Subsurface hydrocarbon degradation strategies in low- and high-sulfate coal seam communities identified with activity-based metagenomics

Schweitzer, Hannah D.; Smith, Heidi J.; Barnhart, Elliott P.; McKay, Luke J.; Gerlach, Robin; Cunningham, Alfred B.; Malmstrom, Rex R.; Goudeau, Danielle; Fields, Matthew W.

doi:10.1038/s41522-022-00267-2

Title: Subsurface hydrocarbon degradation strategies in low- and high-sulfate coal seam communities identified with activity-based metagenomics

Journal Article · 16 February 2022 · npj Biofilms and Microbiomes

DOI: https://doi.org/10.1038/s41522-022-00267-2 · OSTI ID:1865082

^[1];

^[1]; Barnhart, Elliott P. ^[2];

^[1];

^[1]; Cunningham, Alfred B. ^[1];

^[3];

^[1]

Montana State Univ., Bozeman, MT (United States)
Montana State Univ., Bozeman, MT (United States); US Geological Survey, Helena, MT (United States)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)

Environmentally relevant metagenomes and BONCAT-FACS derived translationally active metagenomes from Powder River Basin coal seams were investigated to elucidate potential genes and functional groups involved in hydrocarbon degradation to methane in coal seams with high- and low-sulfate levels. An advanced subsurface environmental sampler allowed the establishment of coal-associated microbial communities under in situ conditions for metagenomic analyses from environmental and translationally active populations. Metagenomic sequencing demonstrated that biosurfactants, aerobic dioxygenases, and anaerobic phenol degradation pathways were present in active populations across the sampled coal seams. In particular, results suggested the importance of anaerobic degradation pathways under high-sulfate conditions with an emphasis on fumarate addition. Under low-sulfate conditions, a mixture of both aerobic and anaerobic pathways was observed but with a predominance of aerobic dioxygenases. The putative low-molecular-weight biosurfactant, lichysein, appeared to play a more important role compared to rhamnolipids. The methods used in this study—subsurface environmental samplers in combination with metagenomic sequencing of both total and translationally active metagenomes—offer a deeper and environmentally relevant perspective on community genetic potential from coal seams poised at different redox conditions broadening the understanding of degradation strategies for subsurface carbon.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: National Science Foundation (NSF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1865082

Journal Information:: npj Biofilms and Microbiomes, Journal Name: npj Biofilms and Microbiomes Journal Issue: 1 Vol. 8; ISSN 2055-5008

Publisher:: Springer NatureCopyright Statement

Country of Publication:: United States

Language:: English

References (68)

Anaerobic metabolism of phenol in proteobacteria and further studies of phenylphosphate carboxylase Schmeling, Sirko; Fuchs, Georg Archives of Microbiology, Vol. 191, Issue 12 https://doi.org/10.1007/s00203-009-0519-2	journal	October 2009
Bacterial metabolism of long-chain n-alkanes Wentzel, Alexander; Ellingsen, Trond E.; Kotlar, Hans-Kristian Applied Microbiology and Biotechnology, Vol. 76, Issue 6 https://doi.org/10.1007/s00253-007-1119-1	journal	August 2007
Biotechnology and microbiology of coal degradation Fakoussa, R. M.; Hofrichter, M. Applied Microbiology and Biotechnology, Vol. 52, Issue 1 https://doi.org/10.1007/s002530051483	journal	July 1999
Biodegradation of petroleum sludge and petroleum polluted soil by a bacterial consortium: a laboratory study Gojgic-Cvijovic, G. D.; Milic, J. S.; Solevic, T. M. Biodegradation, Vol. 23, Issue 1 https://doi.org/10.1007/s10532-011-9481-1	journal	May 2011
Combined effects of DOM and biosurfactant enhanced biodegradation of polycylic armotic hydrocarbons (PAHs) in soil–water systems Yu, Hui; Huang, Guo-He; Xiao, Huining Environmental Science and Pollution Research, Vol. 21, Issue 17 https://doi.org/10.1007/s11356-014-2958-9	journal	May 2014
Characterization of Biosurfactant Produced by Bacillus licheniformis TT42 Having Potential for Enhanced Oil Recovery Suthar, Harish; Nerurkar, Anuradha Applied Biochemistry and Biotechnology, Vol. 180, Issue 2 https://doi.org/10.1007/s12010-016-2096-6	journal	April 2016
Evaluation of orange peel for biosurfactant production by Bacillus licheniformis and their ability to degrade naphthalene and crude oil Kumar, Arthala Praveen; Janardhan, Avilala; Viswanath, Buddolla 3 Biotech, Vol. 6, Issue 1 https://doi.org/10.1007/s13205-015-0362-x	journal	February 2016
Fast bioremediation of petroleum-contaminated soils by a consortium of biosurfactant/bioemulsifier producing bacteria Barin, R.; Talebi, M.; Biria, D. International Journal of Environmental Science and Technology, Vol. 11, Issue 6 https://doi.org/10.1007/s13762-014-0593-0	journal	May 2014
Coal induced production of a rhamnolipid biosurfactant by Pseudomonas stutzeri, isolated from the formation water of Jharia coalbed Singh, Durgesh Narain; Tripathi, Anil Kumar Bioresource Technology, Vol. 128 https://doi.org/10.1016/j.biortech.2012.10.127	journal	January 2013
Carbon mass balance, isotopic tracers of biogenic methane, and the role of acetate in coal beds: Powder River Basin (USA) Vinson, David S.; Blair, Neal E.; Ritter, Daniel J. Chemical Geology, Vol. 530 https://doi.org/10.1016/j.chemgeo.2019.119329	journal	December 2019
Active methanogenesis and acetate utilization in Powder River Basin coals, United States Ulrich, Glenn; Bower, Shane International Journal of Coal Geology, Vol. 76, Issue 1-2 https://doi.org/10.1016/j.coal.2008.03.006	journal	October 2008
Enhanced microbial coalbed methane generation: A review of research, commercial activity, and remaining challenges Ritter, Daniel; Vinson, David; Barnhart, Elliott International Journal of Coal Geology, Vol. 146 https://doi.org/10.1016/j.coal.2015.04.013	journal	July 2015
The effect of coal rank on biogenic methane potential and microbial composition Robbins, Steven J.; Evans, Paul N.; Esterle, Joan S. International Journal of Coal Geology, Vol. 154-155 https://doi.org/10.1016/j.coal.2016.01.001	journal	January 2016
Hydrogeochemistry and coal-associated bacterial populations from a methanogenic coal bed Barnhart, Elliott P.; Weeks, Edwin P.; Jones, Elizabeth J. P. International Journal of Coal Geology, Vol. 162 https://doi.org/10.1016/j.coal.2016.05.001	journal	May 2016
Anaerobic degradation of non-substituted aromatic hydrocarbons Meckenstock, Rainer U.; Mouttaki, Housna Current Opinion in Biotechnology, Vol. 22, Issue 3 https://doi.org/10.1016/j.copbio.2011.02.009	journal	June 2011
The role of surfactants in coal bio-solubilisation Yin, Sudong; Tao, Xiuxiang; Shi, Kaiyi Fuel Processing Technology, Vol. 92, Issue 8 https://doi.org/10.1016/j.fuproc.2011.03.019	journal	August 2011
Evidence that crude oil alkane activation proceeds by different mechanisms under sulfate-reducing and methanogenic conditions Aitken, C. M.; Jones, D. M.; Maguire, M. J. Geochimica et Cosmochimica Acta, Vol. 109 https://doi.org/10.1016/j.gca.2013.01.031	journal	May 2013
Changes in microbial communities and associated water and gas geochemistry across a sulfate gradient in coal beds: Powder River Basin, USA Schweitzer, Hannah; Ritter, Daniel; McIntosh, Jennifer Geochimica et Cosmochimica Acta, Vol. 245 https://doi.org/10.1016/j.gca.2018.11.009	journal	January 2019
Innovating carbon-capture biotechnologies through ecosystem-inspired solutions Schweitzer, Hannah; Aalto, Nerea J.; Busch, Wolfgang One Earth, Vol. 4, Issue 1 https://doi.org/10.1016/j.oneear.2020.12.006	journal	January 2021
Nonribosomal peptide synthetases: structures and dynamics Strieker, Matthias; Tanović, Alan; Marahiel, Mohamed A. Current Opinion in Structural Biology, Vol. 20, Issue 2, p. 234-240 https://doi.org/10.1016/j.sbi.2010.01.009	journal	April 2010
Genome-Resolved Metagenomics Is Essential for Unlocking the Microbial Black Box of the Soil Lemos, Leandro Nascimento; Mendes, Lucas William; Baldrian, Petr Trends in Microbiology, Vol. 29, Issue 4 https://doi.org/10.1016/j.tim.2021.01.013	journal	April 2021
Diversity of Benzyl- and Alkylsuccinate Synthase Genes in Hydrocarbon-Impacted Environments and Enrichment Cultures Callaghan, Amy V.; Davidova, Irene A.; Savage-Ashlock, Kristen Environmental Science & Technology, Vol. 44, Issue 19 https://doi.org/10.1021/es1002023	journal	October 2010
Metagenomics of Hydrocarbon Resource Environments Indicates Aerobic Taxa and Genes to be Unexpectedly Common An, Dongshan; Caffrey, Sean M.; Soh, Jung Environmental Science & Technology, Vol. 47, Issue 18 https://doi.org/10.1021/es4020184	journal	September 2013
The major volatile elements of the Earth: Their origin, behavior, and fate Javoy, M. Geophysical Research Letters, Vol. 24, Issue 2 https://doi.org/10.1029/96GL03931	journal	January 1997
Diverse sulfate-reducing bacteria of the Desulfosarcina/Desulfococcus clade are the key alkane degraders at marine seeps Kleindienst, Sara; Herbst, Florian-Alexander; Stagars, Marion The ISME Journal, Vol. 8, Issue 10 https://doi.org/10.1038/ismej.2014.51	journal	April 2014
Energy and carbon metabolisms in a deep terrestrial subsurface fluid microbial community Momper, Lily; Jungbluth, Sean P.; Lee, Michael D. The ISME Journal, Vol. 11, Issue 10 https://doi.org/10.1038/ismej.2017.94	journal	June 2017
Insights into the phylogeny and coding potential of microbial dark matter Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander Nature, Vol. 499, Issue 7459 https://doi.org/10.1038/nature12352	journal	July 2013
Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage Haroon, Mohamed F.; Hu, Shihu; Shi, Ying Nature, Vol. 500, Issue 7464 https://doi.org/10.1038/nature12375	journal	July 2013
The ecology and biotechnology of sulphate-reducing bacteria Muyzer, Gerard; Stams, Alfons J. M. Nature Reviews Microbiology, Vol. 6, Issue 6 https://doi.org/10.1038/nrmicro1892	journal	May 2008
Long-term succession in a coal seam microbiome during in situ biostimulation of coalbed-methane generation Beckmann, Sabrina; Luk, Alison W. S.; Gutierrez-Zamora, Maria-Luisa The ISME Journal, Vol. 13, Issue 3 https://doi.org/10.1038/s41396-018-0296-5	journal	October 2018
Activity-based, genome-resolved metagenomics uncovers key populations and pathways involved in subsurface conversions of coal to methane McKay, Luke J.; Smith, Heidi J.; Barnhart, Elliott P. The ISME Journal, Vol. 16, Issue 4 https://doi.org/10.1038/s41396-021-01139-x	journal	October 2021
Improved genome recovery and integrated cell-size analyses of individual uncultured microbial cells and viral particles Stepanauskas, Ramunas; Fergusson, Elizabeth A.; Brown, Joseph Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00128-z	journal	July 2017
Probing the active fraction of soil microbiomes using BONCAT-FACS Couradeau, Estelle; Sasse, Joelle; Goudeau, Danielle Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10542-0	journal	June 2019
Occurrence and expression of novel methyl-coenzyme M reductase gene (mcrA) variants in hot spring sediments McKay, Luke J.; Hatzenpichler, Roland; Inskeep, William P. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-07354-x	journal	August 2017
Anaerobic degradation of hexadecane and phenanthrene coupled to sulfate reduction by enriched consortia from northern Gulf of Mexico seafloor sediment Shin, Boryoung; Kim, Minjae; Zengler, Karsten Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-018-36567-x	journal	February 2019
Potential Role of Acetyl-CoA Synthetase (acs) and Malate Dehydrogenase (mae) in the Evolution of the Acetate Switch in Bacteria and Archaea Barnhart, Elliott P.; McClure, Marcella A.; Johnson, Kiki Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep12498	journal	August 2015
Ribosomal peptide natural products: bridging the ribosomal and nonribosomal worlds McIntosh, John A.; Donia, Mohamed S.; Schmidt, Eric W. Natural Product Reports, Vol. 26, Issue 4 https://doi.org/10.1039/b714132g	journal	January 2009
UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota Campbell, J. H.; O'Donoghue, P.; Campbell, A. G. Proceedings of the National Academy of Sciences, Vol. 110, Issue 14, p. 5540-5545 https://doi.org/10.1073/pnas.1303090110	journal	March 2013
Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia Hatzenpichler, Roland; Connon, Stephanie A.; Goudeau, Danielle Proceedings of the National Academy of Sciences, Vol. 113, Issue 28 https://doi.org/10.1073/pnas.1603757113	journal	June 2016
AromaDeg, a novel database for phylogenomics of aerobic bacterial degradation of aromatics Duarte, Márcia; Jauregui, Ruy; Vilchez-Vargas, Ramiro Database, Vol. 2014 https://doi.org/10.1093/database/bau118	journal	January 2014
Interrogation of Chesapeake Bay sediment microbial communities for intrinsic alkane-utilizing potential under anaerobic conditions Johnson, Jamie M.; Wawrik, Boris; Isom, Catherine FEMS Microbiology Ecology, Vol. 91, Issue 2 https://doi.org/10.1093/femsec/fiu035	journal	February 2015
Functional screening of a metagenomic library for genes involved in microbial degradation of aromatic compounds Suenaga, Hikaru; Ohnuki, Tsutomu; Miyazaki, Kentaro Environmental Microbiology, Vol. 9, Issue 9 https://doi.org/10.1111/j.1462-2920.2007.01342.x	journal	September 2007
Field and laboratory studies on the bioconversion of coal to methane in the San Juan Basin Wawrik, Boris; Mendivelso, Margarita; Parisi, Victoria A. FEMS Microbiology Ecology, Vol. 81, Issue 1 https://doi.org/10.1111/j.1574-6941.2011.01272.x	journal	January 2012
The bacterial degradation of benzoic acid and benzenoid compounds under anaerobic conditions: Unifying trends and new perspectives Elder, Douglas J. E.; Kelly, David J. FEMS Microbiology Reviews, Vol. 13, Issue 4 https://doi.org/10.1111/j.1574-6976.1994.tb00061.x	journal	April 1994
Heterologous production of Pseudomonas aeruginosa rhamnolipid under anaerobic conditions for microbial enhanced oil recovery Zhao, F.; Shi, R.; Zhao, J. Journal of Applied Microbiology, Vol. 118, Issue 2 https://doi.org/10.1111/jam.12698	journal	December 2014
Stimulation of Methane Generation from Nonproductive Coal by Addition of Nutrients or a Microbial Consortium Jones, E. J. P.; Voytek, M. A.; Corum, M. D. Applied and Environmental Microbiology, Vol. 76, Issue 21 https://doi.org/10.1128/AEM.00728-10	journal	September 2010
Phenol Degradation in the Strictly Anaerobic Iron-Reducing Bacterium Geobacter metallireducens GS-15 Schleinitz, Kathleen M.; Schmeling, Sirko; Jehmlich, Nico Applied and Environmental Microbiology, Vol. 75, Issue 12 https://doi.org/10.1128/AEM.01525-08	journal	April 2009
Enhanced Gene Detection Assays for Fumarate-Adding Enzymes Allow Uncovering of Anaerobic Hydrocarbon Degraders in Terrestrial and Marine Systems von Netzer, Frederick; Pilloni, Giovanni; Kleindienst, Sara Applied and Environmental Microbiology, Vol. 79, Issue 2 https://doi.org/10.1128/AEM.02362-12	journal	November 2012
Anaerobic Biodegradation of n -Hexadecane by a Nitrate-Reducing Consortium Callaghan, Amy V.; Tierney, Meghan; Phelps, Craig D. Applied and Environmental Microbiology, Vol. 75, Issue 5 https://doi.org/10.1128/AEM.02491-08	journal	March 2009
Comparison of Mechanisms of Alkane Metabolism under Sulfate-Reducing Conditions among Two Bacterial Isolates and a Bacterial Consortium Callaghan, A. V.; Gieg, L. M.; Kropp, K. G. Applied and Environmental Microbiology, Vol. 72, Issue 6 https://doi.org/10.1128/AEM.02896-05	journal	June 2006
Functional Metagenomics of a Biostimulated Petroleum-Contaminated Soil Reveals an Extraordinary Diversity of Extradiol Dioxygenases Terrón-González, Laura; Martín-Cabello, Guadalupe; Ferrer, Manuel Applied and Environmental Microbiology, Vol. 82, Issue 8 https://doi.org/10.1128/AEM.03811-15	journal	February 2016
Diversity of Benzylsuccinate Synthase-Like ( bssA ) Genes in Hydrocarbon-Polluted Marine Sediments Suggests Substrate-Dependent Clustering Acosta-González, Alejandro; Rosselló-Móra, Ramon; Marqués, Silvia Applied and Environmental Microbiology, Vol. 79, Issue 12 https://doi.org/10.1128/AEM.03934-12	journal	April 2013
Anaerobic Toluene Activation by Benzylsuccinate Synthase in a Highly Enriched Methanogenic Culture Beller, Harry R.; Edwards, Elizabeth A. Applied and Environmental Microbiology, Vol. 66, Issue 12 https://doi.org/10.1128/AEM.66.12.5503-5505.2000	journal	December 2000
Characterization and Description of Anaeromyxobacter dehalogenans gen. nov., sp. nov., an Aryl-Halorespiring Facultative Anaerobic Myxobacterium Sanford, R. A.; Cole, J. R.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 68, Issue 2 https://doi.org/10.1128/AEM.68.2.893-900.2002	journal	February 2002
The Surfactant of Legionella pneumophila Is Secreted in a TolC-Dependent Manner and Is Antagonistic toward Other Legionella Species Stewart, Catherine R.; Burnside, Denise M.; Cianciotto, Nicholas P. Journal of Bacteriology, Vol. 193, Issue 21 https://doi.org/10.1128/JB.05405-11	journal	November 2011
Kinetics of Acetate Utilization by Two Thermophilic Acetotrophic Methanogens: Methanosarcina sp. Strain CALS-1 and Methanothrix sp. Strain CALS-1 Min, Hang; Zinder, Stephen H. Applied and Environmental Microbiology, Vol. 55, Issue 2 https://doi.org/10.1128/aem.55.2.488-491.1989	journal	January 1989
Metagenomic analysis of an anaerobic alkane-degrading microbial culture: potential hydrocarbon-activating pathways and inferred roles of community members Tan, Boonfei; Dong, Xiaoli; Sensen, Christoph W. Genome, Vol. 56, Issue 10 https://doi.org/10.1139/gen-2013-0069	journal	October 2013
Biogeochemistry of Microbial Coal-Bed Methane Strąpoć, Dariusz; Mastalerz, Maria; Dawson, Katherine Annual Review of Earth and Planetary Sciences, Vol. 39, Issue 1 https://doi.org/10.1146/annurev-earth-040610-133343	journal	May 2011
Metabolism of Hydrocarbons in n-Alkane-Utilizing Anaerobic Bacteria Wilkes, Heinz; Buckel, Wolfgang; Golding, Bernard T. Journal of Molecular Microbiology and Biotechnology, Vol. 26, Issue 1-3 https://doi.org/10.1159/000442160	journal	January 2016
Comparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine Borrel, Guillaume; Parisot, Nicolas; Harris, Hugh MB BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-679	journal	January 2014
Enhanced biosurfactant production through cloning of three genes and role of esterase in biosurfactant release Sekhon, Kamaljeet; Khanna, Sunil; Cameotra, Swaranjit Microbial Cell Factories, Vol. 10, Issue 1 https://doi.org/10.1186/1475-2859-10-49	journal	January 2011
Could petroleum biodegradation be a joint achievement of aerobic and anaerobic microrganisms in deep sea reservoirs? da Cruz, Georgiana F.; de Vasconcellos, Suzan P.; Angolini, Célio FF AMB Express, Vol. 1, Issue 1 https://doi.org/10.1186/2191-0855-1-47	journal	December 2011
Anaerolineaceae and Methanosaeta turned to be the dominant microorganisms in alkanes-dependent methanogenic culture after long-term of incubation Liang, Bo; Wang, Li-Ying; Mbadinga, Serge Maurice AMB Express, Vol. 5, Issue 1 https://doi.org/10.1186/s13568-015-0117-4	journal	June 2015
Synthesis and Characterization of Anaerobic Degradation Biomarkers of n -Alkanes via Hydroxylation/Carboxylation Pathways Zhou, Jing; Bian, Xin-Yu; Zhou, Lei European Journal of Mass Spectrometry, Vol. 22, Issue 1 https://doi.org/10.1255/ejms.1402	journal	February 2016
Comparison of Synthetic Surfactants and Biosurfactants in Enhancing Biodegradation of Polycyclic Aromatic Hydrocarbons Makkar, Randhir S.; Rockne, Karl J. Environmental Toxicology and Chemistry, Vol. 22, Issue 10 https://doi.org/10.1897/02-472	journal	January 2003
Metabolic Flexibility of Sulfate-Reducing Bacteria Plugge, Caroline M.; Zhang, Weiwen; Scholten, Johannes C. M. Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00081	journal	January 2011
Conversion of crude oil to methane by a microbial consortium enriched from oil reservoir production waters Berdugo-Clavijo, Carolina; Gieg, Lisa M. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00197	journal	May 2014
Anaerolineaceae and Methanosaeta turned to be the dominant microorganisms in alkanes-dependent methanogenic culture after long-term of incubation Liang, Bo; Wang, Li-Ying; Mbadinga, Serge figshare https://doi.org/10.6084/m9.figshare.c.3609809.v1	collection	January 2015