Community dynamics and functional characteristics of naphthalene‐degrading populations in contaminated surface sediments and hypoxic/anoxic groundwater

Wilhelm, Roland C.; Hanson, Buck T.; Chandra, Subhash; Madsen, Eugene

doi:10.1111/1462-2920.14309

Community dynamics and functional characteristics of naphthalene‐degrading populations in contaminated surface sediments and hypoxic/anoxic groundwater

Journal Article · Wed Aug 29 00:00:00 EDT 2018 · Environmental Microbiology

DOI:https://doi.org/10.1111/1462-2920.14309· OSTI ID:1467755

^[1]; Hanson, Buck T. ^[2]; Chandra, Subhash ^[3]; Madsen, Eugene ^[4]

Soil and Crop Sciences, School of Integrative Plant Science Cornell University Ithaca NY 14853 USA
Department of Microbiology and Ecosystem Science University of Vienna Vienna Austria
Cornell SIMS Laboratory, Department of Earth and Atmospheric Sciences Cornell University Ithaca NY 14853 USA
Department of Microbiology Cornell University Ithaca NY 14853 USA

Summary

Earlier research on the biogeochemical factors affecting natural attenuation in coal‐tar contaminated groundwater, at South Glens Falls, NY, revealed the importance of anaerobic metabolism and trophic interactions between degrader and bacterivore populations. Field‐based characterizations of both phenomena have proven challenging, but advances in stable isotope probing (SIP), single‐cell imaging and shotgun metagenomics now provide cultivation‐independent tools for their study. We tracked carbon from ¹³ C‐labelled naphthalene through microbial populations in contaminated surface sediments over 6 days using respiration assays, secondary ion mass spectrometry imaging and shotgun metagenomics to disentangle the contaminant‐based trophic web. Contaminant‐exposed communities in hypoxic/anoxic groundwater were contrasted with those from oxic surface sediments to identify putative features of anaerobic catabolism of naphthalene. In total, six bacteria were responsible for naphthalene degradation. Cupriavidus , Ralstonia and Sphingomonas predominated at the earliest stages of SIP incubations and were succeeded in later stages by Stenotrophomonas and Rhodococcus. Metagenome‐assembled genomes provided evidence for the ecological and functional characteristics underlying these temporal shifts. Identical species of Stenotrophomonas and Rhodococcus were abundant in the most contaminated, anoxic groundwater. Apparent increases in bacterivorous protozoa were observed following exposure to naphthalene, though insignificant amounts of carbon were transferred between bacterial degraders and populations of secondary feeders.

View Accepted Manuscript (Publisher)

Sponsoring Organization:: USDOE

OSTI ID:: 1467755

Journal Information:: Environmental Microbiology, Journal Name: Environmental Microbiology Journal Issue: 10 Vol. 20; ISSN 1462-2912

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (92)

Surfactant-enhanced biodegradation of high molecular weight polycyclic aromatic hydrocarbons byStenotrophomonas maltophilia Boonchan, Sudarat; Britz, Margaret L.; Stanley, Grant A. Biotechnology and Bioengineering, Vol. 59, Issue 4 https://doi.org/10.1002/(SICI)1097-0290(19980820)59:4<482::AID-BIT11>3.0.CO;2-C	journal	August 1998
Oxygen limitations and aging as explanations for the field persistence of naphthalene in coal tar-contaminated surface sediments Madsen, E. L.; Mann, C. L.; Bilotta, S. E. Environmental Toxicology and Chemistry, Vol. 15, Issue 11 https://doi.org/10.1002/etc.5620151104	journal	November 1996
Elucidation of in situ polycyclic aromatic hydrocarbon degradation by functional metaproteomics (protein-SIP) Herbst, Florian-Alexander; Bahr, Arne; Duarte, Marcia PROTEOMICS, Vol. 13, Issue 18-19 https://doi.org/10.1002/pmic.201200569	journal	June 2013
ggplot2 Wickham, Hadley Springer New York, NY https://doi.org/10.1007/978-0-387-98141-3	book	January 2009
Role of Protists in Microbial Interactions with Hydrocarbons Stoeck, T.; Edgcomb, V. Handbook of Hydrocarbon and Lipid Microbiology https://doi.org/10.1007/978-3-540-77587-4_178	book	January 2010
The Family Nocardiaceae Goodfellow, Michael The Prokaryotes https://doi.org/10.1007/978-3-642-30138-4_404	book	January 2014
Contrasts between subsurface microbial communities and their metabolic adaptation to polycyclic aromatic hydrocarbons at a forested and an urban coal-tar disposal site Madsen, EugeneL.; Winding, Anne; Malachowsky, Kenneth Microbial Ecology, Vol. 24, Issue 2 https://doi.org/10.1007/BF00174455	journal	September 1992
Hypoxia in Chesapeake Bay, 1950–2001: Long-term change in relation to nutrient loading and river flow Hagy, James D.; Boynton, Walter R.; Keefe, Carolyn W. Estuaries, Vol. 27, Issue 4 https://doi.org/10.1007/BF02907650	journal	August 2004
Geochemical and Physiological Evidence for Mixed Aerobic and Anaerobic Field Biodegradation of Coal Tar Waste by Subsurface Microbial Communities Bakermans, C.; Hohnstock-Ashe, A. M.; Padmanabhan, S. Microbial Ecology, Vol. 44, Issue 2 https://doi.org/10.1007/s00248-002-3011-y	journal	September 2002
Protozoan Grazing Increases Mineralization of Naphthalene in Marine Sediment Tso, Suk-Fong; Taghon, Gary L. Microbial Ecology, Vol. 51, Issue 4 https://doi.org/10.1007/s00248-006-9058-4	journal	April 2006
Gene cloning and in vivo characterization of a dibenzothiophene dioxygenase from Xanthobacter polyaromaticivorans Hirano, Shin-ichi; Haruki, Mitsuru; Takano, Kazufumi Applied Microbiology and Biotechnology, Vol. 69, Issue 6 https://doi.org/10.1007/s00253-005-0007-9	journal	June 2005
Molecular characteristics of xenobiotic-degrading sphingomonads Stolz, Andreas Applied Microbiology and Biotechnology, Vol. 81, Issue 5 https://doi.org/10.1007/s00253-008-1752-3	journal	November 2008
Kinetics of chlorobenzene biodegradation under reduced oxygen levels Balcke, Gerd Ulrich; Wegener, Silke; Kiesel, Bärbel Biodegradation, Vol. 19, Issue 4 https://doi.org/10.1007/s10532-007-9156-0	journal	October 2007
Functional response of an adapted subtidal macrobenthic community to an oil spill: macrobenthic structure and bioturbation activity over time throughout an 18-month field experiment Gilbert, Franck; Stora, Georges; Cuny, Philippe Environmental Science and Pollution Research, Vol. 22, Issue 20 https://doi.org/10.1007/s11356-014-3906-4	journal	December 2014
Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene Juhasz, Albert L.; Naidu, Ravendra International Biodeterioration & Biodegradation, Vol. 45, Issue 1-2 https://doi.org/10.1016/S0964-8305(00)00052-4	journal	January 2000
Dynamic SIMS ion microscopy imaging of individual bacterial cells for studies of isotopically labeled molecules Chandra, Subhash; Pumphrey, Graham; Abraham, Joshua M. Applied Surface Science, Vol. 255, Issue 4 https://doi.org/10.1016/j.apsusc.2008.05.129	journal	December 2008
Microbial fuel cell in enhancing anaerobic biodegradation of diesel Morris, Jeffrey M.; Jin, Song; Crimi, Barbara Chemical Engineering Journal, Vol. 146, Issue 2 https://doi.org/10.1016/j.cej.2008.05.028	journal	February 2009
Targeted metagenomics of active microbial populations with stable-isotope probing Coyotzi, Sara; Pratscher, Jennifer; Murrell, J. Colin Current Opinion in Biotechnology, Vol. 41 https://doi.org/10.1016/j.copbio.2016.02.017	journal	October 2016
Tracking microbial interactions with NanoSIMS Musat, Niculina; Musat, Florin; Weber, Peter Kilian Current Opinion in Biotechnology, Vol. 41 https://doi.org/10.1016/j.copbio.2016.06.007	journal	October 2016
Ciliated protists from the nepheloid layer and water column of sites affected by the Deepwater Horizon oil spill in the Northeastern Gulf of Mexico Moss, Joseph A.; McCurry, Chelsea; Tominack, Sarah Deep Sea Research Part I: Oceanographic Research Papers, Vol. 106 https://doi.org/10.1016/j.dsr.2015.10.001	journal	December 2015
Impact of protists on a hydrocarbon-degrading bacterial community from deep-sea Gulf of Mexico sediments: A microcosm study Beaudoin, David J.; Carmichael, Catherine A.; Nelson, Robert K. Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 129 https://doi.org/10.1016/j.dsr2.2014.01.007	journal	July 2016
Betaproteobacteria dominance and diversity shifts in the bacterial community of a PAH-contaminated soil exposed to phenanthrene Martin, Florence; Torelli, Stéphane; Le Paslier, Denis Environmental Pollution, Vol. 162 https://doi.org/10.1016/j.envpol.2011.11.032	journal	March 2012
BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences Kanehisa, Minoru; Sato, Yoko; Morishima, Kanae Journal of Molecular Biology, Vol. 428, Issue 4 https://doi.org/10.1016/j.jmb.2015.11.006	journal	February 2016
Inorganic Carbon Limitation and Mixotrophic Growth in Chlamydomonas from an Acidic Mining Lake Tittel, Jörg; Bissinger, Vera; Gaedke, Ursula Protist, Vol. 156, Issue 1 https://doi.org/10.1016/j.protis.2004.09.001	journal	June 2005
Enhanced removal of petroleum hydrocarbons using a bioelectrochemical remediation system with pre-cultured anodes Venkidusamy, Krishnaveni; Megharaj, Mallavarapu; Marzorati, Massimo Science of The Total Environment, Vol. 539 https://doi.org/10.1016/j.scitotenv.2015.08.098	journal	January 2016
Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil Eilers, Kathryn G.; Lauber, Christian L.; Knight, Rob Soil Biology and Biochemistry, Vol. 42, Issue 6 https://doi.org/10.1016/j.soilbio.2010.02.003	journal	June 2010
One-year monitoring of meta-cleavage dioxygenase gene expression and microbial community dynamics reveals the relevance of subfamily I.2.C extradiol dioxygenases in hypoxic, BTEX-contaminated groundwater Táncsics, András; Farkas, Milán; Szoboszlay, Sándor Systematic and Applied Microbiology, Vol. 36, Issue 5 https://doi.org/10.1016/j.syapm.2013.03.008	journal	July 2013
Peer Reviewed: A Subcellular Imaging by Dynamic SIMS Ion Microscopy. Chandra, Subhash; Smith, Duane R.; Morrison, George H. Analytical Chemistry, Vol. 72, Issue 3 https://doi.org/10.1021/ac002716i	journal	February 2000
Stable Isotope Probing and Raman Spectroscopy for Monitoring Carbon Flow in a Food Chain and Revealing Metabolic Pathway Li, Mengqiu; Huang, Wei E.; Gibson, Christopher M. Analytical Chemistry, Vol. 85, Issue 3 https://doi.org/10.1021/ac302910x	journal	January 2013
Field Evidence for a Protistan Role in an Organically-Contaminated Aquifer Kinner, Nancy E.; Harvey, Ronald W.; Shay, David M. Environmental Science & Technology, Vol. 36, Issue 20 https://doi.org/10.1021/es020611m	journal	October 2002
Microbial Metabolism and Community Structure in Response to Bioelectrochemically Enhanced Remediation of Petroleum Hydrocarbon-Contaminated Soil Lu, Lu; Huggins, Tyler; Jin, Song Environmental Science & Technology, Vol. 48, Issue 7 https://doi.org/10.1021/es4057906	journal	March 2014
Subsurface ecosystem resilience: long-term attenuation of subsurface contaminants supports a dynamic microbial community Yagi, Jane M.; Neuhauser, Edward F.; Ripp, John A. The ISME Journal, Vol. 4, Issue 1 https://doi.org/10.1038/ismej.2009.101	journal	September 2009
Metaproteogenomic insights beyond bacterial response to naphthalene exposure and bio-stimulation Guazzaroni, María-Eugenia; Herbst, Florian-Alexander; Lores, Iván The ISME Journal, Vol. 7, Issue 1 https://doi.org/10.1038/ismej.2012.82	journal	July 2012
Spatial patterns of microbial diversity and activity in an aged creosote-contaminated site Mukherjee, Shinjini; Juottonen, Heli; Siivonen, Pauli The ISME Journal, Vol. 8, Issue 10 https://doi.org/10.1038/ismej.2014.151	journal	August 2014
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
Phylogenetic organization of bacterial activity Morrissey, Ember M.; Mau, Rebecca L.; Schwartz, Egbert The ISME Journal, Vol. 10, Issue 9 https://doi.org/10.1038/ismej.2016.28	journal	March 2016
Extracellular electron transfer mechanisms between microorganisms and minerals Shi, Liang; Dong, Hailiang; Reguera, Gemma Nature Reviews Microbiology, Vol. 14, Issue 10 https://doi.org/10.1038/nrmicro.2016.93	journal	August 2016
The versatility and adaptation of bacteria from the genus Stenotrophomonas Ryan, Robert P.; Monchy, Sebastien; Cardinale, Massimiliano Nature Reviews Microbiology, Vol. 7, Issue 7 https://doi.org/10.1038/nrmicro2163	journal	July 2009
Accurate binning of metagenomic contigs via automated clustering sequences using information of genomic signatures and marker genes Lin, Hsin-Hung; Liao, Yu-Chieh Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep24175	journal	April 2016
Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens Pritchard, Leighton; Glover, Rachel H.; Humphris, Sonia Analytical Methods, Vol. 8, Issue 1 https://doi.org/10.1039/C5AY02550H	journal	January 2016
Stable isotope probing of rRNA and DNA reveals a dynamic methylotroph community and trophic interactions with fungi and protozoa in oxic rice field soil: SIP of methylotrophs in rice field soil Lueders, Tillmann; Wagner, Bianca; Claus, Peter Environmental Microbiology, Vol. 6, Issue 1 https://doi.org/10.1046/j.1462-2920.2003.00535.x	journal	December 2003
Discovery of a bacterium, with distinctive dioxygenase, that is responsible for in situ biodegradation in contaminated sediment Jeon, C. O.; Park, W.; Padmanabhan, P. Proceedings of the National Academy of Sciences, Vol. 100, Issue 23 https://doi.org/10.1073/pnas.1735529100	journal	November 2003
Morphology and morphogenesis of the poorly-known marine urostylid ciliate, Metaurostylopsis marina(Kahl, 1932) nov. gen., nov. comb. (Protozoa, Ciliophora, Hypotrichida) Song, Weibo; Petz, Wolfgang; Warren, Alan European Journal of Protistology, Vol. 37, Issue 1 https://doi.org/10.1078/0932-4739-00802	journal	January 2001
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
IMG ER: a system for microbial genome annotation expert review and curation Markowitz, Victor M.; Mavromatis, Konstantinos; Ivanova, Natalia N. Bioinformatics, Vol. 25, Issue 17 https://doi.org/10.1093/bioinformatics/btp393	journal	June 2009
FLASH: fast length adjustment of short reads to improve genome assemblies Magoc, T.; Salzberg, S. L. Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr507	journal	September 2011
QUAST: quality assessment tool for genome assemblies Gurevich, Alexey; Saveliev, Vladislav; Vyahhi, Nikolay Bioinformatics, Vol. 29, Issue 8 https://doi.org/10.1093/bioinformatics/btt086	journal	February 2013
Infernal 1.1: 100-fold faster RNA homology searches Nawrocki, E. P.; Eddy, S. R. Bioinformatics, Vol. 29, Issue 22 https://doi.org/10.1093/bioinformatics/btt509	journal	September 2013
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
Reconstructing 16S rRNA genes in metagenomic data Yuan, Cheng; Lei, Jikai; Cole, James Bioinformatics, Vol. 31, Issue 12 https://doi.org/10.1093/bioinformatics/btv231	journal	June 2015
Anaerobic naphthalene degradation by sulfate-reducing Desulfobacteraceae from various anoxic aquifers Kümmel, Steffen; Herbst, Florian-Alexander; Bahr, Arne FEMS Microbiology Ecology, Vol. 91, Issue 3 https://doi.org/10.1093/femsec/fiv006	journal	January 2015
SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB Pruesse, E.; Quast, C.; Knittel, K. Nucleic Acids Research, Vol. 35, Issue 21 https://doi.org/10.1093/nar/gkm864	journal	November 2007
rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development Stoddard, Steven F.; Smith, Byron J.; Hein, Robert Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1201	journal	November 2014
Polaromonas naphthalenivorans sp. nov., a naphthalene-degrading bacterium from naphthalene-contaminated sediment Jeon, C. O. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 1 https://doi.org/10.1099/ijs.0.02636-0	journal	January 2004
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
Impact of protist grazing on a key bacterial group for biogeochemical cycling in Baltic Sea pelagic oxic/anoxic interfaces: Protist grazing on a redoxcline bacterial key-player Anderson, Ruth; Wylezich, Claudia; Glaubitz, Sabine Environmental Microbiology, Vol. 15, Issue 5 https://doi.org/10.1111/1462-2920.12078	journal	January 2013
Naphthalene biodegradation under oxygen‐limiting conditions: community dynamics and the relevance of biofilm‐forming capacity Martirani‐Von Abercron, Sophie‐Marie; Marín, Patricia; Solsona‐Ferraz, Marta Microbial Biotechnology, Vol. 10, Issue 6 https://doi.org/10.1111/1751-7915.12842	journal	August 2017
Intra-genomic variation in G + C content and its implications for DNA stable isotope probing: DNA-SIP and intra-genomic variation in G + C content Youngblut, Nicholas D.; Buckley, Daniel H. Environmental Microbiology Reports, Vol. 6, Issue 6 https://doi.org/10.1111/1758-2229.12201	journal	October 2014
In situ expression of nitrite-dependent anaerobic methane oxidation proteins by Candidatus Methylomirabilis oxyfera co-occurring with expressed anammox proteins in a contaminated aquifer : In situ Hanson, Buck T.; Madsen, Eugene L. Environmental Microbiology Reports, Vol. 7, Issue 2 https://doi.org/10.1111/1758-2229.12239	journal	February 2015
Field-based and laboratory stable isotope probing surveys of the identities of both aerobic and anaerobic benzene-metabolizing microorganisms in freshwater sediment Liou, J. S. -C.; DeRito, C. M.; Madsen, E. L. Environmental Microbiology, Vol. 10, Issue 8 https://doi.org/10.1111/j.1462-2920.2008.01612.x	journal	August 2008
Dynamic secondary ion mass spectrometry imaging of microbial populations utilizing ¹³ C-labelled substrates in pure culture and in soil Pumphrey, Graham M.; Hanson, Buck T.; Chandra, Subhash Environmental Microbiology, Vol. 11, Issue 1 https://doi.org/10.1111/j.1462-2920.2008.01757.x	journal	January 2009
Use of stable isotope-labelled cells to identify active grazers of picocyanobacteria in ocean surface waters Frias-Lopez, Jorge; Thompson, Anne; Waldbauer, Jacob Environmental Microbiology, Vol. 11, Issue 2 https://doi.org/10.1111/j.1462-2920.2008.01793.x	journal	February 2009
Size-selective feeding by Cyclidium sp. on bacterioplankton and various sizes of cultured bacteria Å imek, Karel; Vrba, Jaroslav; Hartman, Petr FEMS Microbiology Ecology, Vol. 14, Issue 2 https://doi.org/10.1111/j.1574-6941.1994.tb00102.x	journal	June 1994
Assimilation of benzene carbon through multiple trophic levels traced by different stable isotope probing methodologies: Benzene food webs by stable isotope probing Bastida, Felipe; Jechalke, Sven; Bombach, Petra FEMS Microbiology Ecology, Vol. 77, Issue 2 https://doi.org/10.1111/j.1574-6941.2011.01118.x	journal	May 2011
Anaerobic free-living protozoa: growth efficiencies and the structure of anaeorobic communities Fenchel, Tom; Finaly, Bland J. FEMS Microbiology Letters, Vol. 74, Issue 4 https://doi.org/10.1111/j.1574-6968.1990.tb04073.x	journal	December 1990
Metabolic reconstruction of aromatic compounds degradation from the genome of the amazing pollutant-degrading bacterium Cupriavidus necator JMP134 Pérez-Pantoja, Danilo; De la Iglesia, Rodrigo; Pieper, Dietmar H. FEMS Microbiology Reviews, Vol. 32, Issue 5 https://doi.org/10.1111/j.1574-6976.2008.00122.x	journal	August 2008
Fear in the dark? Community-level effects of non-lethal predators change with light regime Forbes, Coreen; Hammill, Edd Oikos, Vol. 122, Issue 12 https://doi.org/10.1111/j.1600-0706.2013.00557.x	journal	June 2013
Monitored Natural Attenuation of Manufactured Gas Plant Tar Mono- and Polycyclic Aromatic Hydrocarbons in Ground Water: A 14-Year Field Study Neuhauser, Edward F.; Ripp, John A.; Azzolina, Nicholas A. Ground Water Monitoring & Remediation, Vol. 29, Issue 3 https://doi.org/10.1111/j.1745-6592.2009.01244.x	journal	June 2009
The Morphology of Three Loxophyllum Species (Ciliophora, Pleurostomatida) from Southern China, L. lembum sp. n., L. vesiculosum sp. n. and L. perihoplophorum Buddenbrock, 1920, with Notes on the Molecular Phylogeny of Loxophyllum Wu, Lei; Chen, Ruimin; Yi, Zhenzhen Journal of Eukaryotic Microbiology, Vol. 61, Issue 2 https://doi.org/10.1111/jeu.12089	journal	December 2013
In situ biodegradation: microbiological patterns in a contaminated aquifer Madsen, E.; Sinclair, J.; Ghiorse, W. Science, Vol. 252, Issue 5007 https://doi.org/10.1126/science.2028258	journal	May 1991
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy Wang, Q.; Garrity, G. M.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/AEM.00062-07	journal	June 2007
Subsurface Cycling of Nitrogen and Anaerobic Aromatic Hydrocarbon Biodegradation Revealed by Nucleic Acid and Metabolic Biomarkers Yagi, J. M.; Suflita, J. M.; Gieg, L. M. Applied and Environmental Microbiology, Vol. 76, Issue 10 https://doi.org/10.1128/AEM.00172-10	journal	March 2010
Diversity, Abundance, and Consistency of Microbial Oxygenase Expression and Biodegradation in a Shallow Contaminated Aquifer Yagi, J. M.; Madsen, E. L. Applied and Environmental Microbiology, Vol. 75, Issue 20 https://doi.org/10.1128/AEM.01091-09	journal	August 2009
Development of a Fatty Acid and RNA Stable Isotope Probing-Based Method for Tracking Protist Grazing on Bacteria in Wastewater Kuppardt, S.; Chatzinotas, A.; Kastner, M. Applied and Environmental Microbiology, Vol. 76, Issue 24 https://doi.org/10.1128/AEM.01632-10	journal	October 2010
From Rare to Dominant: a Fine-Tuned Soil Bacterial Bloom during Petroleum Hydrocarbon Bioremediation Fuentes, Sebastián; Barra, Bárbara; Caporaso, J. Gregory Applied and Environmental Microbiology, Vol. 82, Issue 3 https://doi.org/10.1128/AEM.02625-15	journal	November 2015
Benzene Degradation by a Variovorax Species within a Coal Tar-Contaminated Groundwater Microbial Community Posman, Kevin M.; DeRito, Christopher M.; Madsen, Eugene L. Applied and Environmental Microbiology, Vol. 83, Issue 4 https://doi.org/10.1128/AEM.02658-16	journal	December 2016
Identification of Ciliate Grazers of Autotrophic Bacteria in Ammonia-Oxidizing Activated Sludge by RNA Stable Isotope Probing Moreno, A. M.; Matz, C.; Kjelleberg, S. Applied and Environmental Microbiology, Vol. 76, Issue 7 https://doi.org/10.1128/AEM.02777-09	journal	February 2010
Natural horizontal transfer of a naphthalene dioxygenase gene between bacteria native to a coal tar-contaminated field site Herrick, J. B.; Stuart-Keil, K. G.; Ghiorse, W. C. Applied and Environmental Microbiology, Vol. 63, Issue 6 https://doi.org/10.1128/AEM.63.6.2330-2337.1997	journal	June 1997
Rapid Method for Coextraction of DNA and RNA from Natural Environments for Analysis of Ribosomal DNA- and rRNA-Based Microbial Community Composition Griffiths, R. I.; Whiteley, A. S.; O'Donnell, A. G. Applied and Environmental Microbiology, Vol. 66, Issue 12 https://doi.org/10.1128/AEM.66.12.5488-5491.2000	journal	December 2000
Wide Distribution of a Novel pmoA-Like Gene Copy among Type II Methanotrophs, and Its Expression in Methylocystis Strain SC2 Tchawa Yimga, M.; Dunfield, P. F.; Ricke, P. Applied and Environmental Microbiology, Vol. 69, Issue 9 https://doi.org/10.1128/AEM.69.9.5593-5602.2003	journal	September 2003
Use of Field-Based Stable Isotope Probing To Identify Adapted Populations and Track Carbon Flow through a Phenol-Degrading Soil Microbial Community DeRito, C. M.; Pumphrey, G. M.; Madsen, E. L. Applied and Environmental Microbiology, Vol. 71, Issue 12 https://doi.org/10.1128/AEM.71.12.7858-7865.2005	journal	December 2005
Microbial Oxidation of Hydrocarbons: Properties of a Soluble Methane Monooxygenase from a Facultative Methane-Utilizing Organism, Methylobacterium sp. Strain CRL-26 Patel, Ramesh N.; Hou, Ching T.; Laskin, Allen I. Applied and Environmental Microbiology, Vol. 44, Issue 5 https://doi.org/10.1128/aem.44.5.1130-1137.1982	journal	November 1982
Catechol 2,3-dioxygenases functional in oxygen-limited (hypoxic) environments. Kukor, J. J.; Olsen, R. H. Applied and environmental microbiology, Vol. 62, Issue 5 https://doi.org/10.1128/aem.62.5.1728-1740.1996	journal	January 1996
Methylobacterium populi VP2: Plant Growth-Promoting Bacterium Isolated from a Highly Polluted Environment for Polycyclic Aromatic Hydrocarbon (PAH) Biodegradation Ventorino, Valeria; Sannino, Filomena; Piccolo, Alessandro The Scientific World Journal, Vol. 2014 https://doi.org/10.1155/2014/931793	journal	January 2014
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
A novel bacterial isolate Stenotrophomonas maltophilia as living factory for synthesis of gold nanoparticles Nangia, Yogesh; Wangoo, Nishima; Goyal, Nisha Microbial Cell Factories, Vol. 8, Issue 1 https://doi.org/10.1186/1475-2859-8-39	journal	January 2009
Versatile and open software for comparing large genomes Kurtz, Stefan; Phillippy, Adam; Delcher, Arthur L. Genome Biology, Vol. 5, Issue 2, R12 https://doi.org/10.1186/gb-2004-5-2-r12	journal	January 2004
A Filamentous Hemagglutinin-Like Protein of Xanthomonas axonopodis pv. citri, the Phytopathogen Responsible for Citrus Canker, Is Involved in Bacterial Virulence Gottig, Natalia; Garavaglia, Betiana S.; Garofalo, Cecilia G. PLoS ONE, Vol. 4, Issue 2 https://doi.org/10.1371/journal.pone.0004358	journal	February 2009
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data McMurdie, Paul J.; Holmes, Susan PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061217	journal	April 2013
Reshaping Data with the reshape Package Wickham, Hadley Journal of Statistical Software, Vol. 21, Issue 12 https://doi.org/10.18637/jss.v021.i12	journal	January 2007
The Split-Apply-Combine Strategy for Data Analysis Wickham, Hadley Journal of Statistical Software, Vol. 40, Issue 1 https://doi.org/10.18637/jss.v040.i01	journal	January 2011
Identification of Electrode Respiring, Hydrocarbonoclastic Bacterial Strain Stenotrophomonas maltophilia MK2 Highlights the Untapped Potential for Environmental Bioremediation Venkidusamy, Krishnaveni; Megharaj, Mallavarapu Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01965	journal	December 2016

Similar Records

Transformation of monoaromatic hydrocarbons to organic acids in anoxic groundwater environment

Journal Article · Sun Dec 31 23:00:00 EST 1989 · Environmental Geology and Water Sciences; (United States) · OSTI ID:5115157

Anaerobic benzene oxidation in Geotalea daltonii involves activation by methylation and is regulated by the transition state regulator AbrB

Journal Article · Tue Oct 22 20:00:00 EDT 2024 · Applied and Environmental Microbiology · OSTI ID:2446545

Biostimulation and microbial community profiling reveal insights on RDX transformation in groundwater

Journal Article · Wed Nov 16 19:00:00 EST 2016 · MicrobiologyOpen · OSTI ID:1332767

Community dynamics and functional characteristics of naphthalene‐degrading populations in contaminated surface sediments and hypoxic/anoxic groundwater

Citation Formats

References (92)

Similar Records

Related Subjects