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Title: 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). 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 ofmore » marine hydrocarbons.« less

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [5];  [6]
  1. Max-Planck Inst. for Marine Microbiology, Bremen (Germany)
  2. Univ. of Bremen (Germany). MARUM, Center for Marine Environmental Sciences
  3. Univ. of Calgary, AB (Canada). Dept. of Geoscience
  4. Univ. of North Carolina, Charlotte, NC (United States). Dept. of Biological Sciences
  5. Univ. of California, Santa Barbara, CA (United States). Dept. of Earth Science
  6. Max-Planck Inst. for Marine Microbiology, Bremen (Germany); Univ. of Bremen (Germany). MARUM, Center for Marine Environmental Sciences
Publication Date:
Research Org.:
Univ. of California, Santa Barbara, CA (United States)
Sponsoring Org.:
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)
OSTI Identifier:
1469810
Grant/Contract Number:  
AC02-05CH11231; AC52-07NA27344; GBMF3811; OCE-1155855; OCE-1046144
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Nature Microbiology
Additional Journal Information:
Journal Volume: 2; Journal ID: ISSN 2058-5276
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Rubin-Blum, Maxim, Antony, Chakkiath Paul, Borowski, Christian, Sayavedra, Lizbeth, Pape, Thomas, Sahling, Heiko, Bohrmann, Gerhard, Kleiner, Manuel, Redmond, Molly C., Valentine, David L., and Dubilier, Nicole. Short-chain alkanes fuel mussel and sponge Cycloclasticus symbionts from deep-sea gas and oil seeps. United States: N. p., 2017. Web. doi:10.1038/nmicrobiol.2017.93.
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. Short-chain alkanes fuel mussel and sponge Cycloclasticus symbionts from deep-sea gas and oil seeps. United States. doi:10.1038/nmicrobiol.2017.93.
Rubin-Blum, Maxim, Antony, Chakkiath Paul, Borowski, Christian, Sayavedra, Lizbeth, Pape, Thomas, Sahling, Heiko, Bohrmann, Gerhard, Kleiner, Manuel, Redmond, Molly C., Valentine, David L., and Dubilier, Nicole. Mon . "Short-chain alkanes fuel mussel and sponge Cycloclasticus symbionts from deep-sea gas and oil seeps". United States. doi:10.1038/nmicrobiol.2017.93. https://www.osti.gov/servlets/purl/1469810.
@article{osti_1469810,
title = {Short-chain alkanes fuel mussel and sponge Cycloclasticus symbionts from deep-sea gas and oil seeps},
author = {Rubin-Blum, Maxim and Antony, Chakkiath Paul and Borowski, Christian and Sayavedra, Lizbeth and Pape, Thomas and Sahling, Heiko and Bohrmann, Gerhard and Kleiner, Manuel and Redmond, Molly C. and Valentine, David L. and Dubilier, Nicole},
abstractNote = {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.},
doi = {10.1038/nmicrobiol.2017.93},
journal = {Nature Microbiology},
number = ,
volume = 2,
place = {United States},
year = {Mon Jun 19 00:00:00 EDT 2017},
month = {Mon Jun 19 00:00:00 EDT 2017}
}

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Works referenced in this record:

Propane Respiration Jump-Starts Microbial Response to a Deep Oil Spill
journal, September 2010

  • Valentine, David L.; Kessler, John D.; Redmond, Molly C.
  • Science, Vol. 330, Issue 6001, p. 208-211
  • DOI: 10.1126/science.1196830