Drought re-routes soil microbial carbon metabolism towards emission of volatile metabolites in an artificial tropical rainforest

Honeker, Linnea K.; Pugliese, Giovanni; Ingrisch, Johannes; Fudyma, Jane D.; Gil-Loaiza, Juliana; Carpenter, Elizabeth M.; Singer, Esther; Hildebrand, Gina; Shi, Lingling; Hoyt, David W.; Chu, Rosalie K.; Toyoda, Jason G.; Krechmer, Jordan E.; Claflin, Megan S.; Ayala-Ortiz, Christian O.; Freire-Zapata, Viviana; Pfannerstill, Eva Y.; Daber, L. Erik; Meeran, Kathiravan; Dippold, Michaela A.; Kreuzwieser, Jürgen; Williams, Jonathan; Ladd, S. Nemiah; Werner, Christiane; Tfaily, Malak M.; Meredith, Laura K.

doi:10.1038/s41564-023-01432-9

Drought re-routes soil microbial carbon metabolism towards emission of volatile metabolites in an artificial tropical rainforest

Journal Article · Mon Jul 31 00:00:00 EDT 2023 · Nature Microbiology

DOI:https://doi.org/10.1038/s41564-023-01432-9· OSTI ID:2036569

^[1]; ^[2]; ^[3]; Fudyma, Jane D. ^[4]; ^[1]; Carpenter, Elizabeth M. ^[5]; ^[5]; Hildebrand, Gina ^[1]; Shi, Lingling ^[6]; ^[7]; ^[7]; Toyoda, Jason G. ^[7]; ^[8]; ^[9]; ^[1]; ^[1]; ^[10]; ^[11]; ^[12]; Dippold, Michaela A. ^[6] more »

Univ. of Arizona, Tucson, AZ (United States)
Univ. of Freiburg (Germany); Max Planck Society, Mainz (Germany). Max Planck Inst. for Chemistry
Univ. of Freiburg (Germany); Univ. Innsbruck (Austria)
Univ. of California, Davis, CA (United States); Univ. of Arizona, Tucson, AZ (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Univ. of Tubingen (Germany)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
Aerodyne Research, Inc., Billerica, MA (United States); Bruker Daltonics Inc., Billerica, MA (United States)
Aerodyne Research, Inc., Billerica, MA (United States)
Univ. of California, Berkeley, CA (United States); Max Planck Society, Mainz (Germany). Max Planck Inst. for Chemistry
Univ. of Freiburg (Germany)
Univ. Innsbruck (Austria)
Max Planck Society, Mainz (Germany). Max Planck Inst. for Chemistry
Univ. of Freiburg (Germany); Univ. of Basel (Switzerland)

Drought impacts on microbial activity can alter soil carbon fate and lead to the loss of stored carbon to the atmosphere as CO₂ and volatile organic compounds (VOCs). Here we examined drought impacts on carbon allocation by soil microbes in the Biosphere 2 artificial tropical rainforest by tracking ¹³C from position-specific ¹³C-pyruvate into CO₂ and VOCs in parallel with multi-omics. During drought, efflux of ¹³C-enriched acetate, acetone and C₄H₆O₂ (diacetyl) increased. These changes represent increased production and buildup of intermediate metabolites driven by decreased carbon cycling efficiency. Simultaneously,¹³C-CO₂ efflux decreased, driven by a decrease in microbial activity. However, the microbial carbon allocation to energy gain relative to biosynthesis was unchanged, signifying maintained energy demand for biosynthesis of VOCs and other drought-stress-induced pathways. Overall, while carbon loss to the atmosphere via CO₂ decreased during drought, carbon loss via efflux of VOCs increased, indicating microbially induced shifts in soil carbon fate.

View Accepted Manuscript (DOE)

Research Organization:: Environmental Molecular Sciences Laboratory (EMSL), Richland, WA (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; AC05-76RL01830; SC0021349; SC0023189

OSTI ID:: 2036569

Report Number(s):: PNNL-SA--176253

Journal Information:: Nature Microbiology, Journal Name: Nature Microbiology Journal Issue: 8 Vol. 8; ISSN 2058-5276

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (95)

Dimethyl sulfide in the Amazon rain forest: DMS in the Amazon Jardine, K.; Yañez-Serrano, A. M.; Williams, J. Global Biogeochemical Cycles, Vol. 29, Issue 1 https://doi.org/10.1002/2014GB004969	journal	January 2015
Vertical Stratification of Peat Pore Water Dissolved Organic Matter Composition in a Peat Bog in Northern Minnesota: Pore Water DOM composition in a peat bog Tfaily, Malak M.; Wilson, Rachel M.; Cooper, William T. Journal of Geophysical Research: Biogeosciences, Vol. 123, Issue 2 https://doi.org/10.1002/2017JG004007	journal	February 2018
Measurements of volatile organic compounds in the earth's atmosphere using proton-transfer-reaction mass spectrometry de Gouw, Joost; Warneke, Carsten Mass Spectrometry Reviews, Vol. 26, Issue 2 https://doi.org/10.1002/mas.20119	journal	January 2007
KEGG Mapper for inferring cellular functions from protein sequences Kanehisa, Minoru; Sato, Yoko Protein Science, Vol. 29, Issue 1 https://doi.org/10.1002/pro.3711	journal	August 2019
Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments Kempf, Bettina; Bremer, E. Archives of Microbiology, Vol. 170, Issue 5 https://doi.org/10.1007/s002030050649	journal	September 1998
Short-Term Precipitation Exclusion Alters Microbial Responses to Soil Moisture in a Wet Tropical Forest Waring, Bonnie G.; Hawkes, Christine V. Microbial Ecology, Vol. 69, Issue 4 https://doi.org/10.1007/s00248-014-0436-z	journal	June 2014
Volatile organic compounds (VOCs) in soils Insam, Heribert; Seewald, Martin S. A. Biology and Fertility of Soils, Vol. 46, Issue 3 https://doi.org/10.1007/s00374-010-0442-3	journal	February 2010
Drought differentially affects autotrophic and heterotrophic soil respiration rates and their temperature sensitivity Sun, Shouqin; Lei, Haiqing; Chang, Scott X. Biology and Fertility of Soils, Vol. 55, Issue 3 https://doi.org/10.1007/s00374-019-01347-w	journal	February 2019
Volatile methanol and acetone additions increase labile soil carbon and inhibit nitrification McBride, Steven G.; Osburn, Ernest D.; Barrett, John E. Biogeochemistry, Vol. 145, Issue 1-2 https://doi.org/10.1007/s10533-019-00595-0	journal	September 2019
Vegetation controls methane emissions in a coastal brackish fen Koebsch, Franziska; Glatzel, Stephan; Jurasinski, Gerald Wetlands Ecology and Management, Vol. 21, Issue 5 https://doi.org/10.1007/s11273-013-9304-8	journal	June 2013
Changes in soil heterotrophic respiration, carbon availability, and microbial function in seven forests along a climate gradient Fang, Huajun; Cheng, Shulan; Wang, Yongsheng Ecological Research, Vol. 29, Issue 6 https://doi.org/10.1007/s11284-014-1194-6	journal	August 2014
Effects of biochar application in forest ecosystems on soil properties and greenhouse gas emissions: a review Li, Yongfu; Hu, Shuaidong; Chen, Junhui Journal of Soils and Sediments, Vol. 18, Issue 2 https://doi.org/10.1007/s11368-017-1906-y	journal	December 2017
Crystalline flavin pyruvate oxidase from Escherichia coli Williams, F. Robert; Hager, Lowell P. Archives of Biochemistry and Biophysics, Vol. 116 https://doi.org/10.1016/0003-9861(66)90025-7	journal	January 1966
A direct interaction between the H+-F1F0-ATPase and the K+ transport within the membrane of anaerobically grown bacteria Trchounian, Armen A. Bioelectrochemistry and Bioenergetics, Vol. 33, Issue 1 https://doi.org/10.1016/0302-4598(94)87026-8	journal	February 1994
Identification of volatile sporostatic factors from cultures of Fusarium oxysporum Robinson, P. M.; Garrett, M. K. Transactions of the British Mycological Society, Vol. 52, Issue 2 https://doi.org/10.1016/S0007-1536(69)80042-2	journal	April 1969
Reconstitution of the Ubiquinone-dependent pyruvate oxidase system of Escherichia coli with the cytochrome o terminal oxidase complex. Carter, K.; Gennis, R. B. Journal of Biological Chemistry, Vol. 260, Issue 20 https://doi.org/10.1016/S0021-9258(17)39135-4	journal	September 1985
Tropical rainforest biome of Biosphere 2: Structure, composition and results of the first 2 years of operation Leigh, Linda S.; Burgess, Tony; Marino, Bruno D. V. Ecological Engineering, Vol. 13, Issue 1-4 https://doi.org/10.1016/S0925-8574(98)00092-5	journal	June 1999
BVOCs: plant defense against climate warming? Peñuelas, J. Trends in Plant Science, Vol. 8, Issue 3 https://doi.org/10.1016/S1360-1385(03)00008-6	journal	March 2003
Sensitivity and specificity of atmospheric trace gas detection by proton-transfer-reaction mass spectrometry de Gouw, Joost; Warneke, Carsten; Karl, Thomas International Journal of Mass Spectrometry, Vol. 223-224 https://doi.org/10.1016/S1387-3806(02)00926-0	journal	January 2003
Sequential extraction protocol for organic matter from soils and sediments using high resolution mass spectrometry Tfaily, Malak M.; Chu, Rosalie K.; Toyoda, Jason Analytica Chimica Acta, Vol. 972 https://doi.org/10.1016/j.aca.2017.03.031	journal	June 2017
Drought stress induced increase of fungi:bacteria ratio in a poplar plantation Sun, Yuan; Chen, Han Y. H.; Jin, Long CATENA, Vol. 193 https://doi.org/10.1016/j.catena.2020.104607	journal	October 2020
Industrial PLS model variable selection using moving window variable importance in projection Lu, Bo; Castillo, Ivan; Chiang, Leo Chemometrics and Intelligent Laboratory Systems, Vol. 135 https://doi.org/10.1016/j.chemolab.2014.03.020	journal	July 2014
Research frontiers in climate change: Effects of extreme meteorological events on ecosystems Jentsch, Anke; Beierkuhnlein, Carl Comptes Rendus Geoscience, Vol. 340, Issue 9-10 https://doi.org/10.1016/j.crte.2008.07.002	journal	September 2008
Re-characterisation of Saccharomyces cerevisiae Ach1p: Fungal CoA-transferases are involved in acetic acid detoxification Fleck, Christian B.; Brock, Matthias Fungal Genetics and Biology, Vol. 46, Issue 6-7 https://doi.org/10.1016/j.fgb.2009.03.004	journal	June 2009
Drought changed soil organic carbon composition and bacterial carbon metabolizing patterns in a subtropical evergreen forest Su, Xin; Su, Xueling; Yang, Songchen Science of The Total Environment, Vol. 736 https://doi.org/10.1016/j.scitotenv.2020.139568	journal	September 2020
Interannual and interseasonal soil CO2 efflux and VOC exchange rates in a Mediterranean holm oak forest in response to experimental drought Asensio, Dolores; Peñuelas, Josep; Llusià, Joan Soil Biology and Biochemistry, Vol. 39, Issue 10 https://doi.org/10.1016/j.soilbio.2007.04.019	journal	October 2007
Probing carbon flux patterns through soil microbial metabolic networks using parallel position-specific tracer labeling Dijkstra, Paul; Blankinship, Joseph C.; Selmants, Paul C. Soil Biology and Biochemistry, Vol. 43, Issue 1 https://doi.org/10.1016/j.soilbio.2010.09.022	journal	January 2011
Modeling soil metabolic processes using isotopologue pairs of position-specific 13C-labeled glucose and pyruvate Dijkstra, Paul; Dalder, Jacob J.; Selmants, Paul C. Soil Biology and Biochemistry, Vol. 43, Issue 9 https://doi.org/10.1016/j.soilbio.2011.05.001	journal	September 2011
Response of osmolytes in soil to drying and rewetting Warren, Charles R. Soil Biology and Biochemistry, Vol. 70 https://doi.org/10.1016/j.soilbio.2013.12.008	journal	March 2014
Partitioning sources of CO2 emission after soil wetting using high-resolution observations and minimal models Slessarev, Eric W.; Schimel, Joshua P. Soil Biology and Biochemistry, Vol. 143 https://doi.org/10.1016/j.soilbio.2020.107753	journal	April 2020
Rates of dark CO2 fixation are driven by microbial biomass in a temperate forest soil Akinyede, Rachael; Taubert, Martin; Schrumpf, Marion Soil Biology and Biochemistry, Vol. 150 https://doi.org/10.1016/j.soilbio.2020.107950	journal	November 2020
Use of metabolomics to quantify changes in soil microbial function in response to fertiliser nitrogen supply and extreme drought Brown, Robert W.; Chadwick, David R.; Zang, Huadong Soil Biology and Biochemistry, Vol. 160 https://doi.org/10.1016/j.soilbio.2021.108351	journal	September 2021
Capturing the microbial volatilome: an oft overlooked 'ome' Meredith, Laura K.; Tfaily, Malak M. Trends in Microbiology, Vol. 30, Issue 7 https://doi.org/10.1016/j.tim.2021.12.004	journal	July 2022
Advanced Solvent Based Methods for Molecular Characterization of Soil Organic Matter by High-Resolution Mass Spectrometry Tfaily, Malak M.; Chu, Rosalie K.; Tolić, Nikola Analytical Chemistry, Vol. 87, Issue 10 https://doi.org/10.1021/acs.analchem.5b00116	journal	April 2015
Formularity: Software for Automated Formula Assignment of Natural and Other Organic Matter from Ultrahigh-Resolution Mass Spectra Tolić, Nikola; Liu, Yina; Liyu, Andrey Analytical Chemistry, Vol. 89, Issue 23 https://doi.org/10.1021/acs.analchem.7b03318	journal	November 2017
Evaluation of a New Reagent-Ion Source and Focusing Ion–Molecule Reactor for Use in Proton-Transfer-Reaction Mass Spectrometry Krechmer, Jordan; Lopez-Hilfiker, Felipe; Koss, Abigail Analytical Chemistry, Vol. 90, Issue 20 https://doi.org/10.1021/acs.analchem.8b02641	journal	September 2018
Elucidating Drought-Tolerance Mechanisms in Plant Roots through ¹H NMR Metabolomics in Parallel with MALDI-MS, and NanoSIMS Imaging Techniques Honeker, Linnea K.; Hildebrand, Gina A.; Fudyma, Jane D. Environmental Science & Technology, Vol. 56, Issue 3 https://doi.org/10.1021/acs.est.1c06772	journal	January 2022
MestRe Nova Willcott, Mark Robert Journal of the American Chemical Society, Vol. 131, Issue 36 https://doi.org/10.1021/ja906709t	journal	August 2009
Ecological consequences of the phylogenetic and physiological diversities of acetogens Drake, Harold L.; Küsel, Kirsten; Matthies, Carola Antonie van Leeuwenhoek, Vol. 81, Issue 1/4, p. 203-213 https://doi.org/10.1023/A:1020514617738	journal	December 2002
Responses of soil bacterial and fungal communities to extreme desiccation and rewetting Barnard, Romain L.; Osborne, Catherine A.; Firestone, Mary K. The ISME Journal, Vol. 7, Issue 11 https://doi.org/10.1038/ismej.2013.104	journal	July 2013
Soil microorganisms can overcome respiration inhibition by coupling intra- and extracellular metabolism: 13C metabolic tracing reveals the mechanisms K. Bore, Ezekiel; Apostel, Carolin; Halicki, Sara The ISME Journal, Vol. 11, Issue 6 https://doi.org/10.1038/ismej.2017.3	journal	February 2017
Climate extremes and the carbon cycle Reichstein, Markus; Bahn, Michael; Ciais, Philippe Nature, Vol. 500, Issue 7462 https://doi.org/10.1038/nature12350	journal	August 2013
Strong sesquiterpene emissions from Amazonian soils Bourtsoukidis, E.; Behrendt, T.; Yañez-Serrano, A. M. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-04658-y	journal	June 2018
Drought-induced soil microbial amino acid and polysaccharide change and their implications for C-N cycles in a climate change world Kakumanu, Madhavi L.; Ma, Li; Williams, Mark A. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-46984-1	journal	July 2019
Effect of elevated CO2 concentration and vapour pressure deficit on isoprene emission from leaves of Populus deltoides during drought Pegoraro, Emiliano; Rey, Ana; Bobich, Edward G. Functional Plant Biology, Vol. 31, Issue 12 https://doi.org/10.1071/FP04142	journal	January 2004
Urban flux measurements reveal a large pool of oxygenated volatile organic compound emissions Karl, T.; Striednig, M.; Graus, M. Proceedings of the National Academy of Sciences, Vol. 115, Issue 6 https://doi.org/10.1073/pnas.1714715115	journal	January 2018
Functional Characterization and Localization of Acetyl-CoA Hydrolase, Ach1p, in Saccharomyces cerevisiae Buu, Leh-Miauh; Chen, Yee-Chun; Lee, Fang-Jen S. Journal of Biological Chemistry, Vol. 278, Issue 19 https://doi.org/10.1074/jbc.M213268200	journal	February 2003
The Acetone-Butanol-Ethanol Fermentation: Recent Progress in Technology Maddox, Ian S. Biotechnology and Genetic Engineering Reviews, Vol. 7, Issue 1 https://doi.org/10.1080/02648725.1989.10647859	journal	December 1989
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
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
Differences in substrate use linked to divergent carbon flow during litter decomposition Albright, Michaeline B. N.; Thompson, Jaron; Kroeger, Marie E. FEMS Microbiology Ecology, Vol. 96, Issue 8 https://doi.org/10.1093/femsec/fiaa135	journal	July 2020
Ach1 is involved in shuttling mitochondrial acetyl units for cytosolic C2 provision in Saccharomyces cerevisiae lacking pyruvate decarboxylase Chen, Yun; Zhang, Yiming; Siewers, Verena FEMS Yeast Research, Vol. 15, Issue 3 https://doi.org/10.1093/femsyr/fov015	journal	April 2015
tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence Lowe, Todd M.; Eddy, Sean R. Nucleic Acids Research, Vol. 25, Issue 5 https://doi.org/10.1093/nar/25.5.955	journal	March 1997
Pyruvate oxidase contributes to the aerobic growth efficiency of Escherichia coli Abdel-Hamid, Ahmed M.; Attwood, Margaret M.; Guest, John R. Microbiology, Vol. 147, Issue 6 https://doi.org/10.1099/00221287-147-6-1483	journal	June 2001
Leaf-level metabolic changes in response to drought affect daytime CO₂ emission and isoprenoid synthesis pathways Ladd, S. Nemiah; Daber, L. Erik; Bamberger, Ines https://doi.org/10.1101/2022.04.29.490001	posted_content	March 2023
Adaptive seeds tame genomic sequence comparison Kielbasa, S. M.; Wan, R.; Sato, K. Genome Research, Vol. 21, Issue 3 https://doi.org/10.1101/gr.113985.110	journal	January 2011
metaSPAdes: a new versatile metagenomic assembler Nurk, Sergey; Meleshko, Dmitry; Korobeynikov, Anton Genome Research, Vol. 27, Issue 5 https://doi.org/10.1101/gr.213959.116	journal	March 2017
Modeling leaderless transcription and atypical genes results in more accurate gene prediction in prokaryotes Lomsadze, Alexandre; Gemayel, Karl; Tang, Shiyuyun Genome Research, Vol. 28, Issue 7 https://doi.org/10.1101/gr.230615.117	journal	May 2018
Drought impacts on microbial trait distribution and feedback to soil carbon cycling Malik, Ashish A.; Bouskill, Nicholas J. Functional Ecology, Vol. 36, Issue 6 https://doi.org/10.1111/1365-2435.14010	journal	February 2022
Drought-induced nitrous oxide flux dynamics in an enclosed tropical forest van Haren, Joost L. M.; Handley, Linda L.; Biel, Karl Y. Global Change Biology, Vol. 11, Issue 8 https://doi.org/10.1111/j.1365-2486.2005.00987.x	journal	August 2005
Drought effect on isoprene production and consumption in Biosphere 2 tropical rainforest: ISOPRENE FLUXES IN A TROPICAL RAINFOREST MESOCOSM Pegoraro, Emiliano; Rey, Ana; Abrell, Leif Global Change Biology, Vol. 12, Issue 3 https://doi.org/10.1111/j.1365-2486.2006.01112.x	journal	March 2006
ggplot2: Elegant Graphics for Data Analysis by WICKHAM, H. Wilkinson, Leland Biometrics, Vol. 67, Issue 2 https://doi.org/10.1111/j.1541-0420.2011.01616.x	journal	June 2011
Biogenic volatile emissions from the soil: Biogenic volatile emissions from the soil PeÑUelas, J.; Asensio, D.; Tholl, D. Plant, Cell & Environment, Vol. 37, Issue 8 https://doi.org/10.1111/pce.12340	journal	May 2014
Ecosystem fluxes during drought and recovery in an experimental forest Werner, Christiane; Meredith, Laura K.; Ladd, S. Nemiah Science, Vol. 374, Issue 6574 https://doi.org/10.1126/science.abj6789	journal	December 2021
Role of Acetyl Coenzyme A Synthesis and Breakdown in Alternative Carbon Source Utilization in Candida albicans Carman, Aaron J.; Vylkova, Slavena; Lorenz, Michael C. Eukaryotic Cell, Vol. 7, Issue 10 https://doi.org/10.1128/EC.00253-08	journal	October 2008
Pyruvate:Quinone Oxidoreductase from Corynebacterium glutamicum : Purification and Biochemical Characterization Schreiner, Mark E.; Eikmanns, Bernhard J. Journal of Bacteriology, Vol. 187, Issue 3 https://doi.org/10.1128/JB.187.3.862-871.2005	journal	February 2005
The Acetate Switch Wolfe, Alan Microbiology and Molecular Biology Reviews, Vol. 69, Issue 1, p. 12-50 https://doi.org/10.1128/MMBR.69.1.12-50.2005	journal	March 2005
Volatile metabolites produced by six fungal species compared with other indicators of fungal growth on cereal grains Börjesson, T.; Stöllman, U.; Schnürer, J. Applied and Environmental Microbiology, Vol. 58, Issue 8 https://doi.org/10.1128/aem.58.8.2599-2605.1992	journal	August 1992
DOE JGI Metagenome Workflow Clum, Alicia; Huntemann, Marcel; Bushnell, Brian mSystems, Vol. 6, Issue 3 https://doi.org/10.1128/mSystems.00804-20	journal	June 2021
Biosynthesis of α-acetolactate and its conversion to diacetyl and acetoin in cell-free extracts of Lactobacillus casei Branen, A. L.; Keenan, T. W. Canadian Journal of Microbiology, Vol. 18, Issue 4 https://doi.org/10.1139/m72-074	journal	April 1972
Life in Dry Soils: Effects of Drought on Soil Microbial Communities and Processes Schimel, Joshua P. Annual Review of Ecology, Evolution, and Systematics, Vol. 49, Issue 1 https://doi.org/10.1146/annurev-ecolsys-110617-062614	journal	November 2018
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
CRISPR Recognition Tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats Bland, Charles; Ramsey, Teresa L.; Sabree, Fareedah BMC Bioinformatics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2105-8-209	journal	June 2007
WGCNA: an R package for weighted correlation network analysis Langfelder, Peter; Horvath, Steve BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-559	journal	December 2008
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
MetaboDirect: an analytical pipeline for the processing of FT-ICR MS-based metabolomic data Ayala-Ortiz, Christian; Graf-Grachet, Nathalia; Freire-Zapata, Viviana Microbiome, Vol. 11, Issue 1 https://doi.org/10.1186/s40168-023-01476-3	journal	February 2023
BBMerge – Accurate paired shotgun read merging via overlap Bushnell, Brian; Rood, Jonathan; Singer, Esther PLOS ONE, Vol. 12, Issue 10 https://doi.org/10.1371/journal.pone.0185056	journal	October 2017
Real-time carbon allocation into biogenic volatile organic compounds (BVOCs) and respiratory carbon dioxide (CO2) traced by PTR-TOF-MS, 13CO2 laser spectroscopy and 13C-pyruvate labelling Fasbender, Lukas; Yáñez-Serrano, Ana Maria; Kreuzwieser, Jürgen PLOS ONE, Vol. 13, Issue 9 https://doi.org/10.1371/journal.pone.0204398	journal	September 2018
Exopolysaccharide Production by Drought Tolerant Bacillus spp. and Effect on soil Aggregation Under Drought Stress Vardharajula, Sandhya; Sk Z., Ali Journal of microbiology, biotechnology and food sciences, Vol. 4, Issue 1 https://doi.org/10.15414/jmbfs.2014.4.1.51-57	journal	August 2014
The pls Package: Principal Component and Partial Least Squares Regression in R Mevik, Bjørn-Helge; Wehrens, Ron Journal of Statistical Software, Vol. 18, Issue 2 https://doi.org/10.18637/jss.v018.i02	journal	January 2007
Fast R Functions for Robust Correlations and Hierarchical Clustering Langfelder, Peter; Horvath, Steve Journal of Statistical Software, Vol. 46, Issue 11 https://doi.org/10.18637/jss.v046.i11	journal	January 2012
Microbial Stress-Response Physiology and its Implications for Ecosystem Function Schimel, Joshua; Balser, Teri C.; Wallenstein, Matthew Ecology, Vol. 88, Issue 6 https://doi.org/10.1890/06-0219	journal	June 2007
The Acetone-Butanol-Ethanol Fermentation Awang, Gregor M.; Jones, G. A.; Ingledew, W. M. CRC Critical Reviews in Microbiology, Vol. 15, Issue sup1 https://doi.org/10.3109/10408418809104464	journal	January 1988
The Volatilome: A Vital Piece of the Complete Soil Metabolome Honeker, Linnea K.; Graves, Kelsey R.; Tfaily, Malak M. Frontiers in Environmental Science, Vol. 9 https://doi.org/10.3389/fenvs.2021.649905	journal	April 2021
Microbial control over carbon cycling in soil Schimel, Joshua P.; Schaeffer, Sean M. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00348	journal	January 2012
Single-throughput Complementary High-resolution Analytical Techniques for Characterizing Complex Natural Organic Matter Mixtures Tfaily, Malak M.; Wilson, Rachel M.; Brewer, Heather M. Journal of Visualized Experiments, Issue 143 https://doi.org/10.3791/59035	journal	January 2019
A simple and efficient method for the solid-phase extraction of dissolved organic matter (SPE-DOM) from seawater: SPE-DOM from seawater Dittmar, Thorsten; Koch, Boris; Hertkorn, Norbert Limnology and Oceanography: Methods, Vol. 6, Issue 6 https://doi.org/10.4319/lom.2008.6.230	journal	June 2008
Measurements of delays of gas-phase compounds in a wide variety of tubing materials due to gas–wall interactions Deming, Benjamin L.; Pagonis, Demetrios; Liu, Xiaoxi Atmospheric Measurement Techniques, Vol. 12, Issue 6 https://doi.org/10.5194/amt-12-3453-2019	journal	January 2019
Validity and limitations of simple reaction kinetics to calculate concentrations of organic compounds from ion counts in PTR-MS Holzinger, Rupert; Acton, W. Joe F.; Bloss, William J. Atmospheric Measurement Techniques, Vol. 12, Issue 11 https://doi.org/10.5194/amt-12-6193-2019	journal	November 2019
An in situ gas chromatograph with automatic detector switching between PTR- and EI-TOF-MS: isomer-resolved measurements of indoor air Claflin, Megan S.; Pagonis, Demetrios; Finewax, Zachary Atmospheric Measurement Techniques, Vol. 14, Issue 1 https://doi.org/10.5194/amt-14-133-2021	journal	January 2021
PTRwid: A new widget tool for processing PTR-TOF-MS data Holzinger, R. Atmospheric Measurement Techniques, Vol. 8, Issue 9 https://doi.org/10.5194/amt-8-3903-2015	journal	January 2015
Reviews and syntheses: Heterotrophic fixation of inorganic carbon – significant but invisible flux in environmental carbon cycling Braun, Alexander; Spona-Friedl, Marina; Avramov, Maria Biogeosciences, Vol. 18, Issue 12 https://doi.org/10.5194/bg-18-3689-2021	journal	June 2021
Versatile soil gas concentration and isotope monitoring: optimization and integration of novel soil gas probes with online trace gas detection Gil-Loaiza, Juliana; Roscioli, Joseph R.; Shorter, Joanne H. Biogeosciences, Vol. 19, Issue 1 https://doi.org/10.5194/bg-19-165-2022	journal	January 2022
Vertical Stratification Of Peat Pore Water Dissolved Organic Matter Composition In A Peat Bog In Northern Minnesota Tfaily, Malak M.; Wilson, Rachel M.; William, Cooper T. Zenodo https://doi.org/10.5281/zenodo.816210	dataset	January 2017
Drought re-routes soil microbial carbon metabolism towards emission of volatile metabolites in an artificial tropical rainforest Honeker, Linnea; Pugliese, Giovanni; Ingrisch, Johannes figshare https://doi.org/10.6084/m9.figshare.20334537	dataset	January 2023

Similar Records

Microbial growth under drought is confined to distinct taxa and modified by potential future climate conditions

Journal Article · Thu Sep 21 20:00:00 EDT 2023 · Nature Communications · OSTI ID:2229517

Belowground Response to Drought in a Tropical Forest Soil. II. Change in Microbial Function Impacts Carbon Composition

Journal Article · Mon Mar 14 20:00:00 EDT 2016 · Frontiers in Microbiology · OSTI ID:1379159

Green Leaf Volatile Emissions during High Temperature and Drought Stress in a Central Amazon Rainforest

Journal Article · Mon Aug 31 20:00:00 EDT 2015 · Plants · OSTI ID:1512246

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
bacterial genes
biogeochemistry
carbon
drought
metagenomics
metatranscriptomics
microbial VOC
soil microbial ecology
stable isotope
tropical rainforest

Drought re-routes soil microbial carbon metabolism towards emission of volatile metabolites in an artificial tropical rainforest

Citation Formats

References (95)

Similar Records

Related Subjects