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

Rubin-Blum, Maxim; Antony, Chakkiath Paul; Borowski, Christian; Sayavedra, Lizbeth; Pape, Thomas; Sahling, Heiko; Bohrmann, Gerhard; Kleiner, Manuel; Redmond, Molly C.; Valentine, David L.; Dubilier, Nicole

doi:10.1038/nmicrobiol.2017.93

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

Journal Article · Mon Jun 19 00:00:00 EDT 2017 · Nature Microbiology

DOI:https://doi.org/10.1038/nmicrobiol.2017.93· OSTI ID:1469810

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Max-Planck Inst. for Marine Microbiology, Bremen (Germany); osti
Max-Planck Inst. for Marine Microbiology, Bremen (Germany)
Univ. of Bremen (Germany). MARUM, Center for Marine Environmental Sciences
Univ. of Calgary, AB (Canada). Dept. of Geoscience
Univ. of North Carolina, Charlotte, NC (United States). Dept. of Biological Sciences
Univ. of California, Santa Barbara, CA (United States). Dept. of Earth Science
Max-Planck Inst. for Marine Microbiology, Bremen (Germany); Univ. of Bremen (Germany). MARUM, Center for Marine Environmental Sciences

Cycloclasticus bacteria are ubiquitous in oil-rich regions of the ocean and are known for their ability to degrade polycyclic aromatic hydrocarbons (PAHs). Here 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. Finally, 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.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of California, Santa Barbara, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); German Research Foundation (DFG); Gordon and Betty Moore Foundation (GBMF); National Science Foundation (NSF)

Grant/Contract Number:: AC02-05CH11231; AC52-07NA27344

OSTI ID:: 1469810

Journal Information:: Nature Microbiology, Journal Name: Nature Microbiology Vol. 2; ISSN 2058-5276

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Can hydrocarbons entrapped in seep carbonates serve as gas geochemistry recorder? Blumenberg, Martin; Pape, Thomas; Seifert, Richard Geo-Marine Letters, Vol. 38, Issue 2 https://doi.org/10.1007/s00367-017-0522-6	journal	August 2017
Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts Rubin-Blum, Maxim; Antony, Chakkiath Paul; Sayavedra, Lizbeth The ISME Journal, Vol. 13, Issue 5 https://doi.org/10.1038/s41396-019-0346-7	journal	January 2019
Horizontal acquisition of a patchwork Calvin cycle by symbiotic and free-living Campylobacterota (formerly Epsilonproteobacteria) Assié, Adrien; Leisch, Nikolaus; Meier, Dimitri V. The ISME Journal, Vol. 14, Issue 1 https://doi.org/10.1038/s41396-019-0508-7	journal	September 2019
Oil seepage and carbonate formation: A case study from the southern Gulf of Mexico Smrzka, Daniel; Zwicker, Jennifer; Misch, David Sedimentology, Vol. 66, Issue 6 https://doi.org/10.1111/sed.12593	journal	May 2019
Novel facultative Methylocella strains are active methane consumers at terrestrial natural gas seeps Farhan Ul Haque, Muhammad; Crombie, Andrew T.; Murrell, J. Colin Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0741-3	journal	October 2019
Resource partitioning among brachiopods and bivalves at ancient hydrocarbon seeps: A hypothesis Kiel, Steffen; Peckmann, Jörn PLOS ONE, Vol. 14, Issue 9 https://doi.org/10.1371/journal.pone.0221887	journal	September 2019
Liquid biopsies for omics-based analysis in sentinel mussels Caza, France; Joly de Boissel, Philippine Granger; Villemur, Richard PLOS ONE, Vol. 14, Issue 10 https://doi.org/10.1371/journal.pone.0223525	journal	October 2019
Application of in situ Solid-Phase Microextraction on Mediterranean Sponges for Untargeted Exometabolome Screening and Environmental Monitoring Bojko, Barbara; Onat, Bora; Boyaci, Ezel Frontiers in Marine Science, Vol. 6 https://doi.org/10.3389/fmars.2019.00632	journal	October 2019
More Is Not Always Better: Evaluation of 1D and 2D-LC-MS/MS Methods for Metaproteomics Hinzke, Tjorven; Kouris, Angela; Hughes, Rebecca-Ayme Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00238	journal	February 2019

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