Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Short-chain alkanes fuel mussel and sponge Cycloclasticus symbionts from deep-sea gas and oil seeps

Nature Microbiology volume 2, Article number: 17093 (2017) Cite this article

Subjects

Abstract

Cycloclasticus bacteria are ubiquitous in oil-rich regions of the ocean and are known for their ability to degrade polycyclic aromatic hydrocarbons (PAHs). In this study, we describe Cycloclasticus that have established a symbiosis with Bathymodiolus heckerae mussels and poecilosclerid sponges from asphalt-rich, deep-sea oil seeps at Campeche Knolls in the southern Gulf of Mexico. Genomic and transcriptomic analyses revealed that, in contrast to all previously known Cycloclasticus, the symbiotic Cycloclasticus appears to lack the genes needed for PAH degradation. Instead, these symbionts use propane and other short-chain alkanes such as ethane and butane as carbon and energy sources, thus expanding the limited range of substrates known to power chemosynthetic symbioses. Analyses of short-chain alkanes in the environment of the Campeche Knolls symbioses revealed that these are present at high concentrations (in the μM to mM range). Comparative genomic analyses revealed high similarities between the genes used by the symbiotic Cycloclasticus to degrade short-chain alkanes and those of free-living Cycloclasticus that bloomed during the Deepwater Horizon oil spill. Our results indicate that the metabolic versatility of bacteria within the Cycloclasticus clade is higher than previously assumed, and highlight the expanded role of these keystone species in the degradation of marine hydrocarbons.

Fossil hydrocarbons, abundant in seafloor reservoirs as petroleum and natural gas deposits, fuel the global economy and play an important role in biogeochemical cycles1. Natural seepage of fossil hydrocarbon has a pronounced effect on marine ecosystems2 and the atmosphere3–5, and anthropogenic oil discharge has far-reaching ramifications for the environment6–8. The presence of oil and natural gas in the water column affects the microbial community, which responds rapidly to hydrocarbon infusions9–12. These intrinsic microbes play an important role in the bioremediation of hydrocarbon pollution13. For example, oil plume bacteria have the potential to mitigate persistent and toxic pollutants, such as polycyclic aromatic hydrocarbons (PAHs)14–16. One group of ubiquitous marine PAH degraders are Cycloclasticus17, so named for their metabolic capability18. To date, all cultured Cycloclasticus are able to degrade PAHs, and there is considerable physiological and genomic evidence that uncultivated Cycloclasticus are also able to derive carbon and energy from the oxidation of PAHs (refs 12, 19–23).

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Invertebrate collection sites at Campeche Knolls.
Figure 2: FISH images of Cycloclasticus endosymbionts.
Figure 3: Phylogeny of Cycloclasticus 16S rRNA genes.
Figure 4: Reconstruction of central carbon and energy metabolic pathways in symbiotic Cycloclasticus.
Figure 5: Phylogeny of pHMO subunit A protein sequences.

References

  1. Bolin, B. in Oceanography (ed. Brewer, P. G. ) 305–326 (Springer, 1983).

    Google Scholar 

  2. Dando, P. R. & Hovland, M. Environmental effects of submarine seeping natural gas. Cont. Shelf Res. 12, 1197–1207 (1992).

    Google Scholar 

  3. Cicerone, R. J. & Oremland, R. Biogeological aspects of atmospheric methane. Global Biogeochem. Cycles 2, 229–327 (1988).

    Google Scholar 

  4. Collins, W. J., Derwent, R. G., Johnson, C. E. & Stevenson, D. S. The oxidation of organic compounds in the troposphere and their global warming potentials. Clim. Change 52, 453–479 (2002).

    CAS  Google Scholar 

  5. Katzenstein, A. S., Doezema, L. A., Simpson, I. J., Blake, D. R. & Rowland, F. S. Extensive regional atmospheric hydrocarbon pollution in the southwestern United States. Proc. Natl Acad. Sci. USA 100, 11975–11979 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Peterson, C. et al. Long-term ecosystem response to the Exxon Valdez oil spill. Science 302, 2082–2086 (2003).

    CAS  PubMed  Google Scholar 

  7. Head, I. M. & Swannell, R. P. Bioremediation of petroleum hydrocarbon contaminants in marine habitats. Curr. Opin. Biotechnol. 10, 234–239 (1999).

    CAS  PubMed  Google Scholar 

  8. Joye, S. B. et al. The Gulf of Mexico ecosystem, six years after the Macondo oil well blowout. Deep-Sea Res. II 129, 4–19 (2016).

    Google Scholar 

  9. Redmond, M. C. & Valentine, D. L. Natural gas and temperature structured a microbial community response to the Deepwater Horizon oil spill. Proc. Natl Acad. Sci. USA 109, 20292–20297 (2012).

    CAS  PubMed  Google Scholar 

  10. Valentine, D. L. et al. Propane respiration jump-starts microbial response to a deep oil spill. Science 330, 208–211 (2010).

    CAS  PubMed  Google Scholar 

  11. Kleindienst, S. et al. Diverse, rare microbial taxa responded to the Deepwater Horizon deep-sea hydrocarbon plume. ISME J. 10, 400–415 (2015).

    PubMed  PubMed Central  Google Scholar 

  12. Dombrowski, N. et al. Reconstructing metabolic pathways of hydrocarbon-degrading bacteria from the Deepwater Horizon oil spill. Nat. Microbiol. 1, 16057 (2016).

    CAS  PubMed  Google Scholar 

  13. Hazen, T. C. et al. Deep-sea oil plume enriches indigenous oil-degrading bacteria. Science 330, 204–208 (2010).

    CAS  PubMed  Google Scholar 

  14. Seo, J.-S., Keum, Y.-S. & Li, Q. X. Bacterial degradation of aromatic compounds. Int. J. Environ. Res. Public Health 6, 278–309 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Gutierrez, T. et al. Hydrocarbon-degrading bacteria enriched by the Deepwater Horizon oil spill identified by cultivation and DNA-SIP. ISME J. 7, 2091–2104 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Kappell, A. D. et al. The polycyclic aromatic hydrocarbon degradation potential of Gulf of Mexico native coastal microbial communities after the Deepwater Horizon oil spill. Front. Microbiol. 5, 205 (2014).

    PubMed  PubMed Central  Google Scholar 

  17. Kasai, Y., Kishira, H. & Harayama, S. Bacteria belonging to the genus Cycloclasticus play a primary role in the degradation of aromatic hydrocarbons released in a marine environment. Appl. Environ. Microbiol. 68, 5625–5633 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Yakimov, M. M., Timmis, K. N. & Golyshin, P. N. Obligate oil-degrading marine bacteria. Curr. Opin. Biotechnol. 18, 257–266 (2007).

    CAS  PubMed  Google Scholar 

  19. Kasai, Y., Shindo, K., Harayama, S. & Misawa, N. Molecular characterization and substrate preference of a polycyclic aromatic hydrocarbon dioxygenase from Cycloclasticus sp. strain A5. Appl. Environ. Microbiol. 69, 6688–6697 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Dyksterhouse, S. E., Gray, J. P., Herwig, R. P., Lara, J. C. & Staley, J. T. Cycloclasticus pugetii gen. nov., sp. nov., an aromatic hydrocarbon-degrading bacterium from marine sediments. Int. J. Syst. Bacteriol. 45, 116–123 (1995).

    CAS  PubMed  Google Scholar 

  21. Chung, W. K. & King, G. M. Isolation, characterization, and polyaromatic hydrocarbon degradation potential of aerobic bacteria from marine macrofaunal burrow sediments and description of Lutibacterium anuloederans gen. nov., sp. nov., and Cycloclasticus spirillensus sp. nov. Appl. Environ. Microbiol. 67, 5585–5592 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Cui, Z., Xu, G., Li, Q., Gao, W. & Zheng, L. Genome sequence of the pyrene- and fluoranthene-degrading bacterium Cycloclasticus sp. strain PY97M. Genome Announc. 1, e00536–13 (2013).

    PubMed  PubMed Central  Google Scholar 

  23. Messina, E. et al. Genome sequence of obligate marine polycyclic aromatic hydrocarbons-degrading bacterium Cycloclasticus sp. 78-ME, isolated from petroleum deposits of the sunken tanker Amoco Milford Haven, Mediterranean Sea. Mar. Genomics 25, 11–13 (2015).

    PubMed  Google Scholar 

  24. MacDonald, I. R. et al. Asphalt volcanism and chemosynthetic life in the Campeche Knolls, Gulf of Mexico. Science 304, 999–1002 (2004).

    CAS  PubMed  Google Scholar 

  25. Sahling, H. et al. Massive asphalt deposits, oil seepage, and gas venting support abundant chemosynthetic communities at the Campeche Knolls, southern Gulf of Mexico. Biogeosciences 13, 4491–4512 (2016).

    CAS  Google Scholar 

  26. 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).

    CAS  PubMed  Google Scholar 

  27. Duperron, S. et al. Diversity, relative abundance and metabolic potential of bacterial endosymbionts in three Bathymodiolus mussel species from cold seeps in the Gulf of Mexico. Environ. Microbiol. 9, 1423–1438 (2007).

    CAS  PubMed  Google Scholar 

  28. 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).

    CAS  PubMed  Google Scholar 

  29. Arellano, S. M. et al. Deep sequencing of Myxilla (Ectyomyxilla) methanophila, an epibiotic sponge on cold-seep tubeworms, reveals methylotrophic, thiotrophic, and putative hydrocarbon-degrading microbial associations. Microb. Ecol. 65, 450–461 (2013).

    CAS  PubMed  Google Scholar 

  30. Li, M., Jain, S., Baker, B. J., Taylor, C. & Dick, G. J. Novel hydrocarbon monooxygenase genes in the metatranscriptome of a natural deep-sea hydrocarbon plume. Environ. Microbiol. 16, 60–71 (2014).

    PubMed  Google Scholar 

  31. Tavormina, P. L., Ussler, W. & Orphan, V. J. Planktonic and sediment-associated aerobic methanotrophs in two seep systems along the North American Margin. Appl. Environ. Microbiol. 74, 3985–3995 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Hamamura, N., Yeager, C. M. & Arp, D. J. Two distinct monooxygenases for alkane oxidation in Nocardioides sp. strain CF8. Appl. Environ. Microbiol. 67, 4992–4998 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Coleman, N. V. et al. Hydrocarbon monooxygenase in Mycobacterium: recombinant expression of a member of the ammonia monooxygenase superfamily. ISME J. 6, 171–182 (2012).

    CAS  PubMed  Google Scholar 

  34. Redmond, M. C., Valentine, D. L. & Sessions, A. L. Identification of novel methane-, ethane-, and propane-oxidizing bacteria at marine hydrocarbon seeps by stable isotope probing. Appl. Environ. Microbiol. 76, 6412–6422 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Suzuki, T., Nakamura, T. & Fuse, H. Isolation of two novel marine ethylene-assimilating bacteria, Haliea species ETY-M and ETY-NAG, containing particulate methane monooxygenase-like genes. Microbes Environ. 27, 54–60 (2012).

    PubMed  PubMed Central  Google Scholar 

  36. Rivers, A. R. et al. Transcriptional response of bathypelagic marine bacterioplankton to the Deepwater Horizon oil spill. ISME J. 7, 2315–2329 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Vangnai, A. S. & Arp, D. J. An inducible 1-butanol dehydrogenase, a quinohaemoprotein, is involved in the oxidation of butane by ‘Pseudomonas butanovora’. Microbiology 147, 745–756 (2001).

    CAS  PubMed  Google Scholar 

  38. White, H., Huber, C., Feicht, R. & Simon, H. On a reversible molybdenum-containing aldehyde oxidoreductase from Clostridium formicoaceticum. Arch. Microbiol. 159, 244–249 (1993).

    CAS  Google Scholar 

  39. Vorobev, A. et al. Genomic and transcriptomic analyses of the facultative methanotroph Methylocystis sp. strain SB2 grown on methane or ethanol. Appl. Environ. Microbiol. 80, 3044–3052 (2014).

    PubMed  PubMed Central  Google Scholar 

  40. Matsen, J. B., Yang, S., Stein, L. Y., Beck, D. & Kalyuzhnaya, M. G. Global molecular analyses of methane metabolism in methanotrophic alphaproteobacterium, Methylosinus trichosporium OB3b. Part I: transcriptomic study. Front. Microbiol. 4, 40 (2013).

    PubMed  PubMed Central  Google Scholar 

  41. Schubotz, F. et al. Petroleum degradation and associated microbial signatures at the Chapopote asphalt volcano, Southern Gulf of Mexico. Geochim. Cosmochim. Acta 75, 4377–4398 (2011).

    CAS  Google Scholar 

  42. Joye, S. B., MacDonald, I. R., Leifer, I. & Asper, V. Magnitude and oxidation potential of hydrocarbon gases released from the BP oil well blowout. Nat. Geosci. 4, 160–164 (2011).

    CAS  Google Scholar 

  43. Head, I. M., Jones, D. M. & Röling, W. F. M. Marine microorganisms make a meal of oil. Nat. Rev. Microbiol. 4, 173–182 (2006).

    CAS  PubMed  Google Scholar 

  44. Mendes, S. D. et al. Marine microbes rapidly adapt to consume ethane, propane, and butane within the dissolved hydrocarbon plume of a natural seep. J. Geophys. Res. Ocean. 120, 1937–1953 (2015).

    CAS  Google Scholar 

  45. Schubotz, F. Microbial Community Characterization and Carbon Turnover in Methane-Rich Marine Environments—Case Studies in the Gulf of Mexico and the Black Sea. PhD dissertation, Univ. Bremen (2009).

  46. Gustafson, R. G., Turner, R. D., Lutz, R. A. & Vrijenhoek, R. C. A new genus and five new species of mussels (Bivalvia, Mytilidae) from deep-sea sulfide/hydrocarbon seeps in the Gulf of Mexico. Malacologia 40, 63–112 (1998).

    Google Scholar 

  47. Faure, B., Schaeffer, S. W. & Fisher, C. R. Species distribution and population connectivity of deep-sea mussels at hydrocarbon seeps in the Gulf of Mexico. PLoS ONE 10, e0118460 (2015).

    PubMed  PubMed Central  Google Scholar 

  48. Pape, T. et al. Molecular and isotopic partitioning of low-molecular-weight hydrocarbons during migration and gas hydrate precipitation in deposits of a high-flux seepage site. Chem. Geol. 269, 350–363 (2010).

    CAS  Google Scholar 

  49. Maruyama, A. et al. Dynamics of microbial populations and strong selection for Cycloclasticus pugetii following the Nakhodka oil spill. Microb. Ecol. 46, 442–453 (2003).

    CAS  PubMed  Google Scholar 

  50. Zhou, J., Bruns, M. A. & Tiedje, J. M. DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 62, 316–322 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Peng, Y., Leung, H. C. M., Yiu, S. M. & Chin, F. Y. L. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28, 1420–1428 (2012).

    CAS  PubMed  Google Scholar 

  52. Seah, B. K. B. & Gruber-Vodicka, H. R. Gbtools: interactive visualization of metagenome Bins in R. Front. Microbiol. 6, 1451 (2015).

    PubMed  PubMed Central  Google Scholar 

  53. Albertsen, M. et al. Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat. Biotechnol. 31, 533–538 (2013).

    CAS  PubMed  Google Scholar 

  54. Nurk, S., Bankevich, A. & Antipov, D. Assembling genomes and mini-metagenomes from highly chimeric reads. Res. Comput. Mol. Biol. 10, 158–170 (2013).

    Google Scholar 

  55. Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Gurevich, A., Saveliev, V., Vyahhi, N. & Tesler, G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 1072–1075 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Overbeek, R. et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 42, D206–D214 (2014).

    CAS  PubMed  Google Scholar 

  59. Huntemann, M. et al. The standard operating procedure of the DOE-JGI Microbial Genome Annotation Pipeline (MGAP v.4). Stand. Genomic Sci. 10, 86 (2015).

    PubMed  PubMed Central  Google Scholar 

  60. Johnson, M. et al. NCBI BLAST: a better web interface. Nucleic Acids Res. 36, W5–W9 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. 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).

    CAS  PubMed  Google Scholar 

  62. Petkau, A., Stuart-Edwards, M., Stothard, P. & van Domselaar, G. Interactive microbial genome visualization with GView. Bioinformatics 26, 3125–3126 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).

    CAS  PubMed  Google Scholar 

  64. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).

    Article  CAS  PubMed  Google Scholar 

  65. Rocha, D. J. P., Santos, C. S. & Pacheco, L. G. C. Bacterial reference genes for gene expression studies by RT–qPCR: survey and analysis. Antonie Van Leeuwenhoek 108, 685–693 (2015).

    CAS  PubMed  Google Scholar 

  66. Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinformatics 10, 421 (2009).

    PubMed  PubMed Central  Google Scholar 

  68. Wiśniewski, J. R., Zougman, A., Nagaraj, N. & Mann, M. Universal sample preparation method for proteome analysis. Nat. Methods 6, 359–362 (2009).

    PubMed  Google Scholar 

  69. Hamann, E. et al. Environmental Breviatea harbour mutualistic Arcobacter epibionts. Nature 534, 254–258 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Petersen, J. M. et al. Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation. Nat. Microbiol. 2, 16195 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Bettencourt, R. et al. High-throughput sequencing and analysis of the gill tissue transcriptome from the deep-sea hydrothermal vent mussel Bathymodiolus azoricus. BMC Genomics 11, 559 (2010).

    PubMed  PubMed Central  Google Scholar 

  72. Li, W. & Godzik, A. Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659 (2006).

    CAS  PubMed  Google Scholar 

  73. Florens, L. et al. Analyzing chromatin remodeling complexes using shotgun proteomics and normalized spectral abundance factors. Methods 40, 303–311 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Swan, B. K. et al. Potential for chemolithoautotrophy among ubiquitous bacteria lineages in the dark ocean. Science 333, 1296–1300 (2011).

    CAS  PubMed  Google Scholar 

  75. Le, S. Q. & Gascuel, O. An improved general amino acid replacement matrix. Mol. Biol. Evol. 25, 1307–1320 (2008).

    CAS  PubMed  Google Scholar 

  76. Kimura, M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111–120 (1980).

    CAS  PubMed  Google Scholar 

  77. Kumar, S., Stecher, G. & Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Markowitz, V. M. et al. IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res. 42, 560–567 (2014).

    Google Scholar 

  79. Vizcaíno, J. et al. Proteomexchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotechnol. 32, 223–226 (2014).

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank all who helped during the R/V Meteor research cruise M114, including onboard technical and scientific personnel, the captain and crew, and the ROV MARUM-QUEST 4000m team. The authors thank A. Crombie, University of East Anglia, UK, for discussions on propane metabolism and A. Rivers, DOE Joint Genome Institute, for sharing DWH plume PQQ-ADH transcript sequences. The authors thank M. Strous for access to proteomics equipment and E. Thorson for technical assistance with the determination of peptide concentrations. The purchase of the proteomics equipment was supported by a grant of the Canadian Foundation for Innovation to M. Strous. The authors acknowledge the Max Planck-Genome-Centre Cologne (http://mpgc.mpipz.mpg.de/home/) for generating the metagenomic and metatranscriptomic data used in this study. Cycloclasticus SAG sequencing was supported by the Joint Genome Institute's Community Science Program. The work conducted by the US Department of Energy Joint Genome Institute is supported by the Office of Science, Biological and Environmental Research Program of the US Department of Energy and by the University of California, Lawrence Berkeley National Laboratory under contract no. DE-AC02-05CH11231, Lawrence Livermore National Laboratory under contract no. DE-AC52-07NA27344 and Los Alamos National Laboratory under contract no. DE-AC02-06NA25396. The Campeche Knoll cruise was funded by the German Research Foundation (DFG, Deutsche Forschungsgemeinschaft). Additional support was provided through the MARUM DFG-Research Center/Excellence Cluster ‘The Ocean in the Earth System’ at the University of Bremen. The authors acknowledge the Mexican authorities for granting permission to conduct this research in the southern Gulf of Mexico (permission of DGOPA: 02540/14 from 5th November 2014). This study was funded by the Max Planck Society and the MARUM DFG-Research Center/Excellence Cluster ‘The Ocean in the Earth System’ at the University of Bremen. Further support was provided by an ERC Advanced Grant (BathyBiome, 340535) and a Gordon and Betty Moore Foundation Marine Microbial Initiative Investigator Award to N.D. (grant no. GBMF3811). D.L.V. and M.C.R. received funding from the US National Science Foundation grants OCE-1155855 and OCE-1046144. C.P.A. was supported by a postdoctoral fellowship from the Humboldt Foundation. M.K. was supported by a NSERC Banting Postdoctoral Fellowship.

Author information

Authors and Affiliations

  1. Max-Planck Institute for Marine Microbiology, Celsiusstrasse 1, 28359 Bremen, Germany

    Maxim Rubin-Blum, Chakkiath Paul Antony, Christian Borowski, Lizbeth Sayavedra & Nicole Dubilier

  2. MARUM, Center for Marine Environmental Sciences, University of Bremen, 28359 Bremen, Germany

    Thomas Pape, Heiko Sahling, Gerhard Bohrmann & Nicole Dubilier

  3. Department of Geoscience, University of Calgary, 2500 University Drive Northwest, Calgary, T2N 1N4, Alberta, Canada

    Manuel Kleiner

  4. Department of Biological Sciences, University of North Carolina at Charlotte, 9201 University City Blvd, Charlotte, 28223, North Carolina, USA

    Molly C. Redmond

  5. Department of Earth Science, University of California at Santa Barbara, 1006 Webb Hall, Santa Barbara, 93106, California, USA

    David L. Valentine

Authors
  1. Maxim Rubin-Blum
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chakkiath Paul Antony
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christian Borowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lizbeth Sayavedra
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Thomas Pape
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Heiko Sahling
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gerhard Bohrmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Manuel Kleiner
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Molly C. Redmond
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. David L. Valentine
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Nicole Dubilier
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M.R.-B., C.B., C.P.A. and N.D. conceived the study. H.S. and G.B. provided the framework for deep-sea sample collections. M.R.-B. and C.B. processed the samples onboard. M.R.-B., C.P.A. and L.S. analysed the biological samples. M.K. prepared samples for proteomics, and generated, processed and analysed proteomic data. T.P. provided the short-chain alkane analyses. M.C.R. and D.L.V. collected, prepared and sequenced the samples for the Deepwater Horizon Cycloclasticus SAGs and MCR, and D.L.V., M.R.-B. and C.P.A. analysed their genomes. M.R.-B. and N.D. wrote the manuscript with contributions from all co-authors.

Corresponding authors

Correspondence to Maxim Rubin-Blum or Nicole Dubilier.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Notes, Supplementary Tables 1–8 and Supplementary Figures 1–9. (PDF 8018 kb)

Supplementary Video (AVI 2481 kb)

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rubin-Blum, M., Antony, C., Borowski, C. et al. Short-chain alkanes fuel mussel and sponge Cycloclasticus symbionts from deep-sea gas and oil seeps. Nat Microbiol 2, 17093 (2017). https://doi.org/10.1038/nmicrobiol.2017.93

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nmicrobiol.2017.93

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing