Biochar soil amendment increased bacterial but decreased fungal gene abundance with shifts in community structure in a slightly acid rice paddy from Southwest China

Applied Soil Ecology

Volumn 71, Issue , 2013, Pages 33-44

  Chen, Junhui ^a   Liu, Xiaoyu ^a   Zheng, Jinwei ^a   Zhang, Bin ^a   Lu, Haifei ^a   Chi, Zhongzhi ^b   Pan, Genxing ^a   Li, Lianqing ^a   Zheng, Jufeng ^a   Zhang, Xuhui ^a   Wang, Jiafang ^a   Yu, Xinyan ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b CROP RESEARCH INSTITUTE   (China)

Author keywords

Biochar; Microbial community structure and abundance; Rice paddy soil; Soil enzymes

Indexed keywords

ANAEROLINEAE; ASCOMYCOTA; BACTERIA (MICROORGANISMS); GLOMEROMYCOTA; HYDROGENOPHILACEAE; METHYLOPHILACEAE;

EID: 84879317036     PISSN: 09291393     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.apsoil.2013.05.003     Document Type: Article

References (101)

1. Acosta-Martínez V., Tabatabai M.A. Enzyme activities in a limed agricultural soil. Biol. Fert. Soils 2000, 31:85-91.
2. Anderson C.R., Condron L.M., Clough T.J., Fiers M., Stewart A., Hill R.A., Sherlock R.R. Biochar induced soil microbial community change: implications for biogeochemical cycling of carbon, nitrogen and phosphorus. Pedobiologia 2011, 54:309-320.
3. Bååth E., Frostegård Å., Pennanen T., Fritze H. Microbial community structure and pH response in relation to soil organic matter quality in wood-ash fertilized, clear-cut or burned coniferous forest soils. Soil Biol. Biochem. 1995, 27:229-240.
4. Baertsch C., Paez-Rubio T., Viau E., Peccia J. Source tracking aerosols released from land-applied class B biosolids during high-wind events. Appl. Environ. Microbiol. 2007, 73:4522-4531.
5. Brookes P.C., Landman A., Pruden G., Jenkinson D.S. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol. Biochem. 1985, 17:837-842.
6. Cabezas A. Diversity and function of the microbial community on anodes of sediment microbial fuel cells fueled by root exudates 2010, Philipps-Universität, Marburg, (Ph.D. dissertation).
7. Chan K.Y., Van Zwieten L., Meszaros I., Downie A., Joseph S. Agronomic values of greenwaste biochar as a soil amendment. Aust. J. Soil Res. 2007, 45:629-634.
8. Chen B., Yuan M., Qian L. Enhanced bioremediation of PAH-contaminated soil by immobilized bacteria with plant residue and biochar as carriers. J. Soil. Sediment. 2012, 12:1350-1359.
9. Chu H., Lin X., Fujii T., Morimoto S., Yagi K., Hu J., Zhang J. Soil microbial biomass dehydrogenase activity, bacterial community structure in response to long-term fertilizer management. Soil Biol. Biochem. 2007, 39:2971-2976.
10. Coyne M.S. Soil Microbiology: An Exploratory Approach 1999, 113-122. Delmar Publishers, Albany, NY.
11. Culman S., Bukowski R., Gauch H., Cadillo-Quiroz H., Buckley D. T-REX: software for the processing and analysis of T-RFLP data. BMC Bioinform. 2009, 10:171.
12. Dempster D., Gleeson D., Solaiman Z., Jones D., Murphy D. Decreased soil microbial biomass and nitrogen mineralisation with Eucalyptus biochar addition to a coarse textured soil. Plant Soil 2012, 354:311-324.
13. Dhillon A., Teske A., Dillon J., Stahl D.A., Sogin M.L. Molecular characterization of sulfate-reducing bacteria in the Guaymas Basin. Appl. Environ. Microbiol. 2003, 69:2765-2772.
14. Durenkamp M., Luo Y., Brookes P.C. Impact of black carbon addition to soil on the determination of soil microbial biomass by fumigation extraction. Soil Biol. Biochem. 2010, 42:2026-2029.
15. Eivazi F., Tabatabai M.A. Factors affecting glucosidase and galactosidase activities in soils. Soil Biol. Biochem. 1990, 7:891-897.
16. Elad Y., David D.R., Harel Y.M., Borenshtein M., Ben Kalifa H., Silber A., Graber E.R. Induction of systemic resistance in plants by biochar, a soil-applied carbon sequestering agent. Phytopathology 2010, 100:913-921.
17. Elmer W.H. Use of biochar to increase mycorrhizal colonization and suppress Fusarium crown rot of asparagus in replant soils. Phytopathology 2011, 101:S258.
18. Fang H.H., Liang D.W., Zhang T., Liu Y. Anaerobic treatment of phenol in wastewater under thermophilic condition. Water Res. 2006, 40:427.
19. Feng Y., Xu Y., Yu Y., Xie Z., Lin X. Mechanisms of biochar decreasing methane emission from Chinese paddy soils. Soil Biol. Biochem. 2012, 46:80-88.
20. Fierer N., Jackson J.A., Vilgalys R., Jackson R.B. Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl. Environ. Microbiol. 2005, 71:4117-4120.
21. Fierer N., Jackson R.B. The diversity and biogeography of soil bacterial communities. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:626-631.
22. Frolking S., Qiu J., Boles S., Xiao X.M., Liu J., Zhuang Y., Li C., Qin X. Combing remote sensing and ground census data to develop new maps of the distribution of rice agriculture in China. Global Biogeochem. Cycles 2002, 16:1091-1101.
23. Glaser B., Haumaier L., Guggenberger G., Zech W. The 'Terra Preta' phenomenon: a model for sustainable agriculture in the humid tropics. Naturwissenschaften 2001, 88:37-41.
24. Gong Z.T. Chinese Soil Taxonomic Classification 1999, 5-215. China Science Press, Beijing, (in Chinese).
25. Graber E.R., Harel Y.M., Kolton M., Cytryn E., Silber A., David D.R., Tsechansky L., Borenshtein M., Elad Y. Biochar impact on development and productivity of pepper and tomato grown in fertigated soilless media. Plant Soil 2010, 337:481-496.
26. Grossman J., O'Neill B., Tsai S., Liang B., Neves E., Lehmann J., Thies J. Amazonian Anthrosols support similar microbial communities that differ distinctly from those extant in adjacent unmodified soils of the same mineralogy. Microb. Ecol. 2010, 60:192-205.
27. Guan S., Zhang D., Zhang Z. Soil Enzyme and its Research Methods 1986, Agriculture Press, Beijing, (in Chinese).
28. Hart S.C., Stark J.M., Davidson E.A., Firestone M.K. Nitrogen mineralization, immobilization, and nitrification. Methods of Soil Analysis. Part 2. SSSA Book Series 5 1994, 985-1018. Weaver, R.V.
29. Hedrick D.B., Peacock A., Stephen J.R., Macnaughton S.J., Brüggemann J., White D.C. Measuring soil microbial community diversity using polar lipid fatty acid and denaturing gradient gel electrophoresis data. J. Microbiol. Methods 2000, 41:235-248.
30. He J.-z., Shen J.-p., Zhang L.-m., Zhu Y.-g., Zheng Y.-m., Xu M.-g., Di H. Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ. Microbiol. 2007, 9:2364-2374.
31. Heuer H., Krsek M., Baker P., Smalla K., Wellington E. Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl. Environ. Microbiol. 1997, 63:3233-3241.
32. Holland E.A., Coleman D.C. Litter placement effects on microbial and organic matter dynamics in an agroecosystems. Ecology 1987, 68:425-433.
33. Huber T., Faulkner G., Hugenholtz P. Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 2004, 20:2317-2319.
34. 2 flux. FEMS Microbiol. Ecol. 2011, 78:116-128.
35. Jin H. Characterization of microbial life colonizing biochar and biochar-amended soils 2010, Cornell University, Ithaca, NY, (Ph.D. dissertation).
36. 2 release is both biotically and abiotically mediated. Soil Biol. Biochem. 2011, 43:1723-1731.
37. Jones D.L., Rousk J., Edwards-Jones G., DeLuca T.H., Murphy D.V. Biochar-mediated changes in soil quality and plant growth in a three year field trial. Soil Biol. Biochem. 2012, 45:113-124.
38. Kasozi G.N., Zimmerman A.R., Nkedi-Kizza P., Gao B. Catechol and humic acid sorption onto a range of laboratory-produced black carbons (biochars). Environ. Sci. Technol. 2010, 44:6189-6195.
39. Khodadad C.L.M., Zimmerman A.R., Green S.J., Uthandi S., Foster J.S. Taxa-specific changes in soil microbial community composition induced by pyrogenic carbon amendments. Soil Biol. Biochem. 2011, 43:385-392.
40. Killham K. Soil Ecology 1994, 40-52. Cambridge Univ. Press, Cambridge, UK.
41. Kim J.-S., Sparovek G., Longo R.M., De Melo W.J., Crowley D. Bacterial diversity of terra preta and pristine forest soil from the Western Amazon. Soil Biol. Biochem. 2007, 39:684-690.
42. Kolb S., Fermanich K., Dornbush M. Effect of charcoal quantity on microbial biomass and activity in temperate soils. Soil Sci. Soc. Am. J. 2009, 73:1173-1181.
43. Kolton M., Meller Harel Y., Pasternak Z., Graber E.R., Elad Y., Cytryn E. Impact of biochar application to soil on the root-associated bacterial community structure of fully developed greenhouse pepper plants. Appl. Environ. Microbiol. 2011, 77:4924-4930.
44. Kumar S., Jain M.C., Chhonkar P.K. A note on the stimulation of biogas production from cattle dung by addition of charcoal. Biol. Waste. 1987, 20:1209-1215.
45. 14C labeling. Soil Biol. Biochem. 2009, 41:210-219.
46. Lammirato C., Miltner A., Kaestner M. Effects of wood char and activated carbon on the hydrolysis of cellobiose by β-glucosidase from Aspergillus niger. Soil Biol. Biochem. 2011, 43:1936-1942.
47. Lehmann J., Gaunt J., Rondon M. Bio-char sequestration in terrestrial ecosystems-a review. Mitig. Adapt. Strateg. Global Change 2006, 11:403-427.
48. Lehmann J., Czimczik C., Laird D., Sohi S. Stability of biochar in the soil. Biochar for Environmental Management: Science and Technology 2009, 183-205. Earthscan, London. J. Lehmann, S. Joseph (Eds.).
49. Lehmann J., Joseph S. Biochar for environmental management: an introduction. Biochar for Environmental Management: Science and Technology 2009, 1-12. Earthscan, London. J. Lehmann, S. Joseph (Eds.).
50. Lehmann J., Rillig M.C., Thies J., Masiello C.A., Hockaday W.C., Crowley D. Biochar effects on soil biota - a review. Soil Biol. Biochem. 2011, 43:1812-1836.
51. Liang B., Lehmann J., Sohi S.P., Thies J.E., O'Neill B., Trujillo L., Gaunt J., Solomon D., Grossman J., Neves E.G., Luizão F.J. Black carbon affects the cycling of non-black carbon in soil. Org. Geochem. 2010, 41:206-213.
52. Liang B., Lehmann J., Solomon D., Kinyangi J., Grossman J., O'Neill B., Skjemstad J.O., Thies J., Luizão F.J., Petersen J., Neves E.G. Black carbon increases cation exchange capacity in soils. Soil Sci. Soc. Am. J. 2006, 70:1719-1730.
53. Liu D., Liu X., Liu Y., Li L., Pan G., Crowley D., Tippkötter R. Soil organic carbon (SOC) accumulation in rice paddies under long-term agro-ecosystem experiments in southern China - VI. Changes in microbial community structure and respiratory activity. Biogeosci. Discuss. 2011, 8:1529-1554.
54. 2O emission in rice paddies? A cross site field experiment from South China. Ecol. Eng. 2012, 42:168-173.
55. 2 emissions from waterlogged paddy soil with biochar. J. Soil. Sediment. 2011, 11:930-939.
56. Liu Y., Zhou T., Crowley D., Li L., Liu D., Zheng J., Yu X., Pan G., Hussain Q., Zhang X., Zheng J. Decline in topsoil microbial quotient, fungal abundance and C utilization efficiency of rice paddies under heavy metal pollution across South China. PLoS ONE 2012, 7:e38858.
57. Lu R.K. Methods of Soil and Agro-chemical Analysis 2000, China Agricultural Science and Technology Press, Beijing, (in Chinese).
58. Margesin R. Acid and alkaline phosphomonoesterase activity with the substrate p-nitrophenyl phosphate. Methods in Soil Biology 1997, 213-217. Springler-Verlag, Berlin. F. Schinner, R. Öhlinger, E. Kandeler, R. Margesin (Eds.).
59. Marschner P., Kandeler E., Marschner B. Structure and function of the soil microbial community in a long-term fertilizer experiment. Soil Biol. Biochem. 2003, 35:453-461.
60. Marstorp H., Guan X., Gong P. Relationship between dsDNA, chloroform labile C and ergosterol in soils of different organic matter contents and pH. Soil Biol. Biochem. 2000, 32:879-882.
61. 14C-labeled model and cornstalk lignins phenols, model phenolase humic polymers, and fungal melanins as influenced by a readily available carbon source and soil. Appl. Environ. Microbiol. 1979, 38:283-289.
62. May L.A., Smiley B., Schmidt M.G. Comparative denaturing gradient gel electrophoresis analysis of fungal communities associated with whole plant corn silage. Can. J. Microbiol. 2001, 47:829-841.
63. Meller Harel Y., Elad Y., Rav-David D., Borenstein M., Shulchani R., Lew B., Graber E. Biochar mediates systemic response of strawberry to foliar fungal pathogens. Plant Soil 2012, 357:245-257.
64. Muyzer G., De Waal E., Uitterlinden A. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 1993, 59:695-700.
65. O'Neill B., Grossman J., Tsai M., Gomes J., Lehmann J., Peterson J., Neves E., Thies J. Bacterial community composition in Brazilian anthrosols and adjacent soils characterized using culturing and molecular identification. Microb. Ecol. 2009, 58:23-35.
66. Osborn A.M., Moore E.R.B., Timmis K.N. An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. Environ. Microbiol. 2000, 2:39-50.
67. Pan G., Lin Z., Li L., Zhang A., Zheng J., Zhang X. Perspective on biomass carbon industrialization of organic waste from agriculture and rural areas in China. J. Agric. Sci. Technol. 2011, 13:75-82. (in Chinese).
68. Parton W.J., Schimel D.S., Cole C.V., Ojima D.S. Analysis of factors controlling soil organic matter levels in Great Plains grasslands. Soil Sci. Soc. Am. J. 1987, 51:1173-1179.
69. Paz-Ferreiro J., Gascó G., Gutiérrez B., Méndez A. Soil biochemical activities and the geometric mean of enzyme activities after application of sewage sludge and sewage sludge biochar to soil. Biol. Fert. Soils 2012, 48:511-517.
70. Pietikäinen J., Kiikkilä O., Fritze H. Charcoal as a habitat for microbes and its effect on the microbial community of the underlying humus. Oikos 2000, 89:231-242.
71. Rondon M.A., Ramirez J.A., Lehmann J. Greenhouse gas emissions decrease with charcoal additions to tropical soils. 3rd USDA Symposium on Green-House Gases and Carbon Sequestration in Agriculture and Forestry 2005, 1 pp.
72. Ross D. Invertase and amylase activities as influenced by clay minerals soil-clay fractions and topsoils under grassland. Soil Biol. Biochem. 1983, 15:287-293.
73. Rousk J., Brookes P.C., Bååth E. Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl. Environ. Microbiol. 2009, 75:1589-1596.
74. Saito M., Marumoto T. Inoculation with arbuscular mycorrhizal fungi: the status quo in Japan and the future prospects. Plant Soil 2002, 244:273-279.
75. Schütte U.E., Abdo Z., Bent S., Shyu C., Williams C., Pierson J., Forney L. Advances in the use of terminal restriction fragment length polymorphism (T-RFLP) analysis of 16S rRNA genes to characterize microbial communities. Appl. Microbiol. Biotechnol. 2008, 80:365-380.
76. Serra-Wittling C., Houot S., Barriuso E. Soil enzymatic response to addition of municipal solid-waste compost. Biol. Fert. Soils 1995, 20:226-236.
77. Serra-Wittling C., Houot S., Barriuso E. Modification of soil water retention and biological properties by municipal solid waste compost. Compost Sci. Util. 1996, 4:44-52.
78. Six J., Frey S.D., Thiet R.K., Batten K.M. Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci. Soc. Am. J. 2006, 70:555-569.
79. Smalla K., Oros-Sichler M., Milling A., Heuer H., Baumgarte S., Becker R., Neuber G., Kropf S., Ulrich A., Tebbe C.C. Bacterial diversity of soils assessed by DGGE, T-RFLP and SSCP fingerprints of PCR-amplified 16S rRNA gene fragments: do the different methods provide similar results?. J. Microbiol. Methods 2007, 69:470-479.
80. Sohi S.P., Krull E., Lopez-Capel E., Bol R. A review of biochar and its use and function in soil. Adv. Agron. 2010, 105:47-82.
81. Sohi S.P. Carbon storage with benefits. Science 2012, 338:1034-1035.
82. Soil Survey Staff Soil taxonomy, a basic classification for making and interpreting soil surveys. Agriculture Handbook 436 1999, USDA, Natural Resources Conservation Service, Washington, 869 pp. 2nd ed.
83. Steinbeiss S., Gleixner G., Antonietti M. Effect of biochar amendment on soil carbon balance and soil microbial activity. Soil Biol. Biochem. 2009, 41:1301-1310.
84. Steiner C., Das K.C., Garcia M., Förster B., Zech W. Charcoal and smoke extract stimulate the soil microbial community in a highly weathered xanthic Ferralsol. Pedobiologia 2008, 51:359-366.
85. Stemmer M., Gerzabek M.H., Kandeler E. Invertase and xylanase activity of bulk soil and particle-size fractions during maize straw decomposition. Soil Biol. Biochem. 1998, 31:9-18.
86. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
87. Thies J., Rillig M. Characteristics of biochar: biological properties. Biochar for Environmental Management: Science and Technology 2009, Earthscan, London, 89 pp. J. Lehmann, S. Joseph (Eds.).
88. Thiet R.K., Frey S.D., Six J. Do growth yield efficiencies differ between soil microbial communities differing in fungal:bacterial ratios? Reality check and methodological issues. Soil Biol. Biochem. 2006, 38:837-844.
89. 2 from Ferrosol. Aust. J. Soil Res. 2010, 48:555-568.
90. Waldrop M.P., Balser T.C., Firestone M.K. Linking microbial community composition to function in a tropical soil. Soil Biol. Biochem. 2000, 32:1837-1846.
91. Warnock D., Lehmann J., Kuyper T., Rillig M. Mycorrhizal responses to biochar in soil - concepts and mechanisms. Plant Soil 2007, 300:9-20.
92. Wu J., Jorgensen R.G., Pommerening B., Chaussod R., Brookes P.C. Measurement of soil microbial biomass-C by fumigation-extraction-an automated procedure. Soil Biol. Biochem. 1990, 22:1167-1169.
93. Wu J.-H., Liu W.-T., Tseng I-C., Cheng S.-S. Characterization of microbial consortia in a terephthalate-degrading anaerobic granular sludge system. Microbiology 2001, 147:373-382.
94. Yamada T., Sekiguchi Y. Cultivation of uncultured Chloroflexi subphyla: significance and ecophysiology of formerly uncultured Chloroflexi 'subphylum I' with natural and biotechnological relevance. Microb. Environ. 2009, 24:205-216.
95. 2O emissions from soil resulting from rewetting air-dried soil in short-term laboratory experiments. Soil Sci. Plant Nutr. 2007, 53:181-188.
96. 2. Ecol. Appl. 1996, 6:257-262.
97. Zhang A., Bian R., Pan G., Cui L., Hussain Q., Li L., Zheng J., Zheng J., Zhang X., Han X., Yu X. Effects of biochar amendment on soil quality, crop yield and greenhouse gas emission in a Chinese rice paddy: a field study of 2 consecutive rice growing cycles. Field Crop Res. 2012, 127:153-160.
98. Zhang A., Cui L., Pan G., Li L., Hussain Q., Zhang X., Zheng J., Crowley D. Effect of biochar amendment on yield and methane and nitrous oxide emissions from a rice paddy from Tai Lake plain, China. Agr. Ecosyst. Environ. 2010, 139:469-475.
99. Zhang B., Liu X., Pan G., Zheng J., Chi Z., Li L., Zheng J., Zhang X. Effect of biochar amendment on soil properties, rice yield and GHGs emission: a field study of 2 consecutive rice growing cycles. Sci. Agric. Sin. 2012, 45:4844-4853. (in Chinese).
100. 2 evolution of three paddy soils from South China and the temperature dependence. J. Environ. Sci. China 2007, 19:319-326.
101. Zimmerman A.R. Abiotic and microbial oxidation of laboratory-produced black carbon (Biochar). Environ. Sci. Technol. 2010, 44:1295-1301.