. Environmental acquisition of thiotrophic endosymbionts by deep-sea mussels of the genus Bathymodiolus. Appl. Environ. Microbiol. 69, 6785–6792 (2003).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Laming, S. R., Gaudron, S. M. & Duperron, S. Lifecycle ecology of deep-sea chemosymbiotic mussels: A review. Front. Mar. Sci. 5, 282 (2018).

    Article 

    Google Scholar 

  • Laming, S. R., Duperron, S., Cunha, M. R. & Gaudron, S. M. Settled, symbiotic, then sexually mature: Adaptive developmental anatomy in the deep-sea, chemosymbiotic mussel Idas modiolaeformis. Mar. Biol. 161, 1319–1333 (2014).

    Article 

    Google Scholar 

  • Salerno, J. L. et al. Characterization of symbiont populations in life-history stages of mussels from chemosynthetic environments. Biol. Bull. 208, 145–155 (2005).

    Article 

    Google Scholar 

  • Wentrup, C., Wendeberg, A., Huang, J. Y., Borowski, C. & Dubilier, N. Shift from widespread symbiont infection of host tissues to specific colonization of gills in juvenile deep-sea mussels. ISME J. 7, 1244–1247 (2013).

    Article 
    CAS 

    Google Scholar 

  • Pennec, M. L. & Beninger, P. G. Ultrastructural characteristics of spermatogenesis in three species of deep-sea hydrothermal vent mytilids. Can. J. Zool. 75, 308–316 (1997).

    Article 

    Google Scholar 

  • Eckelbarger, K. & Young, C. Ultrastructure of gametogenesis in a chemosynthetic mytilid bivalve (Bathymodiolus childressi) from a bathyal, methane seep environment (northern Gulf of Mexico). Mar. Biol. 135, 635–646 (1999).

    Article 

    Google Scholar 

  • Ansorge, R. et al. Diversity matters: Deep-sea mussels harbor multiple symbiont strains. bioRxiv 99, 1039 (2019).

    Google Scholar 

  • Petersen, J. M., Wentrup, C., Verna, C., Knittel, K. & Dubilier, N. Origins and evolutionary flexibility of chemosynthetic symbionts from deep-sea animals. Biol. Bull. 223, 123–137 (2012).

    Article 
    CAS 

    Google Scholar 

  • Sayavedra, L. et al. Abundant toxin-related genes in the genomes of beneficial symbionts from deep-sea hydrothermal vent mussels. Elife 4, e07966 (2015).

    Article 

    Google Scholar 

  • Ansorge, R. et al. Functional diversity enables multiple symbiont strains to coexist in deep-sea mussels. Nat. Microbiol. 4, 2487–2497 (2019).

    Article 

    Google Scholar 

  • Petersen, J. M. et al. Hydrogen is an energy source for hydrothermal vent symbioses. Nature 476, 176–180 (2011).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Nakamura, K. & Takai, K. Theoretical constraints of physical and chemical properties of hydrothermal fluids on variations in chemolithotrophic microbial communities in seafloor hydrothermal systems. Prog. Earth Planet Sci. 1, 1–24 (2014).

    Article 
    ADS 

    Google Scholar 

  • Perez, M. & Juniper, S. K. Insights into symbiont population structure among three vestimentiferan tubeworm host species at eastern Pacific spreading centers. Appl. Environ. Microbiol. 82, 5197–5205 (2016).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Wilbanks, E. G. et al. Metagenomic methylation patterns resolve bacterial genomes of unusual size and structural complexity. ISME J. https://doi.org/10.1038/s41396-022-01242-7 (2022).

    Article 

    Google Scholar 

  • Rodriguez-Casariego, J. A., Cunning, R., Baker, A. C. & Eirin-Lopez, J. M. Symbiont shuffling induces differential DNA methylation responses to thermal stress in the coral Montastraea cavernosa. Mol. Ecol. 31, 588–602 (2022).

    Article 
    CAS 

    Google Scholar 

  • Triant, D. A. & Whitehead, A. Simultaneous extraction of high-quality RNA and DNA from small tissue samples. J. Hered. 100, 246–250 (2009).

    Article 
    CAS 

    Google Scholar 

  • Chin, C.-S. et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10, 563–569 (2013).

    Article 
    CAS 

    Google Scholar 

  • Wick, R. R. et al. Trycycler: Consensus long-read assemblies for bacterial genomes. Genome Biol. 22, 1–17 (2021).

    Article 

    Google Scholar 

  • Kolmogorov, M., Yuan, J., Lin, Y. & Pevzner, P. A. Assembly of long, error-prone reads using repeat graphs. Nat. Biotechnol. 37, 540–546 (2019).

    Article 
    CAS 

    Google Scholar 

  • Wick, R. R., Judd, L. M., Gorrie, C. L. & Holt, K. E. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput. Biol. 13, e1005595 (2017).

    Article 
    ADS 

    Google Scholar 

  • Krawczyk, P. S., Lipinski, L. & Dziembowski, A. PlasFlow: Predicting plasmid sequences in metagenomic data using genome signatures. Nucleic Acids Res. 46, e35–e35 (2018).

    Article 

    Google Scholar 

  • Mikheenko, A., Prjibelski, A., Saveliev, V., Antipov, D. & Gurevich, A. Versatile genome assembly evaluation with QUAST-LG. Bioinformatics 34, i142–i150 (2018).

    Article 
    CAS 

    Google Scholar 

  • Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: Assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).

    Article 
    CAS 

    Google Scholar 

  • Couvin, D. et al. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res. 46, W246–W251 (2018).

    Article 
    CAS 

    Google Scholar 

  • Perez, M., Angers, B., Young, C. R. & Juniper, S. K. Shining light on a deep-sea bacterial symbiont population structure with CRISPR. Microbial. Genom. https://doi.org/10.1099/mgen.0.000625 (2021).

    Article 

    Google Scholar 

  • Hyatt, D. et al. Prodigal: Prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 11, 1–11 (2010).

    Article 

    Google Scholar 

  • Nielsen, H. Protein Function Prediction 59–73 (Springer, 2017).

    Book 

    Google Scholar 

  • Krogh, A., Larsson, B., Von Heijne, G. & Sonnhammer, E. L. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 305, 567–580 (2001).

    Article 
    CAS 

    Google Scholar 

  • Lagesen, K. et al. RNAmmer: Consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35, 3100-31C08 (2007).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Chan, P. P. & Lowe, T. M. Gene Prediction 1–14 (Springer, 2019).

    Google Scholar 

  • Griffiths-Jones, S. et al. Rfam: Annotating non-coding RNAs in complete genomes. Nucleic Acids Res. 33, D121–D124 (2005).

    Article 
    CAS 

    Google Scholar 

  • Kanehisa, M., Sato, Y. & Morishima, K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J. Mol. Biol. 428, 726–731 (2016).

    Article 
    CAS 

    Google Scholar 

  • Siguier, P., Pérochon, J., Lestrade, L., Mahillon, J. & Chandler, M. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res. 34, D32–D36 (2006).

    Article 
    CAS 

    Google Scholar 

  • Bertelli, C. et al. IslandViewer 4: Expanded prediction of genomic islands for larger-scale datasets. Nucleic Acids Res. 45, W30–W35 (2017).

    Article 
    CAS 

    Google Scholar 

  • Arndt, D. et al. PHASTER: A better, faster version of the PHAST phage search tool. Nucleic Acids Res. 44, W16–W21 (2016).

    Article 
    CAS 

    Google Scholar 

  • Roeselers, G. et al. Complete genome sequence of Candidatus Ruthia magnifica. Stand Genomic Sci. 3, 163–173 (2010).

    Article 

    Google Scholar 

  • Emms, D. M. & Kelly, S. OrthoFinder: Phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 1–14 (2019).

    Article 

    Google Scholar 

  • Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).

    Article 

    Google Scholar 

  • Minh, B. Q. et al. IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534 (2020).

    Article 
    CAS 

    Google Scholar 

  • Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547 (2018).

    Article 
    CAS 

    Google Scholar 

  • Letunic, I. & Bork, P. Interactive tree of life (iTOL) v4: Recent updates and new developments. Nucleic Acids Res. 47, W256–W259 (2019).

    Article 
    CAS 

    Google Scholar 

  • Eren, A. M. et al. Community-led, integrated, reproducible multi-omics with anvi’o. Nat. Microbiol. 6, 3–6 (2021).

    Article 
    CAS 

    Google Scholar 

  • Darling, A. E., Mau, B. & Perna, N. T. progressiveMauve: Multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5, e11147 (2010).

    Article 
    ADS 

    Google Scholar 

  • Tesler, G. GRIMM: Genome rearrangements web server. Bioinformatics 18, 492–493 (2002).

    Article 
    CAS 

    Google Scholar 

  • Cabanettes, F. & Klopp, C. D-GENIES: Dot plot large genomes in an interactive, efficient and simple way. PeerJ 6, e4958 (2018).

    Article 

    Google Scholar 

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

    Article 
    CAS 

    Google Scholar 

  • Gilchrist, C. L. & Chooi, Y.-H. Clinker & clustermap. js: Automatic generation of gene cluster comparison figures. Bioinformatics 37, 2473–2475 (2021).

    Article 
    CAS 

    Google Scholar 

  • Taboada, B., Estrada, K., Ciria, R. & Merino, E. Operon-mapper: A web server for precise operon identification in bacterial and archaeal genomes. Bioinformatics 34, 4118–4120 (2018).

    Article 
    CAS 

    Google Scholar 

  • Søndergaard, D., Pedersen, C. N. & Greening, C. HydDB: A web tool for hydrogenase classification and analysis. Sci. Rep. 6, 1–8 (2016).

    Article 

    Google Scholar 

  • NCBI Genome Browser. https://www.ncbi.nlm.nih.gov/genome/browse/#!/prokaryotes/. Accessed 12 March 2022.

  • Mcmullin, E. R., Hourdez, S., Schaeffer, S. W. & Fisher, C. R. Review article phylogeny and biogeography of deep sea vestimentiferan tubeworms and their bacterial symbionts. Symbiosis. 34, 1–41 (2003).

    Google Scholar 

  • Won, Y.-J., Jones, W. J. & Vrijenhoek, R. C. Absence of cospeciation between deep-sea mytilids and their thiotrophic endosymbionts. J. Shellfish Res. 27, 129–138 (2008).

    Article 

    Google Scholar 

  • Miyazaki, J.-I., Martins, Ld. O., Fujita, Y., Matsumoto, H. & Fujiwara, Y. Evolutionary process of deep-sea Bathymodiolus mussels. PLoS ONE 5, e10363 (2010).

    Article 
    ADS 

    Google Scholar 

  • Bright, M. & Bulgheresi, S. A complex journey: Transmission of microbial symbionts. Nat. Rev. Microbiol. 8, 218–230 (2010).

    Article 
    CAS 

    Google Scholar 

  • Raggi, L., Schubotz, F., Hinrichs, K. U., Dubilier, N. & Petersen, J. M. Bacterial symbionts of Bathymodiolus mussels and Escarpia tubeworms from Chapopote, an asphalt seep in the southern Gulf of Mexico. Environ. Microbiol. 15, 1969–1987 (2013).

    Article 
    CAS 

    Google Scholar 

  • Goris, J. et al. DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int. J. Syst. Evol. Microbiol. 57, 81–91 (2007).

    Article 
    CAS 

    Google Scholar 

  • Meier-Kolthoff, J. P., Auch, A. F., Klenk, H.-P. & Göker, M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform. 14, 1–14 (2013).

    Article 

    Google Scholar 

  • Konstantinidis, K. T. & Tiedje, J. M. Genomic insights that advance the species definition for prokaryotes. Proc. Natl. Acad. Sci. 102, 2567–2572 (2005).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Ho, P.-T. et al. Geographical structure of endosymbiotic bacteria hosted by Bathymodiolus mussels at eastern Pacific hydrothermal vents. BMC Evol. Biol. 17, 1–16 (2017).

    Article 

    Google Scholar 

  • Romero Picazo, D. et al. Horizontally transmitted symbiont populations in deep-sea mussels are genetically isolated. ISME J. 13, 2954–2968 (2019).

    Article 

    Google Scholar 

  • Perez, M. & Juniper, S. K. Is the trophosome of Ridgeia piscesae monoclonal?. Symbiosis 74, 55–65 (2018).

    Article 
    CAS 

    Google Scholar 

  • Polzin, J., Arevalo, P., Nussbaumer, T., Polz, M. F. & Bright, M. Polyclonal symbiont populations in hydrothermal vent tubeworms and the environment. Proc. R. Soc. B 286, 20181281 (2019).

    Article 
    CAS 

    Google Scholar 

  • Russell, S. L. & Cavanaugh, C. M. Intrahost genetic diversity of bacterial symbionts exhibits evidence of mixed infections and recombinant haplotypes. Mol. Biol. Evol. 34, 2747–2761 (2017).

    Article 
    CAS 

    Google Scholar 

  • Breusing, C., Genetti, M., Russell, S. L., Corbett-Detig, R. B. & Beinart, R. A. Horizontal transmission enables flexible associations with locally adapted symbiont strains in deep-sea hydrothermal vent symbioses. Proc. Natl. Acad. Sci. 119, e2115608119 (2022).

    Article 
    CAS 

    Google Scholar 

  • Lan, Y. et al. Endosymbiont population genomics sheds light on transmission mode, partner specificity, and stability of the scaly-foot snail holobiont. ISME J. https://doi.org/10.1038/s41396-022-01261-4 (2022).

    Article 

    Google Scholar 

  • Anantharaman, K., Breier, J. A., Sheik, C. S. & Dick, G. J. Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria. Proc. Natl. Acad. Sci. 110, 330–335 (2013).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Fritsch, J. et al. Rubredoxin-related maturation factor guarantees metal cofactor integrity during aerobic biosynthesis of membrane-bound [NiFe] hydrogenase. J. Biol. Chem. 289, 7982–7993 (2014).

    Article 
    CAS 

    Google Scholar 

  • Petersen, J. M. et al. Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation. Nat. Microbiol. 2, 1–11 (2016).

    Article 

    Google Scholar 

  • Nakagawa, S. et al. Allying with armored snails: The complete genome of gammaproteobacterial endosymbiont. ISME J. 8, 40–51 (2014).

    Article 
    CAS 

    Google Scholar 

  • Vignais, P. M., Billoud, B. & Meyer, J. Classification and phylogeny of hydrogenases. FEMS Microbiol. Rev. 25, 455–501 (2001).

    Article 
    CAS 

    Google Scholar 

  • Perez, M. et al. Divergent paths in the evolutionary history of maternally transmitted clam symbionts. Proc. R. Soc. B 289, 20212137 (2022).

    Article 
    CAS 

    Google Scholar 

  • Li, S. et al. N 4-cytosine DNA methylation is involved in the maintenance of genomic stability in Deinococcus radiodurans. Front. Microbiol. 10, 1905 (2019).

    Article 

    Google Scholar 

  • Casadesús, J. & Low, D. Epigenetic gene regulation in the bacterial world. Microbiol. Mol. Biol. Rev. 70, 830–856 (2006).

    Article 

    Google Scholar 

  • De Oliveira, A. L., Srivastava, A., Espada-Hinojosa, S. & Bright, M. The complete and closed genome of the facultative generalist Candidatus Endoriftia persephone from deep-sea hydrothermal vents. Mol. Ecol. Resour. https://doi.org/10.1111/1755-0998.13668 (2022).

    Article 

    Google Scholar 

  • Ponnudurai, R. et al. Comparative proteomics of related symbiotic mussel species reveals high variability of host–symbiont interactions. ISME J. 14, 649–656 (2020).

    Article 
    CAS 

    Google Scholar 

  • Yu, N. Y. et al. PSORTb 3.0: Improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 26, 1608–1615 (2010).

    Article 
    CAS 

    Google Scholar 


  • Source: Ecology - nature.com

    Manufacturing a cleaner future

    MIT community in 2022: A year in review