Metabolic capability and in situ activity of microorganisms in an oil reservoir

Liu, Yi-Fan; Galzerani, Daniela Domingos; Mbadinga, Serge Maurice; Zaramela, Livia S.; Gu, Ji-Dong; Mu, Bo-Zhong; Zengler, Karsten

doi:10.1186/s40168-017-0392-1

Title: Metabolic capability and in situ activity of microorganisms in an oil reservoir

Journal Article · Fri Jan 05 00:00:00 EST 2018 · Microbiome

DOI:https://doi.org/10.1186/s40168-017-0392-1· OSTI ID:1510971

Liu, Yi-Fan ^[1]; Galzerani, Daniela Domingos ^[2]; Mbadinga, Serge Maurice ^[3]; Zaramela, Livia S. ^[2]; Gu, Ji-Dong ^[4]; Mu, Bo-Zhong ^[3]; Zengler, Karsten ^[5]

Chinese Academy of Sciences (CAS), Shanghai (China). Shanghai Inst. of Ceramics, Key Lab. for Bioreactor Engineering and Inst. of Applied Chemistry; Univ. of California, San Diego, CA (United States). Dept. of Pediatrics
Univ. of California, San Diego, CA (United States). Dept. of Pediatrics
Chinese Academy of Sciences (CAS), Shanghai (China). Shanghai Inst. of Ceramics, Key Lab. for Bioreactor Engineering and Inst. of Applied Chemistry; Shanghai Collaborative Innovation Center for Biomanufacturing Technology, Shanghai (China)
Univ. of Hong Kong (China). School of Biological Sciences
Univ. of California, San Diego, CA (United States). Dept. of Pediatrics and Center for Microbiome Innovation,

Background: Microorganisms have long been associated with oxic and anoxic degradation of hydrocarbons in oil reservoirs and oil production facilities. While we can readily determine the abundance of microorganisms in the reservoir and study their activity in the laboratory, it has been challenging to resolve what microbes are actively participating in crude oil degradation in situ and to gain insight into what metabolic pathways they deploy. Results: Here, we describe the metabolic potential and in situ activity of microbial communities obtained from the Jiangsu Oil Reservoir (China) by an integrated metagenomics and metatranscriptomics approach. Almost complete genome sequences obtained by differential binning highlight the distinct capability of different community members to degrade hydrocarbons under oxic or anoxic condition. Transcriptomic data delineate active members of the community and give insights that Acinetobacter species completely oxidize alkanes into carbon dioxide with the involvement of oxygen, and Archaeoglobus species mainly ferment alkanes to generate acetate which could be consumed by Methanosaeta species. Furthermore, nutritional requirements based on amino acid and vitamin auxotrophies suggest a complex network of interactions and dependencies among active community members that go beyond classical syntrophic exchanges; this network defines community composition and microbial ecology in oil reservoirs undergoing secondary recovery. Conclusion: Our data expand current knowledge of the metabolic potential and role in hydrocarbon metabolism of individual members of thermophilic microbial communities from an oil reservoir. The study also reveals potential metabolic exchanges based on vitamin and amino acid auxotrophies indicating the presence of complex network of interactions between microbial taxa within the community.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Univ. of California, San Diego, CA (United States)

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

Grant/Contract Number:: SC0012586

OSTI ID:: 1510971

Journal Information:: Microbiome, Vol. 6, Issue 1; ISSN 2049-2618

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 55 works

Citation information provided by
Web of Science

References (61)

Networks of energetic and metabolic interactions define dynamics in microbial communities Embree, Mallory; Liu, Joanne K.; Al-Bassam, Mahmoud M. Proceedings of the National Academy of Sciences, Vol. 112, Issue 50 https://doi.org/10.1073/pnas.1506034112	journal	November 2015
AliView: a fast and lightweight alignment viewer and editor for large datasets Larsson, Anders Bioinformatics, Vol. 30, Issue 22 https://doi.org/10.1093/bioinformatics/btu531	journal	August 2014
Quality control and preprocessing of metagenomic datasets Schmieder, R.; Edwards, R. Bioinformatics, Vol. 27, Issue 6 https://doi.org/10.1093/bioinformatics/btr026	journal	January 2011
Single-cell genome and metatranscriptome sequencing reveal metabolic interactions of an alkane-degrading methanogenic community Embree, Mallory; Nagarajan, Harish; Movahedi, Narjes The ISME Journal, Vol. 8, Issue 4 https://doi.org/10.1038/ismej.2013.187	journal	October 2013
Thermodynamic constraints on methanogenic crude oil biodegradation Dolfing, Jan; Larter, Stephen R.; Head, Ian M. The ISME Journal, Vol. 2, Issue 4 https://doi.org/10.1038/ismej.2007.111	journal	December 2007
A protein trisulfide couples dissimilatory sulfate reduction to energy conservation Santos, A. A.; Venceslau, S. S.; Grein, F. Science, Vol. 350, Issue 6267 https://doi.org/10.1126/science.aad3558	journal	December 2015
Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria Baker, Brett J.; Lazar, Cassandre Sara; Teske, Andreas P. Microbiome, Vol. 3, Issue 1 https://doi.org/10.1186/s40168-015-0077-6	journal	April 2015
Identification of ribosomal RNA genes in metagenomic fragments Huang, Ying; Gilna, Paul; Li, Weizhong Bioinformatics, Vol. 25, Issue 10 https://doi.org/10.1093/bioinformatics/btp161	journal	April 2009
Biocorrosive Thermophilic Microbial Communities in Alaskan North Slope Oil Facilities Duncan, Kathleen E.; Gieg, Lisa M.; Parisi, Victoria A. Environmental Science & Technology, Vol. 43, Issue 20 https://doi.org/10.1021/es9013932	journal	October 2009
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
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
Anaerobic alkane-degrading strain AK-01 contains two alkylsuccinate synthase genes Callaghan, Amy V.; Wawrik, Boris; Ní Chadhain, Sinéad M. Biochemical and Biophysical Research Communications, Vol. 366, Issue 1 https://doi.org/10.1016/j.bbrc.2007.11.094	journal	February 2008
EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data Miller, Christopher S.; Baker, Brett J.; Thomas, Brian C. Genome Biology, Vol. 12, Issue 5 https://doi.org/10.1186/gb-2011-12-5-r44	journal	May 2011
Anaerobic hydrocarbon biodegradation in deep subsurface oil reservoirs Aitken, Carolyn M.; Jones, D. M.; Larter, S. R. Nature, Vol. 431, Issue 7006 https://doi.org/10.1038/nature02922	journal	September 2004
Growth- and substrate-dependent transcription of formate dehydrogenase and hydrogenase coding genes in Syntrophobacter fumaroxidans and Methanospirillum hungatei Worm, P.; Stams, A. J. M.; Cheng, X. Microbiology, Vol. 157, Issue 1 https://doi.org/10.1099/mic.0.043927-0	journal	September 2010
Anaerobic Biodegradation of Aromatic Hydrocarbons: Pathways and Prospects Foght, Julia Journal of Molecular Microbiology and Biotechnology, Vol. 15, Issue 2-3 https://doi.org/10.1159/000121324	journal	January 2008
CD-HIT: accelerated for clustering the next-generation sequencing data Fu, Limin; Niu, Beifang; Zhu, Zhengwei Bioinformatics, Vol. 28, Issue 23 https://doi.org/10.1093/bioinformatics/bts565	journal	October 2012
Streaming fragment assignment for real-time analysis of sequencing experiments Roberts, Adam; Pachter, Lior Nature Methods, Vol. 10, Issue 1 https://doi.org/10.1038/nmeth.2251	journal	November 2012
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Vitamin and Amino Acid Auxotrophy in Anaerobic Consortia Operating under Methanogenic Conditions Hubalek, Valerie; Buck, Moritz; Tan, BoonFei mSystems, Vol. 2, Issue 5 https://doi.org/10.1128/mSystems.00038-17	journal	October 2017
DECIPHER, a Search-Based Approach to Chimera Identification for 16S rRNA Sequences Wright, Erik S.; Yilmaz, L. Safak; Noguera, Daniel R. Applied and Environmental Microbiology, Vol. 78, Issue 3 https://doi.org/10.1128/AEM.06516-11	journal	November 2011
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes Segata, Nicola; Börnigen, Daniela; Morgan, Xochitl C. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3304	journal	August 2013
Ribosomal Database Project: data and tools for high throughput rRNA analysis Cole, James R.; Wang, Qiong; Fish, Jordan A. Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1244	journal	November 2013
Methane formation from long-chain alkanes by anaerobic microorganisms Zengler, Karsten; Richnow, Hans H.; Rosselló-Mora, Ramon Nature, Vol. 401, Issue 6750 https://doi.org/10.1038/45777	journal	September 1999
Insights into the Anaerobic Biodegradation Pathway of n-Alkanes in Oil Reservoirs by Detection of Signature Metabolites Bian, Xin-Yu; Maurice Mbadinga, Serge; Liu, Yi-Fan Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep09801	journal	May 2015
KEGG: Kyoto Encyclopedia of Genes and Genomes Ogata, H.; Goto, S.; Sato, K. Nucleic Acids Research, Vol. 27, Issue 1 https://doi.org/10.1093/nar/27.1.29	journal	January 1999
Novel Type of ADP-Forming Acetyl Coenzyme A Synthetase in Hyperthermophilic Archaea: Heterologous Expression and Characterization of Isoenzymes from the Sulfate Reducer Archaeoglobus fulgidus and the Methanogen Methanococcus jannaschii Musfeldt, M.; Schonheit, P. Journal of Bacteriology, Vol. 184, Issue 3 https://doi.org/10.1128/JB.184.3.636-644.2002	journal	February 2002
Reconstructing metabolic pathways of hydrocarbon-degrading bacteria from the Deepwater Horizon oil spill Dombrowski, Nina; Donaho, John A.; Gutierrez, Tony Nature Microbiology, Vol. 1, Issue 7 https://doi.org/10.1038/nmicrobiol.2016.57	journal	May 2016
The RAST Server: Rapid Annotations using Subsystems Technology Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A. BMC Genomics, Vol. 9, Issue 1, Article No. 75 https://doi.org/10.1186/1471-2164-9-75	journal	January 2008
Comparative analysis of metagenomes from three methanogenic hydrocarbon-degrading enrichment cultures with 41 environmental samples Tan, Boonfei; Jane Fowler, S.; Laban, Nidal Abu The ISME Journal, Vol. 9, Issue 9 https://doi.org/10.1038/ismej.2015.22	journal	March 2015
Biological activity in the deep subsurface and the origin of heavy oil Head, Ian M.; Jones, D. Martin; Larter, Steve R. Nature, Vol. 426, Issue 6964 https://doi.org/10.1038/nature02134	journal	November 2003
Anaerobic oxidation of long-chain n-alkanes by the hyperthermophilic sulfate-reducing archaeon, Archaeoglobus fulgidus Khelifi, Nadia; Amin Ali, Oulfat; Roche, Philippe The ISME Journal, Vol. 8, Issue 11 https://doi.org/10.1038/ismej.2014.58	journal	April 2014
Nonpareil: a redundancy-based approach to assess the level of coverage in metagenomic datasets Rodriguez-R, Luis M.; Konstantinidis, Konstantinos T. Bioinformatics, Vol. 30, Issue 5 https://doi.org/10.1093/bioinformatics/btt584	journal	October 2013
Microbial communities in bulk fluids and biofilms of an oil facility have similar composition but different structure: Microbial communities in produced water and biofilms Stevenson, Bradley S.; Drilling, Heather S.; Lawson, Paul A. Environmental Microbiology, Vol. 13, Issue 4 https://doi.org/10.1111/j.1462-2920.2010.02413.x	journal	January 2011
Stereochemical Investigations Reveal the Mechanism of the Bacterial Activation of n-Alkanes without Oxygen Jarling, René; Sadeghi, Masih; Drozdowska, Marta Angewandte Chemie International Edition, Vol. 51, Issue 6 https://doi.org/10.1002/anie.201106055	journal	November 2011
A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane Rotaru, Amelia-Elena; Shrestha, Pravin Malla; Liu, Fanghua Energy Environ. Sci., Vol. 7, Issue 1 https://doi.org/10.1039/C3EE42189A	journal	January 2014
The genome sequence of Desulfatibacillum alkenivorans AK-01: a blueprint for anaerobic alkane oxidation: Genome sequence of Desulfatibacillum alkenivorans AK-01 Callaghan, A. V.; Morris, B. E. L.; Pereira, I. A. C. Environmental Microbiology, Vol. 14, Issue 1 https://doi.org/10.1111/j.1462-2920.2011.02516.x	journal	June 2011
Anaerobic bacterial metabolism of hydrocarbons Heider, Johann; Spormann, Alfred M.; Beller, Harry R. FEMS Microbiology Reviews, Vol. 22, Issue 5 https://doi.org/10.1111/j.1574-6976.1998.tb00381.x	journal	December 1998
Identification of a novel Baeyer-Villiger monooxygenase from Acinetobacter radioresistens : close relationship to the Mycobacterium tuberculosis prodrug activator EtaA : A new BVMO from Minerdi, Daniela; Zgrablic, Ivan; Sadeghi, Sheila J. Microbial Biotechnology, Vol. 5, Issue 6 https://doi.org/10.1111/j.1751-7915.2012.00356.x	journal	August 2012
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Hydrocarbon-degrading bacteria enriched by the Deepwater Horizon oil spill identified by cultivation and DNA-SIP Gutierrez, Tony; Singleton, David R.; Berry, David The ISME Journal, Vol. 7, Issue 11 https://doi.org/10.1038/ismej.2013.98	journal	June 2013
Spatial isolation and environmental factors drive distinct bacterial and archaeal communities in different types of petroleum reservoirs in China Gao, Peike; Tian, Huimei; Wang, Yansen Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep20174	journal	February 2016
Archaeoglobus fulgidus couples CO oxidation to sulfate reduction and acetogenesis with transient formate accumulation : The CO metabolism of Henstra, Anne M.; Dijkema, Cor; Stams, Alfons J. M. Environmental Microbiology, Vol. 9, Issue 7 https://doi.org/10.1111/j.1462-2920.2007.01306.x	journal	April 2007
metaxa 2: improved identification and taxonomic classification of small and large subunit rRNA in metagenomic data Bengtsson-Palme, Johan; Hartmann, Martin; Eriksson, Karl Martin Molecular Ecology Resources, Vol. 15, Issue 6 https://doi.org/10.1111/1755-0998.12399	journal	March 2015
Comparison of bacterial community in aqueous and oil phases of water-flooded petroleum reservoirs using pyrosequencing and clone library approaches Wang, Li-Ying; Ke, Wen-Ji; Sun, Xiao-Bo Applied Microbiology and Biotechnology, Vol. 98, Issue 9 https://doi.org/10.1007/s00253-013-5472-y	journal	January 2014
GroopM: an automated tool for the recovery of population genomes from related metagenomes Imelfort, Michael; Parks, Donovan; Woodcroft, Ben J. PeerJ, Vol. 2 https://doi.org/10.7717/peerj.603	journal	January 2014
The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes Meyer, F.; Paarmann, D.; D'Souza, M. BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-386	journal	September 2008
The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus Klenk, Hans-Peter; Clayton, Rebecca A.; Tomb, Jean-Francois Nature, Vol. 390, Issue 6658 https://doi.org/10.1038/37052	journal	November 1997
Metagenomic microbial community profiling using unique clade-specific marker genes Segata, Nicola; Waldron, Levi; Ballarini, Annalisa Nature Methods, Vol. 9, Issue 8 https://doi.org/10.1038/nmeth.2066	journal	June 2012
Growth of Pseudomonas chloritidismutans AW-1T on n-alkanes with chlorate as electron acceptor Mehboob, Farrakh; Junca, Howard; Schraa, Gosse Applied Microbiology and Biotechnology, Vol. 83, Issue 4 https://doi.org/10.1007/s00253-009-1985-9	journal	April 2009
Profile hidden Markov models Eddy, S. R. Bioinformatics, Vol. 14, Issue 9 https://doi.org/10.1093/bioinformatics/14.9.755	journal	October 1998
Alkane Hydroxylase from Acinetobactersp. Strain ADP1 Is Encoded by alkM and Belongs to a New Family of Bacterial Integral-Membrane Hydrocarbon Hydroxylases Ratajczak, Andreas; Geißdörfer, Walter; Hillen, Wolfgang Applied and Environmental Microbiology, Vol. 64, Issue 4 https://doi.org/10.1128/AEM.64.4.1175-1179.1998	journal	April 1998
Diversity of Sea Star-Associated Densoviruses and Transcribed Endogenous Viral Elements of Densovirus Origin Jackson, Elliot W.; Wilhelm, Roland C.; Johnson, Mitchell R. Journal of Virology, Vol. 95, Issue 1 https://doi.org/10.1128/jvi.01594-20	journal	December 2020
Hydrocarbon-degrading bacteria enriched by the Deepwater Horizon oil spill identified by cultivation and DNA-SIP David, Berry,; D., Aitken, Michael; Tony, Gutierrez, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/4p5s-2q50	text	January 2013
Salinimonas marina sp. nov. Isolated from Jeju Island Marine Sediment Kim, Minji; Lee, Ki-Eun; Cha, In-Tae Current Microbiology, Vol. 78, Issue 8 https://doi.org/10.1007/s00284-021-02576-9	journal	June 2021
Tritagonist as a new term for uncharacterised microorganisms in environmental systems Freimoser, Florian M.; Pelludat, Cosima; Remus-Emsermann, Mitja N. P. The ISME Journal, Vol. 10, Issue 1 https://doi.org/10.1038/ismej.2015.92	journal	June 2015
Characterizing the molecular regulation of inhibitory immune checkpoints with multimodal single-cell screens Papalexi, Efthymia; Mimitou, Eleni P.; Butler, Andrew W. Nature Genetics, Vol. 53, Issue 3 https://doi.org/10.1038/s41588-021-00778-2	journal	March 2021
The Genes rubA and rubB for Alkane Degradation in Acinetobacter sp. Strain ADP1 Are in an Operon with estB, Encoding an Esterase, andoxyR Geißdörfer, Walter; Kok, Ruben G.; Ratajczak, Andreas Journal of Bacteriology, Vol. 181, Issue 14 https://doi.org/10.1128/jb.181.14.4292-4298.1999	journal	July 1999
Comparative Genetic Diversity of Pseudomonas stutzeri Genomovars, Clonal Structure, and Phylogeny of the Species Cladera, A. M.; Bennasar, A.; Barcelo, M. Journal of Bacteriology, Vol. 186, Issue 16 https://doi.org/10.1128/jb.186.16.5239-5248.2004	journal	August 2004
Commentary: Microbial Small Talk: Volatiles in Fungal–Bacterial Interactions Hacquard, Stéphane Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00001	journal	January 2017

Cited By (11)

Developing an l‐ threonine‐producing strain from wild‐type Escherichia coli by modifying the glucose uptake, glyoxylate shunt, and l ‐threonine biosynthetic pathway Zhu, Lifei; Fang, Yu; Ding, Zhixiang Biotechnology and Applied Biochemistry, Vol. 66, Issue 6 https://doi.org/10.1002/bab.1813	journal	September 2019
Microaerobic conditions caused the overwhelming dominance of Acinetobacter spp. and the marginalization of Rhodococcus spp. in diesel fuel/crude oil mixture-amended enrichment cultures Révész, Fruzsina; Figueroa-Gonzalez, Perla Abigail; Probst, Alexander J. Archives of Microbiology, Vol. 202, Issue 2 https://doi.org/10.1007/s00203-019-01749-2	journal	October 2019
Metabolic potential of uncultured bacteria and archaea associated with petroleum seepage in deep-sea sediments Dong, Xiyang; Greening, Chris; Rattray, Jayne E. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-09747-0	journal	April 2019
Aerobic microbial taxa dominate deep subsurface cores from the Alberta oil sands Ridley, Christina M.; Voordouw, Gerrit FEMS Microbiology Ecology, Vol. 94, Issue 6 https://doi.org/10.1093/femsec/fiy073	journal	April 2018
Novel energy conservation strategies and behaviour of Pelotomaculum schinkii driving syntrophic propionate catabolism Hidalgo‐Ahumada, Catalina A. P.; Nobu, Masaru K.; Narihiro, Takashi Environmental Microbiology, Vol. 20, Issue 12 https://doi.org/10.1111/1462-2920.14388	journal	October 2018
Characteristics of crude oil-degrading bacteria Gordonia iterans isolated from marine coastal in Taean sediment Kim, Hyun-Sook; Dong, Ke; Kim, Jinsoo MicrobiologyOpen, Vol. 8, Issue 6 https://doi.org/10.1002/mbo3.754	journal	October 2018
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
The social network of microorganisms — how auxotrophies shape complex communities Zengler, Karsten; Zaramela, Livia S. Nature Reviews Microbiology, Vol. 16, Issue 6 https://doi.org/10.1038/s41579-018-0004-5	journal	March 2018
Oil reservoirs, an exceptional habitat for microorganisms Pannekens, Mark; Kroll, Lisa; Müller, Hubert New Biotechnology, Vol. 49 https://doi.org/10.1016/j.nbt.2018.11.006	journal	March 2019
Anaerobic hydrocarbon degradation in candidate phylum ‘Atribacteria’ (JS1) inferred from genomics Liu, Yi-Fan; Qi, Zhen-Zhen; Shou, Li-Bin The ISME Journal, Vol. 13, Issue 9 https://doi.org/10.1038/s41396-019-0448-2	journal	June 2019
Composition of Bacterial and Archaeal Communities in an Alkali-Surfactant-Polyacrylamide-Flooded Oil Reservoir and the Responses of Microcosms to Nutrients Gao, Peike; Li, Yu; Tan, Lijie Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02197	journal	September 2019

Linked Research (30)

Figures / Tables (5)

Similar Records

Ecophysiology of an uncultivated lineage of Aigarchaeota from an oxic, hot spring filamentous ‘streamer’ community

Journal Article · Fri Jul 03 00:00:00 EDT 2015 · The ISME Journal · OSTI ID:1510971

Beam, Jacob P.; Jay, Zackary J.; Schmid, Markus C.; +7 more

The social network of microorganisms — how auxotrophies shape complex communities

Journal Article · Thu Mar 29 00:00:00 EDT 2018 · Nature Reviews Microbiology · OSTI ID:1510971

Zengler, Karsten; Zaramela, Livia S.

Genome-Resolved Metagenomic Analysis Reveals Roles for Candidate Phyla and Other Microbial Community Members in Biogeochemical Transformations in Oil Reservoirs

Journal Article · Tue Jan 19 00:00:00 EST 2016 · mBio (Online) · OSTI ID:1510971

Hu, Ping; Tom, Lauren; Singh, Andrea; +5 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Auxotrophy
Hydrocarbon degradation
Metagenomics and metatranscriptomics
Microbial community
Oil reservoir

Additional file 10: Table S7. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765178 The current record is supplemented by this text	text	January 2018
Additional file 10: Table S7. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765178.v1 The current record is supplemented by this text	text	January 2018
Additional file 11: Figure S4. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765193.v1 The current record is supplemented by this image	image	January 2018
Additional file 12: Table S8. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765202 The current record is supplemented by this text	text	January 2018
Additional file 13: Text S1. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765217 The current record is supplemented by this text	text	January 2018
Additional file 13: Text S1. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765217.v1 The current record is supplemented by this text	text	January 2018
Additional file 14: Text S2. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765235 The current record is supplemented by this text	text	January 2018
Additional file 2: Table S2. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765259 The current record is supplemented by this text	text	January 2018
Additional file 3: Table S3. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765271 The current record is supplemented by this text	text	January 2018
Additional file 3: Table S3. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765271.v1 The current record is supplemented by this text	text	January 2018
Additional file 4: Table S4. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765280.v1 The current record is supplemented by this dataset	dataset	January 2018
Additional file 5: Table S5. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765289.v1 The current record is supplemented by this text	text	January 2018
Additional file 6: Figure S1. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765292.v1 The current record is supplemented by this image	image	January 2018
Additional file 7: Figure S2. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765298.v1 The current record is supplemented by this image	image	January 2018
Additional file 8: Table S6. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765307 The current record is supplemented by this dataset	dataset	January 2018
Additional file 8: Table S6. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765307.v1 The current record is supplemented by this dataset	dataset	January 2018
Additional file 9: Figure S3. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765310.v1 The current record is supplemented by this image	image	January 2018
Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/M9.FIGSHARE.C.3970425 The current record is supplemented by this collection	collection	January 2018
Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.c.3970425.v1 The current record is supplemented by this collection	collection	January 2018
Additional file 11: Figure S4. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765193 The current record is supplemented by this image	image	January 2018
Additional file 12: Table S8. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765202.v1 The current record is supplemented by this text	text	January 2018
Additional file 1: Table S1. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765250 The current record is supplemented by this text	text	January 2018
Additional file 4: Table S4. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765280 The current record is supplemented by this dataset	dataset	January 2018
Additional file 5: Table S5. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765289 The current record is supplemented by this text	text	January 2018
Additional file 6: Figure S1. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765292 The current record is supplemented by this image	image	January 2018
Additional file 7: Figure S2. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765298 The current record is supplemented by this image	image	January 2018
Additional file 9: Figure S3. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765310 The current record is supplemented by this image	image	January 2018
Additional file 14: Text S2. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765235.v1 The current record is supplemented by this text	text	January 2018
Additional file 1: Table S1. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765250.v1 The current record is supplemented by this text	text	January 2018
Additional file 2: Table S2. of Metabolic capability and in situ activity of microorganisms in an oil reservoir Liu, Yi-Fan; Galzerani, Daniela; Mbadinga, Serge https://doi.org/10.6084/m9.figshare.5765259.v1 The current record is supplemented by this text	text	January 2018