Short-term transcriptional response of microbial communities to N-fertilization in pine forest soil

Albright, Michaeline Burr Nelson; Johansen, Renee; Lopez, Deanna; Gallegos-Graves, Laverne A; Steven, Blaire; Kuske, Cheryl R.; Dunbar, John

doi:10.1128/AEM.00598-18

Title: Short-term transcriptional response of microbial communities to N-fertilization in pine forest soil

Journal Article · Fri May 25 00:00:00 EDT 2018 · Applied and Environmental Microbiology

DOI:https://doi.org/10.1128/AEM.00598-18· OSTI ID:1441353

Albright, Michaeline Burr Nelson ^[1]; Johansen, Renee ^[1]; Lopez, Deanna ^[1]; Gallegos-Graves, Laverne A ^[1]; Steven, Blaire ^[2];

^[1];

^[1]

Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Connecticut Agricultural Experiment Station, New Haven, CT (United States). Dept. of Environmental Sciences

Numerous studies have examined the long-term effect of experimental nitrogen (N) deposition in terrestrial ecosystems, however N-specific mechanistic markers are difficult to disentangle from responses to other environmental changes. The strongest picture of N-responsive mechanistic markers is likely to arise from measurements over a short (hours to days) timescale immediately after inorganic N deposition. Therefore, we assessed the short-term (3-day) transcriptional response of microbial communities in two soil strata from a pine forest to a high dose of N fertilization (c.a. 1mg/g of soil material) in laboratory microcosms. Here, we hypothesized that N fertilization would repress the expression of fungal and bacterial genes linked to N-mining from plant litter. However, despite N-suppression of microbial respiration, the most pronounced differences in functional gene expression were between strata rather than in response to the N addition. Overall, ~4% of metabolic genes changed in expression with N addition, while three times as many (~12%) were significantly different across the different soil strata in the microcosms. In particular, we found little evidence of N changing expression levels of metabolic genes associated with complex carbohydrate degradation (CAZymes) or inorganic N utilization. This suggests that direct N repression of microbial functional gene expression is not the principle mechanism for reduced soil respiration immediately after N deposition. Instead, changes in expression with N addition occurred primarily in general cell maintenance areas, for example in ribosome-related transcripts. Transcriptional changes in functional gene abundance in response to N-addition observed in longer-term field studies likely results from changes in microbial composition.

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Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

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

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1441353

Report Number(s):: LA-UR-18-21874; 1098-5336 (Electronic)

Journal Information:: Applied and Environmental Microbiology, Vol. 84, Issue 15; ISSN 0099-2240

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 7 works

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References (81)

Molecular analysis of fungal communities and laccase genes in decomposing litter reveals differences among forest types but no impact of nitrogen deposition Blackwood, Christopher B.; Waldrop, Mark P.; Zak, Donald R. Environmental Microbiology, Vol. 9, Issue 5 https://doi.org/10.1111/j.1462-2920.2007.01250.x	journal	May 2007
Common patterns – unique features: nitrogen metabolism and regulation in Gram-positive bacteria Amon, Johannes; Titgemeyer, Fritz; Burkovski, Andreas FEMS Microbiology Reviews, Vol. 34, Issue 4 https://doi.org/10.1111/j.1574-6976.2010.00216.x	journal	July 2010
Genetic regulation of nitrogen metabolism in the fungi. Marzluf, G. A. Microbiology and molecular biology reviews : MMBR, Vol. 61, Issue 1 https://doi.org/10.1128/.61.1.17-32.1997	journal	January 1997
Thermodynamics of the control of metabolism Westerhoff, Hans V.; Plomp, Peter J. A. M.; Groen, Albert K. Cell Biophysics, Vol. 11, Issue 1 https://doi.org/10.1007/BF02797123	journal	December 1987
Technical Report: Human Alteration of the Global Nitrogen Cycle: Sources and Consequences Vitousek, Peter M.; Aber, John D.; Howarth, Robert W. Ecological Applications, Vol. 7, Issue 3 https://doi.org/10.2307/2269431	journal	August 1997
Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies Treseder, Kathleen K. Ecology Letters, Vol. 11, Issue 10 https://doi.org/10.1111/j.1461-0248.2008.01230.x	journal	October 2008
Microbial Responses to Long-Term N Deposition in a Semiarid Grassland Stursova, Martina; Crenshaw, Chelsea L.; Sinsabaugh, Robert L. Microbial Ecology, Vol. 51, Issue 1 https://doi.org/10.1007/s00248-005-5156-y	journal	January 2006
Linkages Between Microbial and Hydrologic Processes in arid and Semiarid Watersheds Belnap, Jayne; Welter, Jill R.; Grimm, Nancy B. Ecology, Vol. 86, Issue 2 https://doi.org/10.1890/03-0567	journal	February 2005
Integrating biogeochemistry with multiomic sequence information in a model oxygen minimum zone Louca, Stilianos; Hawley, Alyse K.; Katsev, Sergei Proceedings of the National Academy of Sciences, Vol. 113, Issue 40 https://doi.org/10.1073/pnas.1602897113	journal	September 2016
Contrasting soil fungal community responses to experimental nitrogen addition using the large subunit rRNA taxonomic marker and cellobiohydrolase I functional marker Mueller, Rebecca C.; Balasch, Monica M.; Kuske, Cheryl R. Molecular Ecology, Vol. 23, Issue 17 https://doi.org/10.1111/mec.12858	journal	August 2014
Steady-state and dynamic gene expression programs in Saccharomyces cerevisiae in response to variation in environmental nitrogen Airoldi, Edoardo M.; Miller, Darach; Athanasiadou, Rodoniki Molecular Biology of the Cell, Vol. 27, Issue 8 https://doi.org/10.1091/mbc.e14-05-1013	journal	April 2016
Microbes as Engines of Ecosystem Function: When Does Community Structure Enhance Predictions of Ecosystem Processes? Graham, Emily B.; Knelman, Joseph E.; Schindlbacher, Andreas Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00214	journal	February 2016
Nitrogen Assimilation in Escherichia coli: Putting Molecular Data into a Systems Perspective van Heeswijk, W. C.; Westerhoff, H. V.; Boogerd, F. C. Microbiology and Molecular Biology Reviews, Vol. 77, Issue 4 https://doi.org/10.1128/MMBR.00025-13	journal	December 2013
Maturation and degradation of RNA in bacteria Condon, Ciarán Current Opinion in Microbiology, Vol. 10, Issue 3 https://doi.org/10.1016/j.mib.2007.05.008	journal	June 2007
MEGAN Community Edition - Interactive Exploration and Analysis of Large-Scale Microbiome Sequencing Data Huson, Daniel H.; Beier, Sina; Flade, Isabell PLOS Computational Biology, Vol. 12, Issue 6 https://doi.org/10.1371/journal.pcbi.1004957	journal	June 2016
Soil Fungal Cellobiohydrolase I Gene ( cbhI ) Composition and Expression in a Loblolly Pine Plantation under Conditions of Elevated Atmospheric CO ₂ and Nitrogen Fertilization Weber, Carolyn F.; Balasch, Monica Moya; Gossage, Zachary Applied and Environmental Microbiology, Vol. 78, Issue 11 https://doi.org/10.1128/AEM.08018-11	journal	March 2012
The influence of precipitation pulses on soil respiration – Assessing the “Birch effect” by stable carbon isotopes Unger, Stephan; Máguas, Cristina; Pereira, João S. Soil Biology and Biochemistry, Vol. 42, Issue 10 https://doi.org/10.1016/j.soilbio.2010.06.019	journal	October 2010
Microbial community response to nitrogen deposition in northern forest ecosystems Waldrop, Mark P.; Zak, Donald R.; Sinsabaugh, Robert L. Soil Biology and Biochemistry, Vol. 36, Issue 9 https://doi.org/10.1016/j.soilbio.2004.04.023	journal	September 2004
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph Li, Dinghua; Liu, Chi-Man; Luo, Ruibang Bioinformatics, Vol. 31, Issue 10 https://doi.org/10.1093/bioinformatics/btv033	journal	January 2015
Microbial mediation of biogeochemical cycles revealed by simulation of global changes with soil transplant and cropping Zhao, Mengxin; Xue, Kai; Wang, Feng The ISME Journal, Vol. 8, Issue 10 https://doi.org/10.1038/ismej.2014.46	journal	April 2014
N dynamics in the rhizosphere of Pinus ponderosa seedlings Norton, Jeanette M.; Firestone, Mary K. Soil Biology and Biochemistry, Vol. 28, Issue 3 https://doi.org/10.1016/0038-0717(95)00155-7	journal	March 1996
A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes van der Wal, Annemieke; Geydan, Thomas D.; Kuyper, Thomas W. FEMS Microbiology Reviews, Vol. 37, Issue 4 https://doi.org/10.1111/1574-6976.12001	journal	July 2013
Ligninolytic enzyme system of Phanaerochaete chrysosporium: synthesized in the absence of lignin in response to nitrogen starvation. Keyser, P.; Kirk, T. K.; Zeikus, J. G. Journal of Bacteriology, Vol. 135, Issue 3 https://doi.org/10.1128/JB.135.3.790-797.1978	journal	January 1978
Identification of laccase-like genes in ectomycorrhizal basidiomycetes and transcriptional regulation by nitrogen in Piloderma byssinum Chen, David M.; Bastias, Brigitte A.; Taylor, Andrew F. S. New Phytologist, Vol. 157, Issue 3 https://doi.org/10.1046/j.1469-8137.2003.00687.x	journal	March 2003
Changes in Fungal Community Composition in Response to Elevated Atmospheric CO2 and Nitrogen Fertilization Varies with Soil Horizon Weber, Carolyn F.; Vilgalys, Rytas; Kuske, Cheryl R. Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00078	journal	January 2013
dbCAN: a web resource for automated carbohydrate-active enzyme annotation Yin, Yanbin; Mao, Xizeng; Yang, Jincai Nucleic Acids Research, Vol. 40, Issue W1 https://doi.org/10.1093/nar/gks479	journal	May 2012
Competition for nitrogen between plants and soil microorganisms Kaye, Jason P.; Hart, Stephen C. Trends in Ecology & Evolution, Vol. 12, Issue 4 https://doi.org/10.1016/S0169-5347(97)01001-X	journal	April 1997
Comparative metatranscriptomics reveals widespread community responses during phenanthrene degradation in soil: Metatranscriptomic analysis of phenanthrene amended soil de Menezes, Alexandre; Clipson, Nicholas; Doyle, Evelyn Environmental Microbiology, Vol. 14, Issue 9 https://doi.org/10.1111/j.1462-2920.2012.02781.x	journal	May 2012
Nitrogen Cycles: Past, Present, and Future Galloway, J. N.; Dentener, F. J.; Capone, D. G. Biogeochemistry, Vol. 70, Issue 2 https://doi.org/10.1007/s10533-004-0370-0	journal	September 2004
Fast and sensitive protein alignment using DIAMOND Buchfink, Benjamin; Xie, Chao; Huson, Daniel H. Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3176	journal	November 2014
Systems biology may work when we learn to understand the parts in terms of the whole Cornish-Bowden, A.; Cárdenas, M. L. Biochemical Society Transactions, Vol. 33, Issue 3 https://doi.org/10.1042/BST0330516	journal	June 2005
Transcriptional regulation of plant cell wall degradation by filamentous fungi Aro, Nina; Pakula, Tiina; Penttilä, Merja FEMS Microbiology Reviews, Vol. 29, Issue 4 https://doi.org/10.1016/j.femsre.2004.11.006	journal	September 2005
Extracellular Enzyme Activities and Soil Organic Matter Dynamics for Northern Hardwood Forests receiving Simulated Nitrogen Deposition Sinsabaugh, Robert L.; Gallo, Marcy E.; Lauber, Christian Biogeochemistry, Vol. 75, Issue 2 https://doi.org/10.1007/s10533-004-7112-1	journal	August 2005
Metagenomic reconstruction of nitrogen cycling pathways in a CO2-enriched grassland ecosystem Tu, Qichao; He, Zhili; Wu, Liyou Soil Biology and Biochemistry, Vol. 106 https://doi.org/10.1016/j.soilbio.2016.12.017	journal	March 2017
Atmospheric N Deposition Increases Bacterial Laccase-Like Multicopper Oxidases: Implications for Organic Matter Decay Freedman, Zachary; Zak, Donald R. Applied and Environmental Microbiology, Vol. 80, Issue 14 https://doi.org/10.1128/AEM.01224-14	journal	May 2014
Simulated Atmospheric N Deposition Alters Fungal Community Composition and Suppresses Ligninolytic Gene Expression in a Northern Hardwood Forest Edwards, Ivan P.; Zak, Donald R.; Kellner, Harald PLoS ONE, Vol. 6, Issue 6 https://doi.org/10.1371/journal.pone.0020421	journal	June 2011
Forest floor community metatranscriptomes identify fungal and bacterial responses to N deposition in two maple forests Hesse, Cedar N.; Mueller, Rebecca C.; Vuyisich, Momchilo Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00337	journal	April 2015
KEGG as a reference resource for gene and protein annotation Kanehisa, Minoru; Sato, Yoko; Kawashima, Masayuki Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1070	journal	October 2015
Expression patterns of elemental cycling genes in the Amazon River Plume Satinsky, Brandon M.; Smith, Christa B.; Sharma, Shalabh The ISME Journal, Vol. 11, Issue 8 https://doi.org/10.1038/ismej.2017.46	journal	April 2017
Systems-based approaches to unravel multi-species microbial community functioning Abram, Florence Computational and Structural Biotechnology Journal, Vol. 13 https://doi.org/10.1016/j.csbj.2014.11.009	journal	January 2015
Bridging the gap between omics and earth system science to better understand how environmental change impacts marine microbes Mock, Thomas; Daines, Stuart J.; Geider, Richard Global Change Biology, Vol. 22, Issue 1 https://doi.org/10.1111/gcb.12983	journal	July 2015
Microbial Mechanisms Mediating Increased Soil C Storage under Elevated Atmospheric N Deposition Eisenlord, Sarah D.; Freedman, Zachary; Zak, Donald R. Applied and Environmental Microbiology, Vol. 79, Issue 4 https://doi.org/10.1128/AEM.03156-12	journal	December 2012
Dispersing misconceptions and identifying opportunities for the use of 'omics' in soil microbial ecology Prosser, James I. Nature Reviews Microbiology, Vol. 13, Issue 7 https://doi.org/10.1038/nrmicro3468	journal	June 2015
The Pfam protein families database: towards a more sustainable future Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1344	journal	December 2015
Global biogeography of microbial nitrogen-cycling traits in soil Nelson, Michaeline B.; Martiny, Adam C.; Martiny, Jennifer B. H. Proceedings of the National Academy of Sciences, Vol. 113, Issue 29 https://doi.org/10.1073/pnas.1601070113	journal	July 2016
Ocean biogeochemistry modeled with emergent trait-based genomics Coles, V. J.; Stukel, M. R.; Brooks, M. T. Science, Vol. 358, Issue 6367 https://doi.org/10.1126/science.aan5712	journal	November 2017
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
Soil carbon and nitrogen dynamics throughout the summer drought in a California annual grassland Schaeffer, Sean M.; Homyak, Peter M.; Boot, Claudia M. Soil Biology and Biochemistry, Vol. 115 https://doi.org/10.1016/j.soilbio.2017.08.009	journal	December 2017
Emergence and Its Place in Nature: A Case Study of Biochemical Networks Boogerd, F. C.; Bruggeman, F. J.; Richardson, R. C. Synthese, Vol. 145, Issue 1 https://doi.org/10.1007/s11229-004-4421-9	journal	May 2005
Diverse Marinimicrobia bacteria may mediate coupled biogeochemical cycles along eco-thermodynamic gradients Hawley, Alyse K.; Nobu, Masaru K.; Wright, Jody J. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01376-9	journal	November 2017
Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation O'Leary, Nuala A.; Wright, Mathew W.; Brister, J. Rodney Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1189	journal	November 2015
Spatial and temporal effects on plant-microbial competition for inorganic nitrogen in a california annual grassland Schimel, Joshua P.; Jackson, Louise E.; Firestone, Mary K. Soil Biology and Biochemistry, Vol. 21, Issue 8 https://doi.org/10.1016/0038-0717(89)90044-8	journal	January 1989
PEAR: a fast and accurate Illumina Paired-End reAd mergeR Zhang, J.; Kobert, K.; Flouri, T. Bioinformatics, Vol. 30, Issue 5 https://doi.org/10.1093/bioinformatics/btt593	journal	October 2013
Pulse dynamics and microbial processes in aridland ecosystems: Pulse dynamics in aridland soils Collins, Scott L.; Sinsabaugh, Robert L.; Crenshaw, Chelsea Journal of Ecology, Vol. 96, Issue 3 https://doi.org/10.1111/j.1365-2745.2008.01362.x	journal	March 2008
MetaQUAST: evaluation of metagenome assemblies Mikheenko, Alla; Saveliev, Vladislav; Gurevich, Alexey Bioinformatics, Vol. 32, Issue 7 https://doi.org/10.1093/bioinformatics/btv697	journal	November 2015
Re-assessment of plant carbon dynamics at the Duke free-air CO2 enrichment site: interactions of atmospheric [CO2] with nitrogen and water availability over stand development McCarthy, Heather R.; Oren, Ram; Johnsen, Kurt H. New Phytologist, Vol. 185, Issue 2 https://doi.org/10.1111/j.1469-8137.2009.03078.x	journal	November 2009
Short-term partitioning of ammonium and nitrate between plants and microbes in an annual grassland Jackson, Louise E.; Schimel, Joshua P.; Firestone, Mary K. Soil Biology and Biochemistry, Vol. 21, Issue 3 https://doi.org/10.1016/0038-0717(89)90152-1	journal	January 1989
Permafrost Meta-Omics and Climate Change Mackelprang, Rachel; Saleska, Scott R.; Jacobsen, Carsten Suhr Annual Review of Earth and Planetary Sciences, Vol. 44, Issue 1 https://doi.org/10.1146/annurev-earth-060614-105126	journal	June 2016
Nitrogen Mineralization: Challenges of a Changing Paradigm Schimel, Joshua P.; Bennett, Jennifer Ecology, Vol. 85, Issue 3 https://doi.org/10.1890/03-8002	journal	March 2004
Reduction of forest soil respiration in response to nitrogen deposition Janssens, I. A.; Dieleman, W.; Luyssaert, S. Nature Geoscience, Vol. 3, Issue 5 https://doi.org/10.1038/ngeo844	journal	April 2010
The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST) Overbeek, Ross; Olson, Robert; Pusch, Gordon D. Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1226	journal	November 2013
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
Deciphering the Principles of Bacterial Nitrogen Dietary Preferences: a Strategy for Nutrient Containment Wang, Jilong; Yan, Dalai; Dixon, Ray mBio, Vol. 7, Issue 4 https://doi.org/10.1128/mBio.00792-16	journal	July 2016
Differential analysis of RNA-seq incorporating quantification uncertainty Pimentel, Harold; Bray, Nicolas L.; Puente, Suzette Nature Methods, Vol. 14, Issue 7 https://doi.org/10.1038/nmeth.4324	journal	June 2017
Microbial Growth and Carbon Use Efficiency in the Rhizosphere and Root-Free Soil Blagodatskaya, Evgenia; Blagodatsky, Sergey; Anderson, Traute-Heidi PLoS ONE, Vol. 9, Issue 4 https://doi.org/10.1371/journal.pone.0093282	journal	April 2014
Nitrogen deposition as an important nutrient from the environment and its impact on ecosystems in China: Nitrogen deposition as an important nutrient from the environment and its impact on ecosystems in China Liu, XueJun; Song, Ling; He, ChunE Journal of Arid Land, Vol. 2, Issue 2 https://doi.org/10.3724/SP.J.1227.2010.00137	journal	June 2010
Systems Biology: The elements and principles of Life Westerhoff, Hans V.; Winder, Catherine; Messiha, Hanan FEBS Letters, Vol. 583, Issue 24 https://doi.org/10.1016/j.febslet.2009.11.018	journal	November 2009
Near-optimal probabilistic RNA-seq quantification Bray, Nicolas L.; Pimentel, Harold; Melsted, Páll Nature Biotechnology, Vol. 34, Issue 5 https://doi.org/10.1038/nbt.3519	journal	April 2016
Field and lab conditions alter microbial enzyme and biomass dynamics driving decomposition of the same leaf litter Rinkes, Zachary L.; Sinsabaugh, Robert L.; Moorhead, Daryl L. Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00260	journal	January 2013
Profile hidden Markov models Eddy, S. R. Bioinformatics, Vol. 14, Issue 9 https://doi.org/10.1093/bioinformatics/14.9.755	journal	October 1998
Nitrogen fertilization inhibits soil microbial respiration regardless of the form of nitrogen applied Ramirez, Kelly S.; Craine, Joseph M.; Fierer, Noah Soil Biology and Biochemistry, Vol. 42, Issue 12 https://doi.org/10.1016/j.soilbio.2010.08.032	journal	December 2010
Detection of Large Numbers of Novel Sequences in the Metatranscriptomes of Complex Marine Microbial Communities Gilbert, Jack A.; Field, Dawn; Huang, Ying PLoS ONE, Vol. 3, Issue 8 https://doi.org/10.1371/journal.pone.0003042	journal	August 2008
FragGeneScan-plus for scalable high-throughput short-read open reading frame prediction Kim, Dongjae; Hahn, Aria S.; Wu, Shang-Ju 2015 IEEE Conference on Computational Intelligence in Bioinformatics and Computational Biology (CIBCB) https://doi.org/10.1109/CIBCB.2015.7300341	conference	August 2015
Nitrogen deposition may enhance soil carbon storage via change of soil respiration dynamic during a spring freeze-thaw cycle period Yan, Guoyong; Xing, Yajuan; Xu, Lijian Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep29134	journal	June 2016
Nitrogen regulation of lignin peroxidase gene transcription. Li, D.; Alic, M.; Gold, M. H. Applied and Environmental Microbiology, Vol. 60, Issue 9 https://doi.org/10.1128/aem.60.9.3447-3449.1994	journal	January 1994
Genetic regulation of nitrogen metabolism in the fungi Marzluf, G. A. Microbiology and Molecular Biology Reviews, Vol. 61, Issue 1 https://doi.org/10.1128/mmbr.61.1.17-32.1997	journal	March 1997
Molecular profiling of microbial community structure and their CAZymes via metagenomics, from Tsomgo lake in the Eastern Himalayas Rai, Aditi; Bhattacharjee, Arindam Archives of Microbiology, Vol. 203, Issue 6 https://doi.org/10.1007/s00203-021-02278-7	journal	April 2021
Extra virgin olive oil improved body weight and insulin sensitivity in high fat diet-induced obese LDLr−/−.Leiden mice without attenuation of steatohepatitis Álvarez-Amor, Leticia; Sierra, Amparo Luque; Cárdenas, Antonio Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-87761-3	journal	April 2021
Polinton-like viruses are abundant in aquatic ecosystems Bellas, Christopher M.; Sommaruga, Ruben Microbiome, Vol. 9, Issue 1 https://doi.org/10.1186/s40168-020-00956-0	journal	January 2021
Microbial Mechanisms Mediating Increased Soil C Storage under Elevated Atmospheric N Deposition Eisenlord, Sarah D.; Freedman, Zachary; Zak, Donald R. Applied and Environmental Microbiology, Vol. 79, Issue 8 https://doi.org/10.1128/aem.00468-13	journal	April 2013
MEGAHIT: An ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph Li, Dinghua; Liu, Chi-Man; Luo, Ruibang arXiv https://doi.org/10.48550/arxiv.1409.7208	preprint	January 2014

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