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

Journal Article · · Nature Microbiology
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

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.

Research Organization:
Univ. of California, Santa Barbara, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); German Research Foundation (DFG); Gordon and Betty Moore Foundation (GBMF); National Science Foundation (NSF)
Grant/Contract Number:
AC02-05CH11231; AC52-07NA27344; GBMF3811; OCE-1155855; OCE-1046144
OSTI ID:
1469810
Journal Information:
Nature Microbiology, Vol. 2; ISSN 2058-5276
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 49 works
Citation information provided by
Web of Science

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Cited By (15)

Liquid biopsies for omics-based analysis in sentinel mussels journal October 2019
Comparative proteomics of related symbiotic mussel species reveals high variability of host–symbiont interactions journal November 2019
Application of in situ Solid-Phase Microextraction on Mediterranean Sponges for Untargeted Exometabolome Screening and Environmental Monitoring journal October 2019
The Effects of Crude Oil and Dispersant on the Larval Sponge Holobiont journal December 2019
(Table 1a) Concentrations of low-molecular-weight alkanes in gas samples of collection site GeoB19325-9 dataset March 2015
Novel facultative Methylocella strains are active methane consumers at terrestrial natural gas seeps journal October 2019
(Table 1b) Relative composition of light hydrocarbons of collection site GeoB19325-13 and GeoB19336-5 dataset January 2018
Horizontal acquisition of a patchwork Calvin cycle by symbiotic and free-living Campylobacterota (formerly Epsilonproteobacteria) journal September 2019
Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts journal January 2019
Oil seepage and carbonate formation: A case study from the southern Gulf of Mexico journal May 2019
Can hydrocarbons entrapped in seep carbonates serve as gas geochemistry recorder? journal August 2017
Variation of Oxygenation Conditions on a Hydrocarbonoclastic Microbial Community Reveals Alcanivorax and Cycloclasticus Ecotypes journal August 2017
Resource partitioning among brachiopods and bivalves at ancient hydrocarbon seeps: A hypothesis journal September 2019
Characterizing the microbiomes of Antarctic sponges: a functional metagenomic approach journal January 2020
More Is Not Always Better: Evaluation of 1D and 2D-LC-MS/MS Methods for Metaproteomics journal February 2019


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