Effects of bio-based residue amendments on greenhouse gas emission from agricultural soil are stronger than effects of soil type with different microbial community composition

Abstract

With the projected rise in the global human population, agriculture intensification and land-use conversion to arable fields is anticipated to meet the food and bio-energy demand to sustain a growing population. Moving towards a circular economy, agricultural intensification results in the increased re-investment of bio-based residues in agricultural soils, with consequences for microbially mediated greenhouse gas (GHG) emission, as well as other aspects of soil functioning. To date, systematic studies to address the impact of bio-based residue amendment on the GHG balance, including the soil microorganisms, and nutrient transformation in agricultural soils are scarce. Here, we assess the global warming potential (GWP) of in situ GHG (i.e., CO₂, CH₄, and N₂O) fluxes after application of six bio-based residues with broad C : N ratios (5–521) in two agricultural soils (sandy loam and clay; representative of vast production areas in north-western Europe). We relate the GHG emission to the decomposability of the residues in a litter bag assay and determined the effects of residue input on crop (common wheat) growth after incubation. The shift in the bacterial community composition and abundance was monitored using IonTorrent^TM sequencing and qPCR, respectively, by targeting the 16S rRNA gene. The decomposability of the residues, independent of C : N ratio, was proportional to the GWP derived from the GHG emitted. The soils harbored distinct bacterial communities, but responded similarly to the residue amendments, because both soils exhibited the highest mean GWP after addition of the same residues (sewage sludge, aquatic plant material, and compressed beet leaves). Our results question the extent of using the C : N ratio alone to predict residue-induced response in GHG emission. Taken together, we show that although soil properties strongly affect the bacterial community composition, microbially mediated GHG emission is residue dependent.

References Bannert A, Kleineidam K, Wissing L et al. (2011) Changes in diversity and functional gene abundances of microbial communities involved in nitrogen fixation, nitrification, and denitrification in a tidal wetland versus paddy soils cultivated for different time periods. Applied and Environmental Microbiology, 77, 6109–6116. Bastida F, Selevsek N, Torres IF, Hernandez T, Garcia C (2015) Soil restoration with organic amendments: linking cellular functionality and ecosystem processes. Scientific Reports, 5, 15550. Bergmann GT, Bates ST, Eilers KG et al. (2011) The under-recognized dominance of Verrucomicrobia in soil bacterial communities. Soil Biology and Biochemistry, 43, 1450–1455. Caporaso JG, Lauber CL, Costello EK et al. (2011) Moving pictures of the human microbiome. Genome Biology, 12, R50. http://genomebiology.com/2011/12/5/R50 Caporaso JG, Lauber CL, Walters WA et al. (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME Journal, 6, 1621–1624. Cayuela ML, Oenema O, Kuikman PJ, Bakker RR, van Groenigen JW (2010) Bioenergy by-products as soil amendments? Implications for carbon sequestration and greenhouse gas emissions. Global Change Biology Bioenergy, 2, 201–213. Ceja-Navarro JA, Rivera-Orduña FN, Patiño-Zúñiga L, Vila-Sanjurjo A, Crossa J, Govaerts B, Dendooven L (2010) Phylogenetic and multivariate analyses to determine the effects of different tillage and residue management practices on soil bacterial communities. Applied and Environmental Microbiology, 76, 3685–3691. Chen C, Zhang J, Lu M et al. (2016) Microbial communities of an arable soil treated for 8 years with organic and inorganic fertilizers. Biology and Fertility of Soils, 52, 445–467. Cleveland CC, Nemergut DR, Schmidt SK, Townsend AR (2007) Increases in soil respiration following labile carbon additions linked to rapid shifts in soil microbial community composition. Biogeochemistry, 82, 229–240. Cole JR, Wang Q, Fish JA et al. (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acid Research, 42, 633–642. Cong WF, Hoffland E, Li L, Janssen BH, van der Werf W (2015) Intercropping affects the rate of decomposition of soil organic matter and root litter. Plant and Soil, 391, 399–411. Delmont TO, Francioli D, Jacquesson S et al. (2014) Microbial community development and unseen diversity recovery in inoculated sterile soil. Biology and Fertility of Soils, 50, 1069–1076. de Ridder-Duine AS, Smant W, van der Wal A, van Veen JA, de Boer, W. (2006) Evaluation of a simple, non-alkaline extraction protocol to quantify soil ergosterol. Pedobiologia, 50, 293–300. Diacono M, Montemurro F (2010) Long-term effects of organic amendments on soil fertility: a review. Agronomy for Sustainable Development, 30, 401–422. Dodt M, Roehr JT, Ahmed R, Dieterich C (2012) FLEXBAR – Flexible barcode and adapter processing for next-generation sequencing platforms. Biology, I, 895–905. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26, 2460–2461. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27, 2194–2200. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology, 88, 1354–1364. Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biology and Biochemistry, 35, 837–843. Galvez A, Sinicco T, Cayuela ML, Mingorance MD, Fornasier F, Mondini C (2012) Short term effects of bioenergy by-products on soil C and N dynamics, nutrient availability and biochemical properties. Agricultural, Ecosystems and Environment, 160, 3–14. Harter J, Krause H-M, Schuettler S et al. (2014) Linking N₂O emissions from biochar-amended soil to the structure and function of the N-cycling microbial community. ISME Journal, 8, 660–674. Hartmann M, Frey B, Mayer J, Mäder P, Widmer F (2015) Distinct soil microbial diversity under long-term organic and conventional farming. ISME Journal, 9, 1177–1194. Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant and Soil, 311, 1–18. Ho A, Lüke C, Cao Z, Frenzel P (2011) Ageing well: methane oxidation and methane-oxidizing bacteria along a chronosequence of 2000 years. Environmental Microbiology Reports, 3, 738–743. Ho A, Lüke C, Reim A, Frenzel P (2013) Selective stimulation in a natural community of methane oxidizing bacteria: effects of copper on pmoA transcription and activity. Soil Biology and Biochemistry, 65, 211–216. Ho A, El-Hawwary A, Kim SY, Meima-Franke M, Bodelier PLE (2015a) Manure-associated stimulation of soil-borne methanogenic activity in agricultural soils. Biology and Fertility of Soils, 51, 511–516. Ho A, Reim A, Kim SY et al. (2015b) Unexpected stimulation of soil methane uptake as emergent property of agricultural soils following bio-based residue application. Global Change Biology, 21, 3864–3879. Ho A, Di LP, Bodelier PLE (2017) Revisiting life strategy concepts in environmental microbial ecology. FEMS Microbiology Ecology, 93, 1–14: https://doi.org/10.1093/femsec/fix006. de Hollander M (2017) nioo-knaw/hydra: 1.1. https://doi.org/10.5281/zenodo.556539. Huang Y, Zou J, Zheng X, Wang Y, Xu X (2004) Nitrous oxide emissions as influenced by amendment of plant residues with different C: N ratios. Soil Biology and Biochemistry, 36, 973–981. IPCC (2007) Summary for policymakers. In: Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds Parry ML, Canziani OF, Palutikof JP, Van der Linden PJ, Hanson CE), pp. 81–82. Cambridge University Press, Cambridge. Jia Z, Conrad R (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environmental Microbiology, 11, 1658–1671. Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME Journal, 3, 442–453. Joshi NA, Fass JN (2011) Sickle: A sliding-window, adaptive, quality-based trimming tool for FastQ files (version 1.33) Software. Available at: https://github.com/najoshi/sickle. (accessed 15 July 2016). Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. Kielak AM, Barreto CC, Kowalchuk GA, van Veen JA, Kuramae EE (2016) The ecology of Acidobacteria: moving beyond genes and genome. Frontiers in Microbiology, 7, 744. Kim SY, Pramanik P, Gutierrez J, Hwang HY, Kim PJ (2014) Comparison of methane emission characteristics in air-dried and composted cattle manure amended paddy soil during rice cultivation. Agriculture, Ecosystems and Environment, 197, 60–67. Kirkby CA, Richardson AE, Wade LJ, Batten GD, Blanchard C, Kirkegaard JA (2013) Carbon-nutrient stoichiometry to increase soil carbon sequestration. Soil Biology and Biochemistry, 60, 77–86. Köster J, Rahmann S (2012) Snakemake – a scalable bioinformatics workflow engine. Bioinformatics, 28, 2520–2522. Kuramae E, Gamper H, van Veen J, Kowalchuk G (2011) Soil and plant factors driving the community of soil-borne microorganisms across chronosequences of secondary succession of chalk grasslands with a neutral pH. FEMS Microbiology Ecology, 77, 285–294. Kuramae EE, Yergeau E, Wong LC, Pijl AS, van Veen JA, Kowalchuk GA (2012) Soil characteristics more strongly influence soil bacterial communities than land-use type. FEMS Microbiology Ecology, 79, 12–24. Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biology Biochemistry, 40, 2407–2415. Li F, Cao X, Zhao L et al. (2013) Short-term effects of raw rice straw and its derived biochar on greenhouse gas emission in five tropical soils in China. Soil Science and Plant Nutrition, 59, 800–811. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550. McDonald D, Clemente JC, Kuczynski J et al. (2012) The biological observation matric (BIOM) format or: how I learned to stop worrying and love the ome-ome. GigaScience, 1, 7. Mendes R, Kruijt M, de Bruijn I et al. (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science, 332, 1097–1100. Morrissey EM, Mau RL, Schwartz E et al. (2016) Phylogenetic organization of bacterial activity. ISME Journal, 10, 2336–2340. Noll M, Matthies D, Frenzel P, Derakshani M, Liesack W (2005) Succession of bacterial community structure and diversity in a paddy soil oxygen gradient. Environmental Microbiology, 7, 382–395. Odlare M, Abubaker J, Lindmark J, Pell M, Thorin E, Nehrenheim E (2012) Emissions of N₂O and CH₄ from agricultural soils amended with two types of biogas residues. Biomass and Bioenergy, 44, 112–116. Oksanen J, Blanchet F, Kindt R et al. (2015) Vegan: community ecology package. R package version 2.2-1, Available at: http://cran.r-project.org/package=vegan (accessed 1 July 2016). Padmanabhan P, Padmanabhan S, De Rito C et al. (2003) Respiration of 13C-labeled substrates added to soil in the field and subsequent 16S rRNA gene analysis of 13C-labeled soil DNA. Applied and Environmental Microbiology, 69, 1614–1622. Pan Y, Bodrossy L, Frenzel P et al. (2010) Impacts of inter- and intralaboratory variations on the reproducibility of microbial community analyses. Applied and Environmental Microbiology, 76, 7451–7458. Paustian K, Lehmann J, Ogle S, Reay D, Robertson GP, Smith P (2016) Climate-smart soils. Nature, 532, 49–57. Pereire ESP, Suddick EC, Mansour I et al. (2015) Biochar alters nitrogen transformations but has minimal effects on nitrous oxide emissions in an organically managed lettuce mesocosm. Biology Fertility of Soils, 51, 573–582. Price MN, Dehal PS, Arkin AP (2010) FastTree 2 – Approximately maximum-likelihood trees for large alignments. PLoS ONE, 5, 9490. Pruesse E, Quast C, Knittel K et al. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acid Research, 35, 7188–7196. Ranjan K, Paula FS, Mueller RC et al. (2015) Forest-to-pasture conversion increases the diversity of the phylum Verrucomicrobia in Amazon rainforest soils. Frontiers Microbiology, 6, 779. https://doi.org/10.3389/fmicb.2015.00779. R Development Core Team (2012) R: a language and environment for statistical computing, 2.15.1. R Foundation for statistical computing, Vienna, Austria. Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: versatile open source tool for metagenomics. PeerJ, 4, 2584. Ryals R, Hartman MD, Parton WJ, DeLonge MS, Silver WL (2015) Long-term climate change mitigation potential with organic matter management on grasslands. Ecological Applications, 25, 531–545. Shade A. (2016). Diversity is the question, not the answer. ISME Journal, Advanced online publication, https://doi.org/10.1038/ismej.2016.118. Serrano-Silva N, Luna-Guidoa M, Fernández-Luqueño F, Marscha R, Dendooven L (2011) Emission of greenhouse gases from an agricultural soil amended with urea: A laboratory study. Applied Soil Ecology, 47, 92–97. Sengupta A, Dick WA (2015) Bacterial community diversity in soil under two tillage practices as determined by pyrosequencing. Microbial Ecology, 70, 853–859. Stempfhuber B, Richter-Heitmann T, Regan KM et al. (2016) Spatial interaction of archaeal ammonia-oxidizers and nitrite-oxidizing bacteria in an unfertilized grassland soil. Frontiers in Microbiology, 6, 1567. Thomson AJ, Giannopoulos G, Pretty J, Baggs EM, Richardson DJ (2012) Biological sources and sinks of nitrous oxide and strategies to mitigate emissions. Philosophical Transactions of the Royal Society B, 367, 1157–1168. Van der Wal A, van Veen JA, Pijl AS, Summerbell RC, de Boer W (2006) Constraints on development of fungal biomass and decomposition processes during restoration of arable sandy soils. Soil Biology and Biochemistry, 38, 2890–2902. Van der Wal A, Geydan TD, Kuyper TW, de Boer W (2013) A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes. FEMS Microbiology Reviews, 37, 477–494. Wagg C, Bender SF, Widmer F, van der Heijden MGA (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proceedings of the National Academy of Science of the United States of America, 111, 5266–5270. Werling BP, Dickson TL, Isaacs R et al. (2014) Perennial grasslands enhance biodiversity and multiple ecosystem services in bioenergy landscapes. Proceedings of the National Academy of Science of the United States of America, 111, 1652–1657. Ye J, Zhang R, Nielsen S, Joseph SD, Huang D, Thomas T (2016) A combination of biochar-mineral complexes and compost improves soil bacterial processes, soil quality, and plant properties. Frontiers in Microbiology, 7, 372.