Soil biochar amendment affects the diversity of nosZ transcripts: implications for N2O formation
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Microbial nitrogen transformation processes such as denitrification represent major sources of the potent greenhouse gas nitrous oxide (N 2 O). Soil biochar amendment has been shown to significantly decrease N 2 O emissions in various soils. However, the effect of biochar on the structure and function of microbial communities that actively perform nitrogen redox transformations has not been studied in detail yet. To analyse the community composition of actively denitrifying and N 2 O-reducing microbial communities, we collected RNA samples at different time points from a soil microcosm experiment conducted under denitrifying conditions and performed Illumina amplicon sequencing targeting nirK, typical nosZ and atypical nosZ mRNA transcripts. Within 10 days, biochar significantly increased the diversity of nirK and typical nosZ transcripts and resulted in taxonomic shifts among the typical nosZ-expressing microbial community. Furthermore, biochar addition led to a significant increase in transcript production among microbial species that are specialized on direct N 2 O reduction from the environment. Our results point towards a potential coupling of biochar-induced N 2 O emission reduction and an increase in microbial N 2 O reduction activity among specific groups of typical and atypical N 2 O reducers. However, experiments with other soils and biochars will be required to verify the transferability of these findings to other soil-biochar systems.
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Biochar application caused a significant shift in denitrifying and N2O-reducing microbial communities within ten days.
“these researchers investigated denitrifying and N 2 O-reducing microbes at the community level, and found a significant shift within ten days after biochar application (Harter et al., 2017)”
From Comparing straw, compost, and biochar regarding their suitability as agricultural soil amendments to affect soil structure, nutrient leaching, microbial communities, and the fate of pesticides (2021) · cites this paper as Harter et al., 2017
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Biochar effects on soil biota – A review
Lehmann, J., Rillig, M. C., Thies, J., Masiello, C. A., Hockaday, W. C., & Crowley, D. (2011) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2011.04.022 · Cited by 5,074 · see citing works
Atkinson, C. J., Fitzgerald, J. D., & Hipps, N. A. (2010) · Plant and Soil · doi:10.1007/s11104-010-0464-5 · Cited by 2,154 · see citing works
Biochar's role in mitigating soil nitrous oxide emissions: A review and meta-analysis
Cayuela, M. L., van Zwieten, L., Singh, B. P., Jeffery, S., Roig, A., & Sánchez-Monedero, M. A. (2014) · Agriculture, Ecosystems & Environment · doi:10.1016/j.agee.2013.10.009 · Cited by 1,053 · see citing works
Yao, Y., Gao, B., Zhang, M., Inyang, M., & Zimmerman, A. R. (2012) · Chemosphere · doi:10.1016/j.chemosphere.2012.06.002 · Cited by 1,030 · see citing works
Van Zwieten, L., Singh, B. P., Kimber, S. W. L., Murphy, D. V., Macdonald, L. M., Rust, J., & Morris, S. (2014) · Agriculture, Ecosystems & Environment · doi:10.1016/j.agee.2014.02.030 · Cited by 215 · see citing works
Flagged first, then by citations
Research works printed but not linked: 70
- [1]Thomson AJ Giannopoulos G Pretty J Baggs EM Richardson DJ Biological sources and sinks of nitrous oxide and strategies to mitigate emissions Philos Trans R Soc, B 2012 367 1157 1168 10.1098/rstb.2011.0415 PMC3306631 22451101 · DOI
- [2]Hartmann, D. L. et al. In Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds T. F. Stocker et al.) Ch. 2, 159–254 (Cambridge University Press, 2013).
- [3]Ciais, P. et al. In Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds T. F. Stocker et al.) Ch. 6, 465–570 (Cambridge University Press, 2013).
- [5]Smith, P. et al. In Climate Change 2014: Mitigation of Climate Change. Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (eds O. Edenhofer et al.) Ch. 11, 811–922 (Cambridge University Press, 2014).
- [7]Hagemann, N. et al. Does soil aging affect the N2O mitigation potential of biochar? A combined microcosm and field study. GCB Bioenergy, doi:10.1111/gcbb.12390 (2016). · DOI · Paper page
- [9]Sohi SP Agriculture Carbon storage with benefits. Science 2012 338 1034 1035 23180849
- [10]Joseph SD An investigation into the reactions of biochar in soil Aust J Soil Res 2010 48 501 515 10.1071/SR10009 · DOI · Paper page
- [11]Singh B Singh BP Cowie AL Characterisation and evaluation of biochars for their application as a soil amendment Aust J Soil Res 2010 48 516 525 10.1071/SR10058 · DOI · Paper page
- [12]Kuzyakov Y Bogomolova I Glaser B Biochar stability in soil: Decomposition during eight years and transformation as assessed by compound-specific 14C analysis Soil Biol Biochem 2014 70 229 236 10.1016/j.soilbio.2013.12.021 · DOI · Paper page
- [13]Jien SH Wang CS Effects of biochar on soil properties and erosion potential in a highly weathered soil Catena 2013 110 225 233 10.1016/j.catena.2013.06.021 · DOI
- [15]Yu O-Y Raichle B Sink S Impact of biochar on the water holding capacity of loamy sand soil Int J Energy Environ Eng 2013 4 1 9 10.1186/2251-6832-4-44 · DOI
- [16]Cayuela ML Jeffery S van Zwieten L The molar H:Corg ratio of biochar is a key factor in mitigating N2O emissions from soil Agr Ecosyst Environ 2015 202 135 138 10.1016/j.agee.2014.12.015 · DOI · Paper page
- [17]Pfab H N2O fluxes from a Haplic Luvisol under intensive production of lettuce and cauliflower as affected by different N-fertilization strategies J Plant Nutr Soil Sci 2011 174 545 553 10.1002/jpln.201000123 · DOI
- [18]Zona D Impact of extreme precipitation and water table change on N2O fluxes in a bio-energy poplar plantation Biogeosciences Discuss 2011 8 2057 2092 10.5194/bgd-8-2057-2011 · DOI
- [19]Philippot L Hallin S Schloter M Ecology of denitrifying prokaryotes in agricultural soil Adv Agron 2007 96 249 305 10.1016/S0065-2113(07)96003-4 · DOI
- [20]Braker G Conrad R Diversity, structure, and size of N2O-producing microbial communities in soils - what matters for their functioning? Adv Appl Microbiol 2011 75 33 70 10.1016/B978-0-12-387046-9.00002-5 21807245 · DOI
- [21]Richardson D Felgate H Watmough N Thomson A Baggs E Mitigating release of the potent greenhouse gas N2O from the nitrogen cycle - could enzymic regulation hold the key? Trends Biotechnol 2009 27 388 397 10.1016/j.tibtech.2009.03.009 19497629 · DOI
- [22]Bakken LR Bergaust L Liu BB Frostegard A Regulation of denitrification at the cellular level: a clue to the understanding of N2O emissions from soils Philos Trans R Soc, B 2012 367 1226 1234 10.1098/rstb.2011.0321 PMC3306626 22451108 · DOI
- [23]Philippot L Andert J Jones CM Bru D Hallin S Importance of denitrifiers lacking the genes encoding the nitrous oxide reductase for N2O emissions from soil Global Change Biol 2011 17 1497 1504 10.1111/j.1365-2486.2010.02334.x · DOI
- [24]Mckenney DJ Kinetics of Denitrification by Pseudomonas fluorescens: Oxygen Effects Soil Biol Biochem 1994 26 901 908 10.1016/0038-0717(94)90306-9 · DOI
- [25]Zumft, W. G. & Körner, H. In Biology of the Nitrogen Cycle (eds H. Bothe, S. J. Ferguson & W. E. Newton) Ch. 5, 67–82 (Elsevier, 2007).
- [26]Jones CM Graf DR Bru D Philippot L Hallin S The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink Isme J 2013 7 417 426 10.1038/ismej.2012.125 23151640 PMC3554408 · DOI
- [27]Sanford RA Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils P Natl Acad Sci USA 2012 109 19709 19714 10.1073/pnas.1211238109 PMC3511753 23150571 · DOI
- [28]Orellana LH Detecting Nitrous Oxide Reductase (nosZ) Genes in Soil Metagenomes: Method Development and Implications for the Nitrogen Cycle Mbio 2014 5 e01193 01114 10.1128/mBio.01193-14 24895307 PMC4049103 · DOI
- [29]Jones CM Recently identified microbial guild mediates soil N2O sink capacity Nat Clim Change 2014 4 801 805 10.1038/nclimate2301 · DOI
- [30]Anderson CR Biochar induced soil microbial community change: Implications for biogeochemical cycling of carbon, nitrogen and phosphorus Pedobiologia 2011 54 309 320 10.1016/j.pedobi.2011.07.005 · DOI · Paper page
- [31]Xu HJ Biochar Impacts Soil Microbial Community Composition and Nitrogen Cycling in an Acidic Soil Planted with Rape Environ Sci Technol 2014 48 9391 9399 10.1021/es5021058 25054835 · DOI
- [32]Harter J Linking N2O emissions from biochar-amended soil to the structure and function of the N-cycling microbial community Isme J 2014 8 660 674 10.1038/ismej.2013.160 24067258 PMC3930306 · DOI · Paper page
- [33]Harter J Soil biochar amendment shapes the composition of N2O-reducing microbial communities Sci Total Environ 2016 562 379 390 10.1016/j.scitotenv.2016.03.220 27100017 · DOI
- [34]Harter J Gas entrapment and microbial N2O reduction reduce N2O emissions from a biochar-amended sandy clay loam soil Sci Rep 2016 6 39574 10.1038/srep39574 28008997 PMC5180216 · DOI
- [35]Chen JH Consistent increase in abundance and diversity but variable change in community composition of bacteria in topsoil of rice paddy under short term biochar treatment across three sites from South China Appl Soil Ecol 2015 91 68 79 10.1016/j.apsoil.2015.02.012 · DOI
- [36]Anderson CR Hamonts K Clough TJ Condron LM Biochar does not affect soil N-transformations or microbial community structure under ruminant urine patches but does alter relative proportions of nitrogen cycling bacteria Agr Ecosyst Environ 2014 191 63 72 10.1016/j.agee.2014.02.021 · DOI
- [38]Ducey TF Ippolito JA Cantrell KB Novak JM Lentz RD Addition of activated switchgrass biochar to an aridic subsoil increases microbial nitrogen cycling gene abundances Appl Soil Ecol 2013 65 65 72 10.1016/j.apsoil.2013.01.006 · DOI · Paper page
- [39]Lane, D. J. In Nucleic acid techniques in bacterial systematics (eds E. Stackebrandt & M. Godfellow) Ch. 6, 115–175 (Wiley, 1991).
- [40]Wilson KH Blitchington RB Greene RC Amplification of Bacterial 16S Ribosomal DNA with Polymerase Chain Reaction J Clin Microbiol 1990 28 1942 1946 2095137 PMC268083
- [41]Throback IN Enwall K Jarvis A Hallin S Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE Fems Microbiol Ecol 2004 49 401 417 10.1016/j.femsec.2004.04.011 19712290 · DOI
- [42]Henry S Bru D Stres B Hallet S Philippot L Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils Appl Environ Microb 2006 72 5181 5189 10.1128/AEM.00231-06 PMC1538733 16885263 · DOI
- [43]Martin M Cutadapt removes adapter sequences from high-throughput sequencing reads EMBnet. journal 2011 17 17.1.200 10.14806/ej.17.1.200 · DOI · Paper page
- [44]Edgar RC Search and clustering orders of magnitude faster than BLAST Bioinformatics 2010 26 2460 2461 10.1093/bioinformatics/btq461 20709691 · DOI
- [45]Edgar RC Flyvbjerg H Error filtering, pair assembly and error correction for next-generation sequencing reads Bioinformatics 2015 31 3476 3482 10.1093/bioinformatics/btv401 26139637 · DOI
- [46]Edgar RC Haas BJ Clemente JC Quince C Knight R UCHIME improves sensitivity and speed of chimera detection Bioinformatics 2011 27 2194 2200 10.1093/bioinformatics/btr381 21700674 PMC3150044 · DOI · Paper page
- [47]Buchfink B Xie C Huson DH Fast and sensitive protein alignment using DIAMOND Nat Methods 2015 12 59 60 10.1038/nmeth.3176 25402007 · DOI · Paper page
- [48]Huson DH Mitra S Ruscheweyh HJ Weber N Schuster SC Integrative analysis of environmental sequences using MEGAN4 Genome Res 2011 21 1552 1560 10.1101/gr.120618.111 21690186 PMC3166839 · DOI
- [49]Huson DH MEGAN Community Edition - Interactive Exploration and Analysis of Large-Scale Microbiome Sequencing Data PLoS Comput Biol 2016 12 e1004957 10.1371/journal.pcbi.1004957 27327495 PMC4915700 · DOI · Paper page
- [50]Huson DH Auch AF Qi J Schuster SC MEGAN analysis of metagenomic data Genome Res 2007 17 377 386 10.1101/gr.5969107 17255551 PMC1800929 · DOI
- [51]Asnicar F Weingart G Tickle TL Huttenhower C Segata N Compact graphical representation of phylogenetic data and metadata with GraPhlAn Peerj 2015 3 e1029 10.7717/peerj.1029 26157614 PMC4476132 · DOI
- [53]Palmer K Horn MA Denitrification Activity of a Remarkably Diverse Fen Denitrifier Community in Finnish Lapland Is N-Oxide Limited PloS one 2015 10 e0123123 10.1371/journal.pone.0123123 25860353 PMC4393310 · DOI
- [54]Bremer C Impact of plant functional group, plant species, and sampling time on the composition of nirK-Type denitrifier communities in soil Appl Environ Microb 2007 73 6876 6884 10.1128/AEM.01536-07 PMC2074960 17766442 · DOI
- [55]Henry S Disentangling the rhizosphere effect on nitrate reducers and denitrifiers: insight into the role of root exudates Environ Microbiol 2008 10 3082 3092 10.1111/j.1462-2920.2008.01599.x 18393993 · DOI
- [56]Palmer K Biasi C Horn MA Contrasting denitrifier communities relate to contrasting N2O emission patterns from acidic peat soils in arctic tundra Isme J 2012 6 1058 1077 10.1038/ismej.2011.172 22134649 PMC3329112 · DOI
- [57]Hu L Cao L Zhang R Bacterial and fungal taxon changes in soil microbial community composition induced by short-term biochar amendment in red oxidized loam soil World J Microbiol Biotechnol 2014 30 1085 1092 10.1007/s11274-013-1528-5 24136343 · DOI
- [58]Graber ER Biochar impact on development and productivity of pepper and tomato grown in fertigated soilless media Plant Soil 2010 337 481 496 10.1007/s11104-010-0544-6 · DOI · Paper page
- [59]Wang CY The chemical composition of native organic matter influences the response of bacterial community to input of biochar and fresh plant material Plant Soil 2015 395 87 104 10.1007/s11104-015-2621-3 · DOI
- [61]Elboutahiri N Thami-Alami I Udupa SM Phenotypic and genetic diversity in Sinorhizobium meliloti and S. medicae from drought and salt affected regions of Morocco BMC Microbiol 2010 10 15 10.1186/1471-2180-10-15 20089174 PMC2823721 · DOI
- [62]Buendiaclaveria AM Rodrigueznavarro DN Santamarialinaza C Ruizsainz JE Tempranovera F Evaluation of the Symbiotic Properties of Rhizobium fredii in European Soils Syst Appl Microbiol 1994 17 155 160 10.1016/S0723-2020(11)80001-9 · DOI
- [63]Delamuta JRM Polyphasic evidence supporting the reclassification of Bradyrhizobium japonicum group la strains as Bradyrhizobium diazoefficiens sp nov Int J Syst Evol Micr 2013 63 3342 3351 10.1099/ijs.0.049130-0 23504968 · DOI
- [64]Krause A Complete genome of the mutualistic, N2-fixing grass endophyte Azoarcus sp strain BH72 Nat Biotechnol 2006 24 1385 1391 10.1038/nbt1243 17057704 · DOI
- [65]Markowitz VM IMG 4 version of the integrated microbial genomes comparative analysis system Nucleic Acids Res 2014 42 D560 D567 10.1093/nar/gkt963 24165883 PMC3965111 · DOI
- [66]Delgado, M. J., Casella, S. & Bedmar, E. J. In Biology of the Nitrogen Cycle (eds H. Bothe, S. J. Ferguson & W. E. Newton) Ch. 6, 83–91 (Elsevier, 2007).
- [67]Tago K Ishii S Nishizawa T Otsuka S Senoo K Phylogenetic and Functional Diversity of Denitrifying Bacteria Isolated from Various Rice Paddy and Rice-Soybean Rotation Fields Microbes Environ 2011 26 30 35 10.1264/jsme2.ME10167 21487200 · DOI
- [68]Bueno E Anoxic growth of Ensifer meliloti 1021 by N2O-reduction, a potential mitigation strategy Front Microbiol 2015 6 537 10.3389/fmicb.2015.00537 26074913 PMC4443521 · DOI
- [69]Sanchez C Itakura M Mitsui H Minamisawa K Linked Expressions of nap and nos Genes in a Bradyrhizobium japonicum Mutant with Increased N2O Reductase Activity Appl Environ Microb 2013 79 4178 4180 10.1128/AEM.00703-13 PMC3697546 23624475 · DOI
- [70]Zumft WG Kroneck PMH Respiratory transformation of nitrous oxide (N2O) to dinitrogen by Bacteria and Archaea Adv Microb Physiol 2007 52 107 227 10.1016/S0065-2911(06)52003-X 17027372 · DOI
- [71]Graf DRH Jones CM Hallin S Intergenomic Comparisons Highlight Modularity of the Denitrification Pathway and Underpin the Importance of Community Structure for N2O Emissions PloS one 2014 9 e114118 10.1371/journal.pone.0114118 25436772 PMC4250227 · DOI
- [72]Matocha, C. J., Dhakal, P. & Pyzola, S. M. In Advances in Agronomy, Volume 115 (ed. D. L. Sparks) Ch. 4, 181–214 (Academic Press, 2012).
- [74]Khodadad CLM Zimmerman AR Green SJ Uthandi S Foster JS Taxa-specific changes in soil microbial community composition induced by pyrogenic carbon amendments Soil Biol Biochem 2011 43 385 392 10.1016/j.soilbio.2010.11.005 · DOI
- [75]Kappler A Biochar as an Electron Shuttle between Bacteria and Fe(III) Minerals Environmental Science & Technology Letters 2014 1 339 344 10.1021/ez5002209 · DOI
- [76]Hagemann, N., Harter, J. & Behrens, S. In Biochar Application: Essential Soil Microbial Ecology (eds T. Komang Ralebitso-Senior & C. Orr) Ch. 8, 163–198 (Elsevier, 2016).
- [77]Albareda M Rodriguez-Navarro DN Temprano FJ Use of Sinorhizobium (Ensifer) fredii for soybean inoculants in South Spain Eur J Agron 2009 30 205 211 10.1016/j.eja.2008.10.002 · DOI
- [78]Latha S Mahadevan A Role of rhizobia in the degradation of aromatic substances World J Microbiol Biotechnol 1997 13 601 607 10.1023/A:1018598200187 · DOI
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- Authors
- Harter, J., El-Hadidi, M., Huson, D. H., Kappler, A., & Behrens, S.
- Affiliations
- University of Tübingen (DE)
- Nile University (EG)
- University of Minnesota (US)
- Corresponding author
- Behrens, Sebastian
- Venue
- Scientific Reports
- Published
- 2017-06-13
- Volume
- 7
- Issue
- 1
- Pages
- 3338-3338
- ISSN
- 2045-2322 (ISSN-L)
- PMC
- PMC5469825
- OpenAlex
- W2622519622
- Cited by
- 82
- References
- 5
- Citations by year
- 2026: 10 · 2025: 8 · 2024: 8 · 2023: 12 · 2022: 7 · 2021: 7 · 2020: 10 · 2019: 10 · 2018: 10
- FWCI
- 9.00
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Scientific Reports (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- National University of Singapore (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Deutsche Forschungsgemeinschaft
- Argonne National Laboratory
- Topics
- Life Sciences › Agricultural and Biological Sciences › Soil Science › Soil Carbon and Nitrogen Dynamics
- Physical Sciences › Environmental Science › Pollution › Wastewater Treatment and Nitrogen Removal
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Keywords
- nitrous oxide, denitrification, nirK, nitrous oxide reduction, microbial community structure, soil microcosms, greenhouse gas emissions, RNA sequencing
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