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

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.

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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.

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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.

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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.

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Correspondence to Maxim Rubin-Blum or Nicole Dubilier.

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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

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