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Complete gammaproteobacterial endosymbiont genome assembly from a seep tubeworm Lamellibrachia satsuma

  • Microbial Genetics, Genomics and Molecular Biology
  • Published:
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Abstract

Siboglinid tubeworms thrive in hydrothermal vent and seep habitats via a symbiotic relationship with chemosynthetic bacteria. Difficulties in culturing tubeworms and their symbionts in a laboratory setting have hindered the study of host-microbe interactions. Therefore, released symbiont genomes are fragmented, thereby limiting the data available on the genome that affect subsequent analyses. Here, we present a complete genome of gammaproteobacterial endosymbiont from the tubeworm Lamellibrachia satsuma collected from a seep in Kagoshima Bay, assembled using a hybrid approach that combines sequences generated from the Illumina and Oxford Nano-pore platforms. The genome consists of a single circular chromosome with an assembly size of 4,323,754 bp and a GC content of 53.9% with 3,624 protein-coding genes. The genome is of high quality and contains no assembly gaps, while the completeness and contamination are 99.33% and 2.73%, respectively. Comparative genome analysis revealed a total of 1,724 gene clusters shared in the vent and seep tubeworm symbionts, while 294 genes were found exclusively in L. satsuma symbionts such as transposons, genes for defense mechanisms, and inorganic ion transportations. The addition of this complete endosymbiont genome assembly would be valuable for comparative studies particularly with tubeworm symbiont genomes as well as with other chemosynthetic microbial communities.

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Data Availability

The sequence and genomic data that support the findings of this study have been deposited in GenBank with under the BioProject accession number PRJNA629652.

References

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

    Article  CAS  PubMed  Google Scholar 

  • Antelmann, H., Scharf, C., and Hecker, M. 2000. Phosphate starvation-inducible proteins of Bacillus subtilis: proteomics and transcriptional analysis. J. Bacteriol. 182, 4478–4490.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D.A., and Horvath, P. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315, 1709–1712.

    Article  CAS  PubMed  Google Scholar 

  • Barrangou, R. and Marraffini, L.A. 2014. CRISPR-Cas systems: prokaryotes upgrade to adaptive immunity. Mol. Cell 54, 234–244.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bren, A. and Eisenbach, M. 2000. How signals are heard during bacterial chemotaxis: protein-protein interactions in sensory signal propagation. J. Bacteriol. 182, 6865–6873.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breusing, C., Schultz, D.T., Sudek, S., Worden, A.Z., and Young, C.R. 2020. High-contiguity genome assembly of the chemosynthetic gammaproteobacterial endosymbiont of the cold seep tubeworm Lamellibrachia barhami. Mol. Ecol. Resour. 20, 1432–1444.

    Article  CAS  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen, L.X., Anantharaman, K., Shaiber, A., Eren, A.M., and Banfield, J.F. 2020. Accurate and complete genomes from metagenomes. Genome Res. 30, 315–333.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cimermancic, P., Medema, M.H., Claesen, J., Kurita, K., Wieland Brown, L.C., Mavrommatis, K., Pati, A., Godfrey, P.A., Koehrsen, M., Clardy, J., et al. 2014. Insights into secondary metabolism from a global analysis of prokaryotic biosynthetic gene clusters. Cell 158, 412–421.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Durand, E., Bernadac, A., Ball, G., Lazdunski, A., Sturgis, J.N., and Filloux, A. 2003. Type II protein secretion in Pseudomonas aeruginosa: the pseudopilus is a multifibrillar and adhesive structure. J. Bacteriol. 185, 2749–2758.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edgar, R.C. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Elsaied, H., Kimura, H., and Naganuma, T. 2002. Molecular characterization and endosymbiotic localization of the gene encoding D-ribulose 1,5-bisphosphate carboxylase-oxygenase (RuBisCO) form II in the deep-sea vestimentiferan trophosome. Microbiology 148, 1947–1957.

    Article  CAS  PubMed  Google Scholar 

  • Eren, A.M., Kiefl, E., Shaiber, A., Veseli, I., Miller, S.E., Schechter, M.S., Fink, I., Pan, J.N., Yousef, M., Fogarty, E.C., et al. 2021. Community-led, integrated, reproducible multi-omics with anvi’o. Nat. Microbiol. 6, 3–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fontanez, K.M. and Cavanaugh, C.M. 2014. Evidence for horizontal transmission from multilocus phylogeny of deep-sea mussel (Mytilidae) symbionts. Environ. Microbiol. 16, 3608–3621.

    Article  PubMed  Google Scholar 

  • Freytag, J.K., Girguis, P.R., Bergquist, D.C., Andras, J.P., Childress, J.J., and Fisher, C.R. 2001. A paradox resolved: sulfide acquisition by roots of seep tubeworms sustains net chemoautotrophy. Proc. Natl. Acad. Sci. USA 98, 13408–13413.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gardebrecht, A., Markert, S., Sievert, S. M., Felbeck, H., Thürmer, A., Albrecht, D., Wollherr, A., Kabisch, J., Le Bris, N., Lehmann, R., et al. 2012. Physiological homogeneity among the endosymbionts of Riftia pachyptila and Tevnia jerichonana revealed by proteogenomics. ISME J. 6, 766–776.

    Article  CAS  PubMed  Google Scholar 

  • Garrett, S.C. 2021. Pruning and tending immune memories: spacer dynamics in the CRISPR array. Front. Microbiol. 12, 664299.

    Article  PubMed  PubMed Central  Google Scholar 

  • Goldstein, S., Beka, L., Graf, J., and Klassen, J.L. 2019. Evaluation of strategies for the assembly of diverse bacterial genomes using MinION long-read sequencing. BMC Genomics 20, 23.

    Article  PubMed  PubMed Central  Google Scholar 

  • Goodwin, S., McPherson, J.D., and McCombie, W.R. 2016. Coming of age: ten years of next-generation sequencing technologies. Nat. Rev. Genet. 17, 333–351.

    Article  CAS  PubMed  Google Scholar 

  • Gregory, A.C., Zayed, A.A., Conceição-Neto, N., Temperton, B., Bolduc, B., Alberti, A., Ardyna, M., Arkhipova, K., Carmichael, M., Cruaud, C., et al. 2019. Marine DNA viral macro- and micro-diversity from pole to pole. Cell 177, 1109–1123.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grubbs, K.J., Bleich, R.M., Santa Maria, K.C., Allen, S.E., Farag, S., AgBiome Team, Shank, E.A., and Bowers, A.A. 2017. Large-scale bioinformatics analysis of Bacillus genomes uncovers conserved roles of natural products in bacterial physiology. mSystems 2, e00040–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hug, L.A., Baker, B.J., Anantharaman, K., Brown, C.T., Probst, A.J., Castelle, C.J., Butterfield, C.N., Hernsdorf, A.W., Amano, Y., Ise, K., et al. 2016. A new view of the tree of life. Nat. Microbiol. 1, 16048.

    Article  CAS  PubMed  Google Scholar 

  • Hügler, M., Petersen, J.M., Dubilier, N., Imhoff, J.F., and Sievert, S.M. 2011. Pathways of carbon and energy metabolism of the epibiotic community associated with the deep-sea hydrothermal vent shrimp Rimicaris exoculata. PLoS ONE 6, e16018.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hügler, M. and Sievert, S.M. 2010. Beyond the Calvin cycle: autotrophic carbon fixation in the ocean. Ann. Rev. Mar. Sci. 3, 261–289.

    Article  Google Scholar 

  • Jayakumar, V. and Sakakibara, Y. 2017. Comprehensive evaluation of non-hybrid genome assembly tools for third-generation Pac-Bio long-read sequence data. Brief. Bioinform. 20, 866–876.

    Article  PubMed Central  CAS  Google Scholar 

  • Jensen, L.J., Julien, P., Kuhn, M., von Mering, C., Muller, J., Doerks, T., and Bork, P. 2008. eggNOG: automated construction and annotation of orthologous groups of genes. Nucleic Acids Res. 36, D250–D254.

    Article  CAS  PubMed  Google Scholar 

  • Jovel, J., Patterson, J., Wang, W., Hotte, N., O’Keefe, S., Mitchel, T., Perry, T., Kao, D., Mason, A.L., Madsen, K.L., et al. 2016. Characterization of the gut microbiome using 16S or shotgun metagenomics. Front. Microbiol. 7, 459.

    Article  PubMed  PubMed Central  Google Scholar 

  • Julian, D., Gaill, F., Wood, E., Arp, A.J., and Fisher, C.R. 1999. Roots as a site of hydrogen sulfide uptake in the hydrocarbon seep vestimentiferan Lamellibrachia sp. J. Exp. Biol. 202, 2245–2257.

    Article  CAS  PubMed  Google Scholar 

  • Kanehisa, M., Sato, Y., Kawashima, M., Furumichi, M., and Tanabe, M. 2015. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res. 44, D457–D462.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Karl, D.M., Taylor, G.T., Novitsky, J.A., Jannasch, H.W., Wirsen, C.O., Pace, N.R., Lane, D.J., Olsen, G.J., and Giovannoni, S.J. 1988. A microbiological study of Guaymas Basin high temperature hydrothermal vents. Deep Sea Res. A 35, 777–791.

    Article  CAS  Google Scholar 

  • Kellogg, C.A. 2010. Enumeration of viruses and prokaryotes in deep-sea sediments and cold seeps of the Gulf of Mexico. Deep Sea Res. 2 Top. Stud. Oceanogr. 57, 2002–2007.

    Article  Google Scholar 

  • Latorre-Pérez, A., Villalba-Bermell, P., Pascual, J., and Vilanova, C. 2020. Assembly methods for nanopore-based metagenomic sequencing: a comparative study. Sci. Rep. 10, 13588.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee, R.W. and Childress, J.J. 1994. Assimilation of inorganic nitrogen by marine invertebrates and their chemoautotrophic and methanotrophic symbionts. Appl. Environ. Microbiol. 60, 1852–1858.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic, I. and Bork, P. 2019. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 47, W256–W259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, H. 2018. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, H. 2020. seqtk. https://github.com/lh3/seqtk. (accessed on January 2020)

  • Li, H. and Durbin, R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., and 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li, Y., Liles, M.R., and Halanych, K.M. 2018. Endosymbiont genomes yield clues of tubeworm success. ISME J. 12, 2785–2795.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, L., Stoeckert, C.J.Jr, and Roos, D.S. 2003. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178–2189.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liao, L., Wankel, S.D., Wu, M., Cavanaugh, C.M., and Girguis, P.R. 2014. Characterizing the plasticity of nitrogen metabolism by the host and symbionts of the hydrothermal vent chemoautotrophic symbioses Ridgeia piscesae. Mol. Ecol. 23, 1544–1557.

    Article  CAS  PubMed  Google Scholar 

  • Lilley, M.D., Butterfield, D.A., Olson, E.J., Lupton, J.E., Macko, S.A., and McDuff, R.E. 1993. Anomalous CH4 and NH4+ concentrations at an unsedimented mid-ocean-ridge hydrothermal system. Nature 364, 45–47.

    Article  CAS  Google Scholar 

  • Loman, N.J., Quick, J., and Simpson, J.T. 2015. A complete bacterial genome assembled de novo using only nanopore sequencing data. Nat. Methods 12, 733–735.

    Article  CAS  PubMed  Google Scholar 

  • Maguire, F., Jia, B., Gray, K.L., Lau, W.Y.V., Beiko, R.G., and Brinkman, F.S.L. 2020. Metagenome-assembled genome binning methods with short reads disproportionately fail for plasmids and genomic Islands. Microb. Genomics 6, mgen000436.

    Article  CAS  Google Scholar 

  • Makarova, K.S. and Koonin, E.V. 2015. Annotation and classification of CRISPR-Cas systems. Methods Mol. Biol. 1311, 47–75.

    Article  PubMed  PubMed Central  Google Scholar 

  • Maki, T., Kume, A., and Ura, T. 2011. Volumetric mapping of tube-worm colonies in Kagoshima Bay through autonomous robotic surveys. Deep Sea Res. 1 Oceanogr. Res. Pap. 58, 757–767.

    Article  Google Scholar 

  • Markert, S., Arndt, C., Felbeck, H., Becher, D., Sievert, S.M., Hügler, M., Albrecht, D., Robidart, J., Bench, S., Feldman, R.A., et al. 2007. Physiological proteomics of the uncultured endosymbiont of Riftia pachyptila. Science 315, 247–250.

    Article  CAS  PubMed  Google Scholar 

  • Medema, M.H., Blin, K., Cimermancic, P., de Jager, V., Zakrzewski, P., Fischbach, M.A., Weber, T., Takano, E., and Breitling, R. 2011. antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res. 39, W339–W346.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meier-Kolthoff, J.P., Auch, A.F., Klenk, H.P., and Göker, M. 2013. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14, 60.

    Article  PubMed  PubMed Central  Google Scholar 

  • Minic, Z. and Herve, G. 2003. Arginine metabolism in the deep sea tube worm Riftia pachyptila and its bacterial endosymbiont. J. Biol. Chem. 278, 40527–40533.

    Article  CAS  PubMed  Google Scholar 

  • Miura, T., Tsukahara, J., and Hashimoto, J. 1997. Lamellibrachia Satsuma, a new species of vestimentiferan worms bay, Japan. Proc. Biol. Soc. Wash. 110, 447–456.

    Google Scholar 

  • Miyake, H., Tsukahara, J., Hashimoto, J., Uematsu, K., and Maruyama, T. 2006. Rearing and observation methods of vestimentiferan tubeworm and its early development at atmospheric pressure. Cah. Biol. Mar. 47, 471–475.

    Google Scholar 

  • Naganuma, T., Elsaied, H.E., Hoshii, D., and Kimura, H. 2005. Bacterial endosymbioses of gutless tube-dwelling worms in nonhydrothermal vent habitats. Mar. Biotechnol. 7, 416–428.

    Article  CAS  Google Scholar 

  • Narasingarao, P. and Häggblom, M.M. 2006. Sedimenticola selenatireducens, gen. nov., sp. nov., an anaerobic selenate-respiring bacterium isolated from estuarine sediment. Syst. Appl. Microbiol. 29, 382–388.

    Article  CAS  PubMed  Google Scholar 

  • Nicholls, S.M., Quick, J.C., Tang, S., and Loman, N.J. 2019. Ultra-deep, long-read nanopore sequencing of mock microbial community standards. GigaScience 8, giz043.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nishimura, Y., Watai, H., Honda, T., Mihara, T., Omae, K., Roux, S., Blanc-Mathieu, R., Yamamoto, K., Hingamp, P., Sako, Y., et al. 2017. Environmental viral genomes shed new light on virushost interactions in the ocean. mSphere 2, e00359–16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nurk, S., Meleshko, D., Korobeynikov, A., and Pevzner, P.A. 2017. metaSPAdes: a new versatile metagenomic assembler. Genome Res. 27, 824–834.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ojeda Alayon, D.I., Tsui, C.K.M., Feau, N., Capron, A., Dhillon, B., Zhang, Y., Massoumi Alamouti, S., Boone, C.K., Carroll, A.L., Cooke, J.E.K., et al. 2017. Genetic and genomic evidence of niche partitioning and adaptive radiation in mountain pine beetle fungal symbionts. Mol. Ecol. 26, 2077–2091.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patra, A.K., Cho, H.H., Kwon, Y.M., Kwon, K.K., Sato, T., Kato, C., Kang, S.G., and Kim, S.J. 2016. Phylogenetic relationship between symbionts of tubeworm Lamellibrachia satsuma and the sediment microbial community in Kagoshima Bay. Ocean Sci. J. 51, 317–332.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petersen, J.M., Zielinski, F.U., Pape, T., Seifert, R., Moraru, C., Amann, R., Hourdez, S., Girguis, P.R., Wankel, S.D., Barbe, V., et al. 2011. Hydrogen is an energy source for hydrothermal vent symbioses. Nature 476, 176–180.

    Article  CAS  PubMed  Google Scholar 

  • Rang, F.J., Kloosterman, W.P., and de Ridder, J. 2018. From squiggle to basepair: computational approaches for improving nanopore sequencing read accuracy. Genome Biol. 19, 90.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Reveillaud, J., Anderson, R., Reves-Sohn, S., Cavanaugh, C., and Huber, J.A. 2018. Metagenomic investigation of vestimentiferan tubeworm endosymbionts from Mid-Cayman Rise reveals new insights into metabolism and diversity. Microbiome 6, 19.

    Article  PubMed  PubMed Central  Google Scholar 

  • Richter, M. and Rosselló-Móra, R. 2009. Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl. Acad. Sci. USA 106, 19126–19131.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robidart, J.C., Bench, S.R., Feldman, R.A., Novoradovsky, A., Podell, S.B., Gaasterland, T., Allen, E.E., and Felbeck, H. 2008. Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics. Environ. Microbiol. 10, 727–737.

    Article  CAS  PubMed  Google Scholar 

  • Rubin-Blum, M., Dubilier, N., and Kleiner, M. 2019. Genetic evidence for two carbon fixation pathways (the Calvin-Benson-Bassham cycle and the reverse tricarboxylic acid cycle) in symbiotic and free-living bacteria. mSphere 4, e00394–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Simão, F.A., Waterhouse, R.M., Ioannidis, P., Kriventseva, E.V., and Zdobnov, E.M. 2015. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212.

    Article  PubMed  CAS  Google Scholar 

  • Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stewart, F.J., Newton, I.L.G., and Cavanaugh, C.M. 2005. Chemosynthetic endosymbioses: adaptations to oxic—anoxic interfaces. Trends Microbiol. 13, 439–448.

    Article  CAS  PubMed  Google Scholar 

  • Susko, E., Leigh, J., Doolittle, W.F., and Bapteste, E. 2006. Visualizing and assessing phylogenetic congruence of core gene sets: a case study of the γ-proteobacteria. Mol. Biol. Evol. 23, 1019–1030.

    Article  CAS  PubMed  Google Scholar 

  • Suttle, C.A. 2005. Viruses in the sea. Nature 437, 356–361.

    Article  CAS  PubMed  Google Scholar 

  • Tatusov, R.L., Galperin, M.Y., Natale, D.A., and Koonin, E.V. 2000. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 28, 33–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tatusova, T., Dicuccio, M., Badretdin, A., Chetvernin, V., Nawrocki, E.P., Zaslavsky, L., Lomsadze, A., Pruitt, K.D., Borodovsky, M., and Ostell, J. 2016. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. 44, 6614–6624.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thiel, V., Hügler, M., Blümel, M., Baumann, H., Gärtner, A., Schmaljohann, R., Strauss, H., Garbe-Schönberg, D., Petersen, S., Cowart, D., et al. 2012. Widespread occurrence of two carbon fixation pathways in tubeworm endosymbionts: lessons from hydrothermal vent associated tubeworms from the Mediterranean Sea. Front. Microbiol. 3, 423.

    Article  PubMed  PubMed Central  Google Scholar 

  • Toft, C. and Andersson, S.G.E. 2010. Evolutionary microbial genomics: insights into bacterial host adaptation. Nat. Rev. Genet. 11, 465–475.

    Article  CAS  PubMed  Google Scholar 

  • Tyson, G.W., Chapman, J., Hugenholtz, P., Allen, E.E., Ram, R.J., Richardson, P.M., Solovyev, V.V, Rubin, E.M., Rokhsar, D.S., and Banfield, J.F. 2004. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428, 37–43.

    Article  CAS  PubMed  Google Scholar 

  • Von Damm, K.L., Edmond, J.M., Measures, C.I., and Grant, B. 1985. Chemistry of submarine hydrothermal solutions at Guaymas Basin, Gulf of California. Geochim. Cosmochim. Acta 49, 2221–2237.

    Article  CAS  Google Scholar 

  • Weirather, J.L., de Cesare, M., Wang, Y., Piazza, P., Sebastiano, V., Wang, X.J., Buck, D., and Au, K.F. 2017. Comprehensive comparison of Pacific Biosciences and Oxford Nanopore Technologies and their applications to transcriptome analysis. F1000Res. 6, 100.

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wilkins, L.G.E., Ettinger, C.L., Jospin, G., and Eisen, J.A. 2019. Metagenome-assembled genomes provide new insight into the microbial diversity of two thermal pools in Kamchatka, Russia. Sci. Rep. 9, 3059.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Won, Y.J., Hallam, S.J., O’Mullan, G.D., Pan, I.L., Buck, K.R., and Vrijenhoek, R.C. 2003. Environmental acquisition of thiotrophic endosymbionts by deep-sea mussels of the genus Bathymodiolus. Appl. Environ. Microbiol. 69, 6785–6792.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue, C. and Sashital, D.G. 2019. Mechanisms of Type I-E and I-F CRISPR-Cas Systems in Enterobacteriaceae. EcoSal Plus 8. doi: https://doi.org/10.1128/ecosalplus.ESP-0008-2018.

  • Yamamoto, H., Fujikura, K., Hiraishi, A., and Kato, K. 2002. Phylogenetic characterization and biomass estimation of bacterial endosymbionts associated with invertebrates dwelling in chemosynthetic communities of hydrothermal vent and cold seep fields. Mar. Ecol. Prog. Ser. 245, 61–67.

    Article  Google Scholar 

  • Yang, Y., Sun, J., Sun, Y., Kwan, Y.H., Wong, W.C., Zhang, Y., Xu, T., Feng, D., Zhang, Y., Qiu, J.W., et al. 2020. Genomic, transcriptomic, and proteomic insights into the symbiosis of deep-sea tubeworm holobionts. ISME J. 14, 135–150.

    Article  CAS  PubMed  Google Scholar 

  • Yu, Y., Ouyang, Y., and Yao, W. 2018. shinyCircos: an R/Shiny application for interactive creation of Circos plot. Bioinformatics 34, 1229–1231.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, Y., Murphy, A.C., Samborskyy, M., Prediger, P., Dias, L.C., and Leadlay, P.F. 2015. Iterative mechanism of macrodiolide formation in the anticancer compound conglobatin. Chem. Biol. 22, 745–754.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This research was financially supported by the National Marine Biodiversity Institute of Korea (MABIK) in-house program (2022M00400).

We would like to thank the captain and crew of R/V Natsushima and the operation team of ROV Hyper-Dolphin, Japan Agency for Marine-Earth Science & Technology (JAMSTEC) for sample collection. The authors also wish to thank Dr. Kyungwha Baek for critically reading the manuscript, interpretation of the analysis results, and helpful discussions. We would like to thank Editage (www.editage.co.kr) for English language editing.

Author information

Authors and Affiliations

  1. Division of Ecoscience, Ewha Womans University, Seoul, 03760, Korea

    Ajit Kumar Patra

  2. Department of Macrobial Resources, National Marine Biodiversity Institute of Korea, Seochun, 33662, Korea

    Yong Min Kwon

  3. Department of Genetic Resources, National Marine Biodiversity Institute of Korea, Seochun, 33662, Korea

    Youngik Yang

Authors
  1. Ajit Kumar Patra
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  2. Yong Min Kwon
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  3. Youngik Yang
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Contributions

A.K.P. and Y.Y. conceived and conducted the experiments; A.K.P., Y.M.K., and Y.Y. analyzed the results; A.K.P., Y.M.K, and Y.Y. wrote the manuscript. All authors reviewed the manuscript.

Corresponding author

Correspondence to Youngik Yang.

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Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Patra, A.K., Kwon, Y.M. & Yang, Y. Complete gammaproteobacterial endosymbiont genome assembly from a seep tubeworm Lamellibrachia satsuma. J Microbiol. 60, 916–927 (2022). https://doi.org/10.1007/s12275-022-2057-4

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  • DOI: https://doi.org/10.1007/s12275-022-2057-4

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