Cited by 76Soil Carbon and Nitrogen DynamicsPlant-Microbe Interactions and ImmunityMicrobial Community Ecology and Physiology

The DOI matches its Crossref record; the references it cites are not checked yet.

Biochar Amendment Stimulates Utilization of Plant-Derived Carbon by Soil Bacteria in an Intercropping System

Open access
Liao, Hongkai, Li, Yaying, Yao, Huaiying·2019·Frontiers in Microbiology

Abstract

Plant-derived carbon (C) is considered fundamental to understand the interaction between rhizosphere microbes and plants in terrestrial ecosystems. Biochar soil amendment may enhance plant performance via changing soil properties or microbial diversity in the rhizosphere. However, our knowledge of how plant-microbiome associations respond to biochar amendment remains rather limited. Herein, 13CO2 steady-state labeling combined with DNA-SIP (stable isotope probing) was used to characterize the microbial communities contributing to the metabolization of plant-derived C. The diversity of soil microbes active in the utilization of root exudates was determined during biochar amendment in a legume-based intercropping system (Vicia faba L., with Zea mays L.). The results show the biochar application not only changed the soil microbial community structure and diversity in the rhizosphere, but also altered soil microbiome members actively assimilating plant-derived C. There were more labeled microbial species in the biochar-amended soils compared with control soils. In the rhizosphere, relative to the controls the biochar amendment increased the relative abundances of Firmicutes and Bacteroidetes members (i.e., Bacillus, Clostridium, Sporomusa, Desulfosporosinus, and Alicyclobacillus) while decreasing the relative abundance of Proteobacteria members (e.g., Methylobacterium and Sphingomonas) utilizing plant-derived C. In contrast, slow-growing bacterial species of the phylum Acidobacteria, Planctomycetes, and Gemmatimonadetes were barely labeled. The microbes found stimulated by the biochar amendment are known for their ability to fix nitrogen, solubilize phosphorus, or reduce iron and sulfur, which may potentially contribute to the ‘biochar effect’ in the rhizosphere. This study is the first to provide empirical evidence that biochar amendment can alter soil microbiome assimilating plant-derived C; this may have consequences for nutrient cycling and improving plant performance in intercropping systems.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fmicb.2019.01361

Cites

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

The citation lists haven’t been fetched yet

References 66 · Cited by 76

Research works printed but not linked: 67

  1. Abel, 2013, Impact of biochar and hydrochar addition on water retention and water repellency of sandy soil., Geoderma, 202, 183, 10.1016/j.geoderma.2013.03.003 · DOI · Paper page
  2. Angel, 2018, Application of stable-isotope labelling techniques for the detection of active diazotrophs., Environ. Microbiol., 20, 44, 10.1111/1462-2920.13954 · DOI
  3. Badri, 2013, Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome., J. Biol. Chem., 288, 4502, 10.1074/jbc.M112.433300 · DOI
  4. Baetz, 2014, Root exudates: the hidden part of palnt defense., Trends Plant Sci., 19, 90, 10.1016/j.tplants.2013.11.006 · DOI
  5. Bao, 1999, Analytical Methods of Soil Agrochemistry (in Chinese).
  6. Benjamini, 1995, Controlling the false discovery rate: a practical and powerful approach to multiple testing., J. R. stat. Soc. Ser. B Stat. Methodol., 57, 289, 10.1111/j.2517-6161.1995.tb02031.x · DOI · Paper page
  7. Caporaso, 2010, QIIME allows analysis of high-throughput community sequencing data., Nat. Methods, 7, 335, 10.1038/nmeth.f.303 · DOI · Paper page
  8. Chapelle, 2016, Fungal invasion of the rhizosphere microbiome., ISME J., 10, 265, 10.1038/ismej.2015.82 · DOI · Paper page
  9. Dalal, 2003, Nitrous oxide emission from Australian agricultural lands and mitigation options: a review., Soil Res., 41, 165, 10.1071/SR02064 · DOI
  10. De Visser, 1997, Kinetics and relative significance of remobilized and current C and N incorporation in leaf and root growth zones of Lolium perenne after defoliation: assessment by 13C and 15N steady-state labelling., Plant Cell. Environ., 20, 37, 10.1046/j.1365-3040.1997.d01-9.x · DOI
  11. Ding, 2017, Bacterial succession along a long-term chronosequence of paddy soil in the Yangtze River Delta., China Soil Biol. Biochem., 104, 59, 10.1016/j.soilbio.2016.10.013 · DOI
  12. Ding, 2015, Long-term nitrogen fertilization of paddy soil shifts iron-reducing microbial community revealed by RNA-13C-acetate probing coupled with pyrosequencing., ISME J., 9, 721, 10.1038/ismej.2014.159 · DOI
  13. Ding, 2016, Biochar to improve soil fertility. a review., Agron. Sustain. Dev., 36, 10.1007/s13593-016-0372-z · DOI · Paper page
  14. Drigo, 2010, Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2., Proc. Natl. Acad. Sci. U.S.A., 107, 10938, 10.1073/pnas.0912421107 · DOI
  15. Edgar, 2010, Search and clustering orders of magnitude faster than BLAST., Bioinformatics, 26, 2460, 10.1093/bioinformatics/btq461 · DOI
  16. Fan, 2008, Plant carbon partitioning below ground in the presence of different neighboring species., Soil Biol. Biochem., 40, 2266, 10.1016/j.soilbio.2008.05.003 · DOI
  17. Fierer, 2007, Toward an ecological classification of soil bacteria., Ecology, 88, 1354, 10.1890/05-1839 · DOI
  18. Fuchslueger, 2016, Drought history affects grassland plant and microbial carbon turnover during and after a subsequent drought event., J. Ecol., 104, 1453, 10.1111/1365-2745.12593 · DOI
  19. Garland, 1996, Patterns of potential C source utilization by rhizosphere communities., Soil Biol. Biochem., 28, 223, 10.1016/0038-0717(95)00113-1 · DOI
  20. Gkarmiri, 2017, Identifying the active microbiome associated with roots and rhizosphere soil of oilseed rape., Appl. Environ. Microbiol., 83, 10.1128/AEM.01938-17 · DOI
  21. Gollany, 2005, Tillage and nitrogen fertilizer influence on carbon and soluble silica relations in a Pacific Northwest Mollisol., Soil Sci. Soc. Am. J., 69, 1102, 10.2136/sssaj2004.0284 · DOI
  22. Gollany, 2004, Nitrogen leaching and denitrification in continuous corn as related to residue management and nitrogen fertilization., Environ. Manage., 33, S289, 10.1007/s00267-003-9138-x · DOI
  23. Graber, 2015, A humic substances product extracted from biochar reduces Arabidopsis root hair density and length under P-sufficient and P-starvation conditions., Plant Soil, 395, 21, 10.1007/s11104-015-2524-3 · DOI
  24. Gschwendtner, 2016, Nitrogen fertilization affects bacteria utilizing plant-derived carbon in the rhizosphere of beech seedlings., Plant Soil, 407, 203, 10.1007/s11104-016-2888-z · DOI
  25. Gu, 2017, Application of biochar reduces Ralstonia solanacearum infection via effecs on pathogen chemotaxis, swarming motility, and root exudate adsorption., Plant Soil, 415, 269, 10.1007/s11104-016-3159-8 · DOI
  26. Hamady, 2008, Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex., Nat. Methods, 5, 235, 10.1038/nmeth.1184 · DOI · Paper page
  27. Hannula, 2017, Shifts in rhizosphere fungal community during secondary succession following abandonment from agriculture., ISME J., 11, 2294, 10.1038/ismej.2017.90 · DOI
  28. Himmelstein, 2017, A meta-analysis of intercropping in Africa: impacts on crop yield, farmer income, and integrated pest management effects., Int. J. Agr. Sustain., 15, 1, 10.1080/14735903.2016.1242332 · DOI
  29. Hu, 2014, 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., 30, 1085, 10.1007/s11274-013-1528-5 · DOI
  30. Imparato, 2016, Gasification biochar has limited effects on functional and structural diversity of soil microbial communities in a temperate agroecosystem., Soil Biol. Biochem., 99, 128, 10.1016/j.soilbio.2016.05.004 · DOI
  31. Jaiswal, 2014, Rhizoctonia solani suppression and plant growth promotion in cucumber as affected by biochar pyrolysis temperature, feedstock and concerntration., Soil Biol. Biochem., 69, 110, 10.1016/j.soilbio.2013.10.051 · DOI · Paper page
  32. Kolton, 2017, Biochar-stimulated plant performance is strongly linked to microbial diversity and metabolic potential in the rhizosphere., New Phytol., 213, 1393, 10.1111/nph.14253 · DOI
  33. 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 · DOI
  34. Kong, 2011, Btrim: a fast, lightweight adapter and quality trimming program for next-generation sequencing technologies., Genomics, 98, 152, 10.1016/j.ygeno.2011.05.009 · DOI
  35. Lehmann, 2011, Biochar effects on soil biota–a review., Soil Biol. Biochem., 43, 1812, 10.1016/j.soilbio.2011.04.022 · DOI · Paper page
  36. Liu, 2017, Biochar amendments increase the yield advantage of legume-based intercropping systems over monoculture., Agric. Ecosyst. Environ., 237, 16, 10.1016/j.agee.2016.12.026 · DOI · Paper page
  37. Long, 2018, Phosphate levels influence the utilisation of rice rhizodeposition carbon and the phosphate-solubilising microbial community in a paddy soil., Soil Biol. Biochem., 118, 103, 10.1016/j.soilbio.2017.12.014 · DOI
  38. Love, 2014, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2., Genome Biol., 15, 10.1186/s13059-014-0550-8 · DOI · Paper page
  39. Magoč, 2011, FLASH: fast length adjustment of short reads to improve genome assemblies., Bioinformatics, 27, 2957, 10.1093/bioinformatics/btr507 · DOI · Paper page
  40. McDonald, 2012, An improved greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea., ISME J., 6, 610, 10.1038/ismej.2011.139 · DOI
  41. McMurdie, 2013, phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data., PLoS One, 8, 10.1371/journal.pone.0061217 · DOI
  42. Mendes, 2017, Influence of resistance breeding in common bean on rhizosphere microbiome composition and function., ISME J., 12, 212, 10.1038/ismej.2017.158 · DOI
  43. Nguyen, 2003, Rhizodeposition of organic C by plants: mechanisms and controls., Agronomie, 23, 375, 10.1051/agro:2003011 · DOI
  44. Oksanen, 2016, Vegan: Community Ecology Package.
  45. Olsen, 1954, Estimation of Available Phosphorus in Soils by Extraction With Sodium Bicarbonate.
  46. Pandit, 2018, Biochar improves maize growth by alleviation of nutrient stress in a moderately acidic low-input Nepalese soil., Sci. Total Environ., 625, 1380, 10.1016/j.scitotenv.2018.01.022 · DOI · Paper page
  47. 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 · DOI
  48. Pausch, 2018, Carbon input by roots into the soil: quantification of rhizodeposition from root to ecosystem scale., Glob. Change Biol., 24, 1, 10.1111/gcb.13850 · DOI · Paper page
  49. Pepe-Ranney, 2016, Non-cyanobacterial diazotrophs mediate dinitrogen fixation in biological soil crusts during early crust formation., ISME J., 10, 287, 10.1038/ismej.2015.106 · DOI
  50. Pietikäinen, 2000, Charcoal as a habitat for microbes and its effects on the microbial community of the underlying humus., Oikos, 89, 231, 10.1034/j.1600-0706.2000.890203.x · DOI
  51. 2013, R: A Language and Environment for Statistical Computing.
  52. Rose, 2015, Faba bean is less susceptible to fertiliser N impacts on biological N2 fixation than chickpea in monoculture and intercropping systems., Biol. Fert. Soils, 52, 271, 10.1007/s00374-015-1062-8 · DOI
  53. Tang, 2014, Increase in microbial biomass and phosphorus availability in the rhizosphere of intercropped cereal and legumes under field conditions., Soil Biol. Biochem., 75, 86, 10.1016/j.soilbio.2014.04.001 · DOI
  54. Tang, 2016, Phosphorus availability and microbial community in the rhizosphere of intercropped cereal and legume along a P-fertilizer gradient., Plant Soil, 407, 119, 10.1007/s11104-016-2949-3 · DOI
  55. Trivedi, 2017, Soil aggregation and associated microbial communities modify the impact of agricultural management on carbon content., Environ. Microbiol., 19, 3070, 10.1111/1462-2920.13779 · DOI
  56. Wang, 2016, Incorporation of 13C-labelled rice rhizodeposition into soil microbial communities under different fertilizer applications., Appl. Soil Ecol., 101, 11, 10.1016/j.apsoil.2016.01.010 · DOI
  57. Whitman, 2016, Dynamics of microbial community composition and soil organic carbon mineralization in soil following addition of pyrogenic and fresh organic matter., ISME J., 10, 2918, 10.1038/ismej.2016.68 · DOI · Paper page
  58. Wickham, 2010, ggplot2: elegant graphics for data analysis., J.Stat. Softw., 35, 65
  59. Willis, 2017, Improved detection of changes in species richness in high diversity microbial communities., J. R. Stat. Soc. Ser. C. Appl. Stat., 66, 963, 10.1111/rssc.12206 · DOI
  60. Wolińska, 2017, Bacteroidetes as a sensitive biological indicator of agricultural soil usage revealed by a culture-independent approach., Appl. Soil Ecol., 119, 128, 10.1016/j.apsoil.2017.06.009 · DOI
  61. Xu, 2014, Biochar impacts soil microbial community compostion and nitrogen cycling in an acidic soil planted with rape., Environ. Sci. Technol., 48, 9391, 10.1021/es5021058 · DOI
  62. Yao, 2012, Incorporation of 13C-labelled rice rhizodeposition carbon into soil microbial communities under different water status., Soil Biol. Biochem., 53, 72, 10.1016/j.soilbio.2012.05.006 · DOI
  63. Youngblut, 2014, Intra-genomic variation in G+ C content and its implications for DNA stable isotope probing., Environ. Microbiol. Rep., 6, 767, 10.1111/1758-2229.12201 · DOI
  64. Zhalnina, 2017, Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly., Nat. Microbiol., 3, 470, 10.1038/s41564-018-0129-3 · DOI
  65. Zhang, 2017, Tobacco bacterial wilt suppression with biochar soil addition associates to improved soil physiochemical properties and increased rhizosphere bacteria abundance., Appl. Soil Ecol., 112, 90, 10.1016/j.apsoil.2016.12.005 · DOI
  66. Zheng, 2018, Enhanced growth of halophyte plants in biochar-amended coastal soil: roles of nutrient availability and rhizosphere microbial modulation., Plant Cell Environ., 41, 517, 10.1111/pce.12944 · DOI
  67. Zhou, 2011, Reproducibility and quantitation of amplicon sequencing-based detection., ISME J., 5, 1303, 10.1038/ismej.2011.11 · DOI

Metadata

Authors
Liao, H., Li, Y., & Yao, H.
Affiliations
  • Guizhou Normal University (CN)
  • Chinese Academy of Sciences (CN)
Corresponding author
  • Li, Yaying
  • Yao, Huaiying
Venue
Frontiers in Microbiology
Published
2019-06-18
Volume
10
Pages
1361-1361
ISSN
1664-302X (ISSN-L)
OpenAlex
W2949776298
Cited by
76
References
66
Citations by year
2026: 11 · 2025: 12 · 2024: 12 · 2023: 14 · 2022: 12 · 2021: 11 · 2020: 4
FWCI
5.37
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Microbiology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
National Natural Science Foundation of China (41525002, 41471206, and 41601249, 41877051)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Soil Science › Soil Carbon and Nitrogen Dynamics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Keywords
biochar amendment, plant-derived carbon, rhizosphere microbiome, intercropping, Vicia faba, maize, soil microbial community structure, Firmicutes, Bacteroidetes, nitrogen fixation, phosphate solubilization

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review