Dynamics of microbial community composition and soil organic carbon mineralization in soil following addition of pyrogenic and fresh organic matter

ISME Journal - Tập 10 Số 12 - Trang 2918-2930 - 2016
Thea Whitman1,2, Charles Pepe‐Ranney2, Akio Enders2, Chantal Koechli2, Ashley Campbell2, Daniel H. Buckley2, Johannes Lehmann3,3
1Department of Soil Science, University of Wisconsin-Madison, Madison, WI, USA
2School of Integrative Plant Science, Cornell University, Ithaca, NY, USA
3Atkinson Center for a Sustainable Future, Cornell University , Ithaca, NY, USA

Tóm tắt

Abstract Pyrogenic organic matter (PyOM) additions to soils can have large impacts on soil organic carbon (SOC) cycling. As the soil microbial community drives SOC fluxes, understanding how PyOM additions affect soil microbes is essential to understanding how PyOM affects SOC. We studied SOC dynamics and surveyed soil bacterial communities after OM additions in a field experiment. We produced and mixed in either 350 °C corn stover PyOM or an equivalent initial amount of dried corn stover to a Typic Fragiudept soil. Stover increased SOC-derived and total CO2 fluxes (up to 6x), and caused rapid and persistent changes in bacterial community composition over 82 days. In contrast, PyOM only temporarily increased total soil CO2 fluxes (up to 2x) and caused fewer changes in bacterial community composition. Of the operational taxonomic units (OTUs) that increased in response to PyOM additions, 70% also responded to stover additions. These OTUs likely thrive on easily mineralizable carbon (C) that is found both in stover and, to a lesser extent, in PyOM. In contrast, we also identified unique PyOM responders, which may respond to substrates such as polyaromatic C. In particular, members of Gemmatimonadetes tended to increase in relative abundance in response to PyOM but not to fresh organic matter. We identify taxa to target for future investigations of the mechanistic underpinnings of ecological phenomena associated with PyOM additions to soil.

Từ khóa


Tài liệu tham khảo

Abel, 2013, Impact of biochar and hydrochar addition on water retention and water repellency of sandy soil, Geoderma, 202-203, 183, 10.1016/j.geoderma.2013.03.003

Ameloot, 2013, Interactions between biochar stability and soil organisms: review and research needs, Eur J Soil Sci, 64, 379, 10.1111/ejss.12064

Balesdent, 1996, Mass Spectrometry of Soils

Bartram, 2013, Exploring links between pH and bacterial community composition in soils from the Craibstone Experimental Farm, FEMS Microbiol Ecol, 87, 403, 10.1111/1574-6941.12231

Bates, 2015, Fitting Linear Mixed-Effects Models Using lme4, J Stat Softw, 67, 1, 10.18637/jss.v067.i01

Bernard, 2007, Dynamics and identification of soil microbial populations actively assimilating carbon from 13C-labelled wheat residue as estimated by DNA- and RNA-SIP techniques, Environ Microbiol, 9, 752, 10.1111/j.1462-2920.2006.01197.x

Bingeman, 1953, The effect of the addition of organic materials on the decomposition of an organic soil, Soil Sci Soc Am J, 17, 34, 10.2136/sssaj1953.03615995001700010008x

Blagodatskaya, 2008, Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review, Biol Fertil Soils, 45, 115, 10.1007/s00374-008-0334-y

Blazewicz, 2013, Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses, ISME J, 7, 2061, 10.1038/ismej.2013.102

Burns, 2013, Soil enzymes in a changing environment: current knowledge and future directions, Soil Biol Biochem, 58, 216, 10.1016/j.soilbio.2012.11.009

Caporaso, 2010, QIIME allows analysis of high-throughput community sequencing data, Nat Methods, 7, 335, 10.1038/nmeth.f.303

Chen, 2013, Biochar soil amendment increased bacterial but decreased fungal gene abundance with shifts in community structure in a slightly acid rice paddy from Southwest China, Appl Soil Ecol, 71, 33, 10.1016/j.apsoil.2013.05.003

Cheng, 2008, Natural oxidation of black carbon in soils: Changes in molecular form and surface charge along a climosequence, Geochim Cosmochim Acta, 72, 1598, 10.1016/j.gca.2008.01.010

Czimczik, 2007, Controls on black carbon storage in soils, Global Biogeochem Cycles, 21, GB3005, 10.1029/2006GB002798

DeBruyn, 2011, Global biogeography and quantitative seasonal dynamics of Gemmatimonadetes in soil, Appl Environ Microbiol, 77, 6295, 10.1128/AEM.05005-11

Dunavin, 1969, A comparison of Gahi-1 millet and Grazer A sorghum x sudangrass at several pH levels, Proc Soil Crop Sci Soc Florida, 29, 163

Edgar, 2013, UPARSE: highly accurate OTU sequences from microbial amplicon reads, Nat Methods, 10, 996, 10.1038/nmeth.2604

Enders, 2012, Characterization of biochars to evaluate recalcitrance and agronomic performance, Bioresour Technol, 114, 644, 10.1016/j.biortech.2012.03.022

Fierer, 2007, Toward an ecological classification of soil bacteria, Ecology, 88, 1354, 10.1890/05-1839

Gomez, 2014, Biochar addition rate influences soil microbial abundance and activity in temperate soils, Eur J Soil Sci, 65, 28, 10.1111/ejss.12097

Gul, 2015, Physico-chemical properties and microbial responses in biochar-amended soils: Mechanisms and future directions, Agric Ecosyst Environ, 206, 46, 10.1016/j.agee.2015.03.015

Guereña, 2015, Partitioning the contributions of biochar properties to enhanced biological nitrogen fixation in common bean (Phaseolus vulgaris, Biol Fertil Soils, 51, 479, 10.1007/s00374-014-0990-z

Husson, 2012, Redox potential (Eh) and pH as drivers of soil/plant/microorganism systems: a transdisciplinary overview pointing to integrative opportunities for agronomy, Plant Soil, 362, 389, 10.1007/s11104-012-1429-7

Jeffery, 2011, A quantitative review of the effects of biochar application to soils on crop productivity using meta-analysis, Agric Ecosyst Environ, 144, 175, 10.1016/j.agee.2011.08.015

Jin, 2010, PhD dissertation

Jindo, 2012, Biochar influences the microbial community structure during manure composting with agricultural wastes, Sci Total Environ, 416, 476, 10.1016/j.scitotenv.2011.12.009

Kolton, 2011, Impact of biochar application to soil on the root-associated bacterial community structure of fully developed greenhouse pepper plants, Appl Environ Microbiol, 77, 4924, 10.1128/AEM.00148-11

Kuzyakov, 2004, Using natural 13C abundances to differentiate between three CO2 sources during incubation of a grassland soil amended with slurry and sugar, J Plant Nutr Soil Sci, 167, 669, 10.1002/jpln.200421412

Laird, 2008, The charcoal vision: a win-win-win scenario for simultaneously producing bioenergy, permanently sequestering carbon, while improving soil and water quality, Agronomy J, 100, 178, 10.2134/agronj2007.0161

Lauber, 2009, Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale, Appl Environ Microbiol, 75, 5111, 10.1128/AEM.00335-09

Lehmann, 2007, A handful of carbon, Nature, 447, 143, 10.1038/447143a

Lehmann, 2015, The contentious nature of soil organic matter, Nature, 528, 60, 10.1038/nature16045

Lehmann, 2011, Biochar effects on soil biota—a review, Soil Biol Biochem, 43, 1812, 10.1016/j.soilbio.2011.04.022

Lehmann, 2008, Australian climate–carbon cycle feedback reduced by soil black carbon, Nat Geosci, 1, 832, 10.1038/ngeo358

Lenth, 2016, Least-Squares Means: The R Package lsmeans, J Stat Softw, 69, 1, 10.18637/jss.v069.i01

Love, 2014, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biol, 15, 550, 10.1186/s13059-014-0550-8

Lozupone, 2011, UniFrac: an effective distance metric for microbial community comparison, ISME J, 5, 169, 10.1038/ismej.2010.133

Maestrini, 2014, A meta-analysis on pyrogenic organic matter induced priming effect, GCB Bioenergy, 7, 577, 10.1111/gcbb.12194

Masiello, 2013, Biochar and microbial signaling: production conditions determine effects on microbial communication, Environ Sci Technol, 47, 11496, 10.1021/es401458s

McMurdie, 2014, Waste not, want not: Why rarefying microbiome data is inadmissible, PLoS Comput Biol, 10, e1003531, 10.1371/journal.pcbi.1003531

Mitchell, 2015, Shifts in microbial community and water-extractable organic matter composition with biochar amendment in a temperate forest soil, Soil Biol Biochem, 81, 244, 10.1016/j.soilbio.2014.11.017

Nickerson, 2013, Iso-FD: A novel method for measuring the isotopic signature of surface flux, Soil Biol Biochem, 62, 99, 10.1016/j.soilbio.2013.03.010

Nielsen, 2014, Comparative analysis of the microbial communities in agricultural soil amended with enhanced biochars or traditional fertilisers, Agric Ecosyst Environ, 191, 73, 10.1016/j.agee.2014.04.006

Pascault, 2013, Stimulation of different functional groups of bacteria by various plant residues as a driver of soil priming effect, Ecosystems, 16, 810, 10.1007/s10021-013-9650-7

Pfeiffer, 2013, Leaf litter is the main driver for changes in bacterial community structures in the rhizosphere of ash and beech, Appl Soil Ecol, 72, 150, 10.1016/j.apsoil.2013.06.008

R Core Team, 2015, R: A Language and Environment for Statistical Computing

Rousk, 2010, Soil bacterial and fungal communities across a pH gradient in an arable soil, ISME J, 4, 1340, 10.1038/ismej.2010.58

Schloss, 2009, Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities, Appl Environ Microbiol, 75, 7537, 10.1128/AEM.01541-09

Schimel, 2012, Microbial control over carbon cycling in soil, Front Microbiol, 3, 348, 10.3389/fmicb.2012.00348

Shinners, 2007, Fractional yield and moisture of corn stover biomass produced in the Northern US Corn Belt, Biomass Bioenergy, 31, 576, 10.1016/j.biombioe.2007.02.002

Song, 2014, Biochar addition affected the dynamics of ammonia oxidizers and nitrification in microcosms of a coastal alkaline soil, Biol Fertil Soils, 50, 321, 10.1007/s00374-013-0857-8

Taketani, 2013, Bacterial community composition of anthropogenic biochar and Amazonian anthrosols assessed by 16S rRNA gene 454 pyrosequencing, Antonie van Leeuwenhoek, 104, 233, 10.1007/s10482-013-9942-0

Talbot, 2011, Litter decay rates are determined by lignin chemistry, Biogeochemistry, 108, 279, 10.1007/s10533-011-9599-6

van Es, 2007, Spatially-balanced complete block designs for field experiments, Geoderma, 140, 346, 10.1016/j.geoderma.2007.04.017

Vishnivetskaya, 2011, Mercury and other heavy metals influence bacterial community structure in contaminated Tennessee streams, Appl Environ Microbiol, 77, 302, 10.1128/AEM.01715-10

Watzinger, 2014, Soil microbial communities responded to biochar application in temperate soils and slowly metabolized 13C-labelled biochar as revealed by 13C PLFA analyses: results from a short-term incubation and pot experiment, Eur J Soil Sci, 65, 40, 10.1111/ejss.12100

Werth, 2010, 13C fractionation at the root-microorganisms-soil interface: a review and outlook for partitioning studies, Soil Biol Biochem, 42, 1372, 10.1016/j.soilbio.2010.04.009

Whitman, 2014, Pyrogenic carbon additions to soil counteract positive priming of soil carbon mineralization by plants, Soil Biol Biochem, 73, 33, 10.1016/j.soilbio.2014.02.009

Whitman, 2013, Predicting pyrogenic organic matter mineralization from its initial properties and implications for carbon management, Organic Geochem, 64, 76, 10.1016/j.orggeochem.2013.09.006

Whitman, 2015, A dual-isotope approach to allow conclusive partitioning between three sources, Nat Communs, 6

Whitman, 2010, Biochar projects for mitigating climate change: an investigation of critical methodology issues for carbon accounting, Carbon Manag, 1, 89, 10.4155/cmt.10.4

Whitman, 2015, Biochar for Environmental Management

Whitman, 2014, Carbon mineralizability determines interactive effects on mineralization of pyrogenic organic matter and soil organic carbon, Environ Sci Technol, 48, 13727, 10.1021/es503331y

Woolf, 2012, Modelling the long-term response to positive and negative priming of soil organic carbon by black carbon, Biogeochemistry, 111, 83, 10.1007/s10533-012-9764-6

Xu, 2014, Biochar impacts soil microbial community composition and nitrogen cycling in an acidic soil planted with rape, Environ Sci Technol, 48, 9391, 10.1021/es5021058

Yarza, 2008, The all-species Living Tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains, Syst Appl Microbiol, 31, 241, 10.1016/j.syapm.2008.07.001

Zhang, 2014, PEAR: a fast and accurate Illumina Paired-End reAd mergeR, Bioinformatics, 30, 614, 10.1093/bioinformatics/btt593

Zhang, 2003, Gemmatimonas aurantiaca gen. nov., sp nov., a gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov, Int J Syst Evol Microbiol, 53, 1155, 10.1099/ijs.0.02520-0

Zimmerman, 2010, Abiotic and microbial oxidation of laboratory-produced black carbon (biochar), Environ Sci Technol, 44, 1295, 10.1021/es903140c