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Title: Anaerobic Oxidation of Ethane, Propane, and Butane by Marine Microbes: A Mini Review

Abstract

The deep ocean and its sediments are a continuous source of non-methane short-chain alkanes (SCAs) including ethane, propane, and butane. Their high global warming potential, and contribution to local carbon and sulfur budgets has drawn significant scientific attention. Importantly, microbes can use gaseous alkanes and oxidize them to CO 2, thus acting as effective biofilters. A relative decrease of these gases with a concomitant 13C enrichment of propane and n-butane in interstitial waters vs. the source suggests microbial anaerobic oxidation. The reported uncoupling of sulfate-reduction (SR) from anaerobic methane oxidation supports their microbial consumption. To date, strain BuS5 isolated from the sediments of Guaymas Basin, Gulf of California, is the only pure culture that can anaerobically degrade propane and n-butane. This organism belongs to a metabolically diverse cluster within the Deltaproteobacteria called Desulfosarcina/Desulfococcus. Other phylotypes involved in gaseous alkane degradation were identified based on stable-isotope labeling and fluorescence in-situ hybridization. A novel syntrophic association of the archaeal genus, Candidatus Syntrophoarchaeum, and a thermophilic SR bacterium, HotSeep-1 was recently discovered from the Guaymas basin, Gulf of California that can anaerobically oxidize n-butane. Strikingly, metagenomic data and the draft genomes of ca. Syntrophoarchaeum suggest that this organism uses a novel mechanism formore » n-butane oxidation, distinct from the well-established fumarate addition mechanism. These recent findings indicate that a lot remains to be understood about our understanding of anaerobic SCA degradation. This mini-review summarizes our current understanding of microbial anaerobic SCA degradation, and provides an outlook for future research.« less

Authors:
 [1];  [1];  [1]
  1. Washington Univ., St. Louis, MO (United States)
Publication Date:
Research Org.:
Washington Univ., St. Louis, MO (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1510493
Grant/Contract Number:  
[SC0014613]
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
[ Journal Volume: 8]; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Gulf of Mexico; short-chain alkanes; sulfate reduction; anaerobic oxidation; Desulfosarcina/Desulfococcus

Citation Formats

Singh, Rajesh, Guzman, Michael S., and Bose, Arpita. Anaerobic Oxidation of Ethane, Propane, and Butane by Marine Microbes: A Mini Review. United States: N. p., 2017. Web. doi:10.3389/fmicb.2017.02056.
Singh, Rajesh, Guzman, Michael S., & Bose, Arpita. Anaerobic Oxidation of Ethane, Propane, and Butane by Marine Microbes: A Mini Review. United States. doi:10.3389/fmicb.2017.02056.
Singh, Rajesh, Guzman, Michael S., and Bose, Arpita. Mon . "Anaerobic Oxidation of Ethane, Propane, and Butane by Marine Microbes: A Mini Review". United States. doi:10.3389/fmicb.2017.02056. https://www.osti.gov/servlets/purl/1510493.
@article{osti_1510493,
title = {Anaerobic Oxidation of Ethane, Propane, and Butane by Marine Microbes: A Mini Review},
author = {Singh, Rajesh and Guzman, Michael S. and Bose, Arpita},
abstractNote = {The deep ocean and its sediments are a continuous source of non-methane short-chain alkanes (SCAs) including ethane, propane, and butane. Their high global warming potential, and contribution to local carbon and sulfur budgets has drawn significant scientific attention. Importantly, microbes can use gaseous alkanes and oxidize them to CO2, thus acting as effective biofilters. A relative decrease of these gases with a concomitant 13C enrichment of propane and n-butane in interstitial waters vs. the source suggests microbial anaerobic oxidation. The reported uncoupling of sulfate-reduction (SR) from anaerobic methane oxidation supports their microbial consumption. To date, strain BuS5 isolated from the sediments of Guaymas Basin, Gulf of California, is the only pure culture that can anaerobically degrade propane and n-butane. This organism belongs to a metabolically diverse cluster within the Deltaproteobacteria called Desulfosarcina/Desulfococcus. Other phylotypes involved in gaseous alkane degradation were identified based on stable-isotope labeling and fluorescence in-situ hybridization. A novel syntrophic association of the archaeal genus, Candidatus Syntrophoarchaeum, and a thermophilic SR bacterium, HotSeep-1 was recently discovered from the Guaymas basin, Gulf of California that can anaerobically oxidize n-butane. Strikingly, metagenomic data and the draft genomes of ca. Syntrophoarchaeum suggest that this organism uses a novel mechanism for n-butane oxidation, distinct from the well-established fumarate addition mechanism. These recent findings indicate that a lot remains to be understood about our understanding of anaerobic SCA degradation. This mini-review summarizes our current understanding of microbial anaerobic SCA degradation, and provides an outlook for future research.},
doi = {10.3389/fmicb.2017.02056},
journal = {Frontiers in Microbiology},
number = ,
volume = [8],
place = {United States},
year = {2017},
month = {10}
}

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Figures / Tables:

Figure 1 Figure 1: Anaerobic activation of propane at the sub-terminal (A) and terminal (B) carbon atom (marked with stars) via fumarate addition yielding isopropylsuccinate and n-propylsuccinate, respectively. A similar activation mechanism exclusively at the sub-terminal carbon atom is proposed for the anaerobic oxidation of n-butane.

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Works referenced in this record:

Marine microorganisms make a meal of oil
journal, March 2006

  • Head, Ian M.; Jones, D. Martin; Röling, Wilfred F. M.
  • Nature Reviews Microbiology, Vol. 4, Issue 3
  • DOI: 10.1038/nrmicro1348

Anaerobic degradation of naphthalene and 2-methylnaphthalene by strains of marine sulfate-reducing bacteria
journal, January 2009


Hydrocarbon geochemistry of cold seeps in the Monterey Bay National Marine Sanctuary
journal, March 2002


Oil Biodegradation and Bioremediation: A Tale of the Two Worst Spills in U.S. History
journal, August 2011

  • Atlas, Ronald M.; Hazen, Terry C.
  • Environmental Science & Technology, Vol. 45, Issue 16, p. 6709-6715
  • DOI: 10.1021/es2013227

Geomicrobiological linkages between short-chain alkane consumption and sulfate reduction rates in seep sediments
journal, January 2013


The anaerobic oxidation of methane and sulfate reduction in sediments from Gulf of Mexico cold seeps
journal, May 2004


Acetone in the atmosphere: Distribution, sources, and sinks
journal, January 1994

  • Singh, H. B.; O'Hara, D.; Herlth, D.
  • Journal of Geophysical Research, Vol. 99, Issue D1
  • DOI: 10.1029/93JD00764

Comparison of Mechanisms of Alkane Metabolism under Sulfate-Reducing Conditions among Two Bacterial Isolates and a Bacterial Consortium
journal, June 2006

  • Callaghan, A. V.; Gieg, L. M.; Kropp, K. G.
  • Applied and Environmental Microbiology, Vol. 72, Issue 6
  • DOI: 10.1128/AEM.02896-05

Distributions of Microbial Activities in Deep Subseafloor Sediments
journal, December 2004


Light nonmethane hydrocarbons in seawater
journal, March 1995

  • Plass-Dülmer, C.; Koppmann, R.; Ratte, M.
  • Global Biogeochemical Cycles, Vol. 9, Issue 1
  • DOI: 10.1029/94GB02416

Nature and Extent of the Deep Biosphere
journal, January 2013

  • Colwell, F. S.; D'Hondt, S.
  • Reviews in Mineralogy and Geochemistry, Vol. 75, Issue 1
  • DOI: 10.2138/rmg.2013.75.17

Extensive regional atmospheric hydrocarbon pollution in the southwestern United States
journal, October 2003

  • Katzenstein, A. S.; Doezema, L. A.; Simpson, I. J.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 21
  • DOI: 10.1073/pnas.1635258100

Genes encoding the candidate enzyme for anaerobic activation of n-alkanes in the denitrifying bacterium, strain HxN1
journal, February 2008


An Improved General Amino Acid Replacement Matrix
journal, April 2008


Unravelling the impact of hydrocarbon structure on the fumarate addition mechanism – a gas-phase ab initio study
journal, January 2015

  • Bharadwaj, Vivek S.; Vyas, Shubham; Villano, Stephanie M.
  • Physical Chemistry Chemical Physics, Vol. 17, Issue 6
  • DOI: 10.1039/C4CP04317K

Quantifying carbon sources in the formation of authigenic carbonates at gas hydrate sites in the Gulf of Mexico
journal, May 2004


Microbial Communities in Methane- and Short Chain Alkane-Rich Hydrothermal Sediments of Guaymas Basin
journal, January 2016


Obligate oil-degrading marine bacteria
journal, June 2007

  • Yakimov, Michail M.; Timmis, Kenneth N.; Golyshin, Peter N.
  • Current Opinion in Biotechnology, Vol. 18, Issue 3
  • DOI: 10.1016/j.copbio.2007.04.006

Microbial Ecology of the Dark Ocean above, at, and below the Seafloor
journal, June 2011

  • Orcutt, B. N.; Sylvan, J. B.; Knab, N. J.
  • Microbiology and Molecular Biology Reviews, Vol. 75, Issue 2
  • DOI: 10.1128/MMBR.00039-10

Molecular survey of sulphate-reducing bacteria in the deep-sea sediments of the west Pacific Warm Pool
journal, July 2008

  • Wang, Peng; Xiao, Xiang; Zhang, Haiyan
  • Journal of Ocean University of China, Vol. 7, Issue 3
  • DOI: 10.1007/s11802-008-0269-9

Biocorrosive Thermophilic Microbial Communities in Alaskan North Slope Oil Facilities
journal, October 2009

  • Duncan, Kathleen E.; Gieg, Lisa M.; Parisi, Victoria A.
  • Environmental Science & Technology, Vol. 43, Issue 20
  • DOI: 10.1021/es9013932

Ubiquitous Presence and Novel Diversity of Anaerobic Alkane Degraders in Cold Marine Sediments
journal, December 2015


Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria
journal, September 2007

  • Kniemeyer, Olaf; Musat, Florin; Sievert, Stefan M.
  • Nature, Vol. 449, Issue 7164
  • DOI: 10.1038/nature06200

Identification of Novel Methane-, Ethane-, and Propane-Oxidizing Bacteria at Marine Hydrocarbon Seeps by Stable Isotope Probing
journal, July 2010

  • Redmond, M. C.; Valentine, D. L.; Sessions, A. L.
  • Applied and Environmental Microbiology, Vol. 76, Issue 19
  • DOI: 10.1128/AEM.00271-10

Anaerobic alkane-degrading strain AK-01 contains two alkylsuccinate synthase genes
journal, February 2008

  • Callaghan, Amy V.; Wawrik, Boris; Ní Chadhain, Sinéad M.
  • Biochemical and Biophysical Research Communications, Vol. 366, Issue 1
  • DOI: 10.1016/j.bbrc.2007.11.094

Microbiological investigation of methane- and hydrocarbon-discharging mud volcanoes in the Carpathian Mountains, Romania
journal, April 2006


Anaerobic oxidation of short-chain alkanes in hydrothermal sediments: potential influences on sulfur cycling and microbial diversity
journal, January 2013

  • Adams, Melissa M.; Hoarfrost, Adrienne L.; Bose, Arpita
  • Frontiers in Microbiology, Vol. 4
  • DOI: 10.3389/fmicb.2013.00110

Microbial communities involved in anaerobic degradation of alkanes
journal, January 2011

  • Mbadinga, Serge Maurice; Wang, Li-Ying; Zhou, Lei
  • International Biodeterioration & Biodegradation, Vol. 65, Issue 1
  • DOI: 10.1016/j.ibiod.2010.11.009

Anaerobic Oxidation of n-Dodecane by an Addition Reaction in a Sulfate-Reducing Bacterial Enrichment Culture
journal, December 2000


Diversity of Benzyl- and Alkylsuccinate Synthase Genes in Hydrocarbon-Impacted Environments and Enrichment Cultures
journal, October 2010

  • Callaghan, Amy V.; Davidova, Irene A.; Savage-Ashlock, Kristen
  • Environmental Science & Technology, Vol. 44, Issue 19
  • DOI: 10.1021/es1002023

Methane formation from long-chain alkanes by anaerobic microorganisms
journal, September 1999

  • Zengler, Karsten; Richnow, Hans H.; Rosselló-Mora, Ramon
  • Nature, Vol. 401, Issue 6750
  • DOI: 10.1038/45777

Three-dimensional model synthesis of the global methane cycle
journal, January 1991

  • Fung, I.; John, J.; Lerner, J.
  • Journal of Geophysical Research, Vol. 96, Issue D7
  • DOI: 10.1029/91JD01247

Methanogenesis, sulfate reduction and crude oil biodegradation in hot Alaskan oilfields: Methanogenic crude oil biodegradation in hot oilfields
journal, November 2010


Enhanced Gene Detection Assays for Fumarate-Adding Enzymes Allow Uncovering of Anaerobic Hydrocarbon Degraders in Terrestrial and Marine Systems
journal, November 2012

  • von Netzer, Frederick; Pilloni, Giovanni; Kleindienst, Sara
  • Applied and Environmental Microbiology, Vol. 79, Issue 2
  • DOI: 10.1128/AEM.02362-12

Impact of natural oil and higher hydrocarbons on microbial diversity, distribution, and activity in Gulf of Mexico cold-seep sediments
journal, November 2010

  • Orcutt, Beth N.; Joye, Samantha B.; Kleindienst, Sara
  • Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 57, Issue 21-23
  • DOI: 10.1016/j.dsr2.2010.05.014

Formation of n-alkane- and cycloalkane-derived organic acids during anaerobic growth of a denitrifying bacterium with crude oil
journal, September 2003


Diverse sulfate-reducing bacteria of the Desulfosarcina/Desulfococcus clade are the key alkane degraders at marine seeps
journal, April 2014

  • Kleindienst, Sara; Herbst, Florian-Alexander; Stagars, Marion
  • The ISME Journal, Vol. 8, Issue 10
  • DOI: 10.1038/ismej.2014.51

Anaerobic Oxidation of Methane: Progress with an Unknown Process
journal, October 2009


Carbon and hydrogen isotope fractionation associated with the aerobic microbial oxidation of methane, ethane, propane and butane
journal, January 2007

  • Kinnaman, Franklin S.; Valentine, David L.; Tyler, Stanley C.
  • Geochimica et Cosmochimica Acta, Vol. 71, Issue 2
  • DOI: 10.1016/j.gca.2006.09.007

Global distribution of microbial abundance and biomass in subseafloor sediment
journal, August 2012

  • Kallmeyer, J.; Pockalny, R.; Adhikari, R. R.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 40
  • DOI: 10.1073/pnas.1203849109

Oceanic Methane Biogeochemistry
journal, February 2007


Anaerobic degradation of propane and butane by sulfate-reducing bacteria enriched from marine hydrocarbon cold seeps
journal, December 2012


Natural seabed gas seeps as sources of atmospheric methane
journal, June 2004


Bacterial methane oxidation in sea-floor gas hydrate: Significance to life in extreme environments
journal, January 1998


Enzymes involved in the anaerobic oxidation of n-alkanes: from methane to long-chain paraffins
journal, January 2013


Desulfotomaculum spp. and related gram-positive sulfate-reducing bacteria in deep subsurface environments
journal, January 2013

  • Aüllo, Thomas; Ranchou-Peyruse, Anthony; Ollivier, Bernard
  • Frontiers in Microbiology, Vol. 4
  • DOI: 10.3389/fmicb.2013.00362

Biological formation of ethane and propane in the deep marine subsurface
journal, September 2006

  • Hinrichs, K. -U.; Hayes, J. M.; Bach, W.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 40
  • DOI: 10.1073/pnas.0606535103

Using Natural Abundance Radiocarbon To Trace the Flux of Petrocarbon to the Seafloor Following the Deepwater Horizon Oil Spill
journal, December 2014

  • Chanton, Jeffrey; Zhao, Tingting; Rosenheim, Brad E.
  • Environmental Science & Technology, Vol. 49, Issue 2
  • DOI: 10.1021/es5046524

Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage
journal, July 2013

  • Haroon, Mohamed F.; Hu, Shihu; Shi, Ying
  • Nature, Vol. 500, Issue 7464
  • DOI: 10.1038/nature12375

The anaerobic degradation of gaseous, nonmethane alkanes — From in situ processes to microorganisms
journal, January 2015


Evidence that crude oil alkane activation proceeds by different mechanisms under sulfate-reducing and methanogenic conditions
journal, May 2013


High Diversity of Anaerobic Alkane-Degrading Microbial Communities in Marine Seep Sediments Based on (1-methylalkyl)succinate Synthase Genes
journal, January 2016


Anaerobic bacterial metabolism of hydrocarbons
journal, December 1998


Metagenomic analysis and metabolite profiling of deep–sea sediments from the Gulf of Mexico following the Deepwater Horizon oil spill
journal, January 2013


Thermophilic archaea activate butane via alkyl-coenzyme M formation
journal, October 2016

  • Laso-Pérez, Rafael; Wegener, Gunter; Knittel, Katrin
  • Nature, Vol. 539, Issue 7629
  • DOI: 10.1038/nature20152

Degradation of alkanes by bacteria
journal, October 2009


MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016

  • Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
  • Molecular Biology and Evolution, Vol. 33, Issue 7
  • DOI: 10.1093/molbev/msw054

Earth's Degassing: A Missing Ethane and Propane Source
journal, January 2009


Field and laboratory studies on the bioconversion of coal to methane in the San Juan Basin
journal, January 2012


Anaerobic activation of toluene and o-xylene by addition to fumarate in denitrifying strain T.
journal, February 1997


Observed and simulated global distribution and budget of atmospheric C 2 -C 5 alkanes
journal, January 2010

  • Pozzer, A.; Pollmann, J.; Taraborrelli, D.
  • Atmospheric Chemistry and Physics, Vol. 10, Issue 9
  • DOI: 10.5194/acp-10-4403-2010

Weak coupling between sulfate reduction and the anaerobic oxidation of methane in methane-rich seafloor sediments during ex situ incubation
journal, January 2011

  • Bowles, Marshall W.; Samarkin, Vladimir A.; Bowles, Kathy M.
  • Geochimica et Cosmochimica Acta, Vol. 75, Issue 2
  • DOI: 10.1016/j.gca.2010.09.043

In situ detection of anaerobic alkane metabolites in subsurface environments
journal, January 2013


Mineralization of organic matter in the sea bed—the role of sulphate reduction
journal, April 1982


Growth of Pseudomonas chloritidismutans AW-1T on n-alkanes with chlorate as electron acceptor
journal, April 2009

  • Mehboob, Farrakh; Junca, Howard; Schraa, Gosse
  • Applied Microbiology and Biotechnology, Vol. 83, Issue 4
  • DOI: 10.1007/s00253-009-1985-9

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