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Journal of Integrative Agriculture  2019, Vol. 18 Issue (7): 1474-1485    DOI: 10.1016/S2095-3119(18)62102-1
Special Focus: Ecological functions of biochar Advanced Online Publication | Current Issue | Archive | Adv Search |
Straw and biochar strongly affect functional diversity of microbial metabolism in paddy soils
YUAN Hong-zhao1, ZHU Zhen-ke1, WEI Xiao-meng1, LIU Shou-long1, PENG Pei-qin2, Anna Gunina1, 3, SHEN Jian-lin1, Yakov Kuzyakov1, 4, 5, 6, GE Ti-da1, WU Jin-shui1, WANG Jiu-rong1 
1 Key Laboratory of Agro-ecological Processes in Subtropical Region/Changsha Research Station for Agricultural and Environmental Monitoring, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha 410125, P.R.China
2 College of Environmental Science and Engineering, Central South University of Forestry and Technology, Changsha 410004, P.R.China
3 Department of Soil Biology and Biochemistry, Dokuchaev Soil Science Institute, Moscow 119017, Russian Federation
4 Department of Agricultural Soil Science, University of Göttingen, Göttingen 37077, Germany
5 Institute of Environmental Sciences, Kazan Federal University, Kazan 420049, Russian Federation
6 Agro-Technology Institute, RUDN University, Moscow 117198, Russian Federation
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The application of straw and biochar is widely practiced for the improvement of soil fertility.  However, its impact on microbial functional profiles, particularly with regard to paddy soils, is not well understood.  The aim of this study was to investigate the diversity of microbial carbon use patterns in paddy soils amended with straw or straw-derived biochar in a 3-year field experiment in fallow soil and at various development stages of a rice crop (i.e., tillering and blooming).  We applied the community level physiological profiling approach, with 15 substrates (sugars, carboxylic and amino acids, and phenolic acid).  In general, straw application resulted in the greatest microbial functional diversity owing to the greater number of  available C sources than in control or biochar plots.  Biochar amendment promoted the use of α-ketoglutaric acid, the mineralization of which was higher than that of any other substrate.  Principal component analyses indicated that microbial functional diversity in the biochar-amended soil was separated from those of the straw-amended and control soils.  Redundancy analyses revealed that soil organic carbon content was the most important factor regulating the pattern of microbial carbon utilization.  Rhizodeposition and nutrient uptake by rice plants modulated microbial functions in paddy soils and stimulated the microbial use of N-rich substances, such as amino acids.  Thus, our results demonstrated that the functional diversity of microorganisms in organic amended paddy soils is affected by both physicochemical properties of amendment and plant growth stage. 
Keywords:  carbon metabolism        microbial functional diversity        biochar amendment        paddy soil        MicroRespTM   
Received: 22 June 2018   Online: 28 September 2018   Accepted:
Fund: This study was financially supported by the National Key Research and Development Program of China (2016YFE0101100), the National Natural Science Foundation of China (41771334, 41771337 and 31470629), the Youth Innovation Team Project of the Institute of Subtropical Agriculture, Chinese Academy of Sciences (2017QNCXTD_GTD), the Chinese Academy of Sciences Instrument Function Development Project, and the Government Program of Competitive Growth of Kazan Federal University and by the “RUDN University program 5–100”.
Corresponding Authors:  Correspondence ZHU Zhen-ke, Tel: +86-731-84615234, Fax: +86-731-84612685, E-mail:   
About author:  YUAN Hong-zhao, Tel: +86-731-84619733, E-mail: yuanhongzhao;

Cite this article: 

YUAN Hong-zhao, ZHU Zhen-ke, WEI Xiao-meng, LIU Shou-long, PENG Pei-qin, Anna Gunina, SHEN Jian-lin, Yakov Kuzyakov, GE Ti-da, WU Jin-shui, WANG Jiu-rong. 2019. Straw and biochar strongly affect functional diversity of microbial metabolism in paddy soils. Journal of Integrative Agriculture, 18(7): 1474-1485.

Alburquerque J A, Salazar P, Barron V, Torrent J, de Campillo M C, Gallardo A, Villar R. 2013. Enhanced wheat yield by biochar addition under different mineral fertilization levels. Agronomy for Sustainable Development, 33, 475–484.
Anderson C R, Condron L M, Clough T J, Fiers M, Stewart A, Hill R A, Sherlock R R. 2011. Biochar induced soil microbial community change: Implications for biogeochemical cycling of carbon, nitrogen and phosphorus. Pedobiologia, 54, 309–320.
Archanjo B S, Mendoza M E, Albu M, Mitchell D R G, Hagemann N, Mayrhofer C, Mai T L A, Weng Z, Kappler A, Behrens S, Munroe P, Achete C A, Donne S, Araujo J R, van Zwieten L, Horvat J, Enders A, Joseph S. 2017. Nanoscale analyses of the surface structure and composition of biochars extracted from field trials or after co-composting using advanced analytical electron microscopy. Geoderma, 294, 70–79.
Aulakh M S, Wassmann R, Bueno C, Kreuzwieser J, Rennenberg H. 2001. Characterization of root exudates at different growth stages of ten rice (Oryza sativa L.) cultivars. Plant Biology, 3, 139–148.
Balasooriya W K, Huygens D, Denef K, Roobroeck D, Verhoest N E C, Boeckx P. 2013. Temporal variation of rhizodeposit-C assimilating microbial communities in a natural wetland. Biology and Fertility of Soils, 49, 333–341.
Banning N C, Lalor B M, Cookson W R, Grigg A H, Murphy D V. 2012. Analysis of soil microbial community level physiological profiles in native and post-mining rehabilitation forest: Which substrates discriminate? Applied Soil Ecology, 56, 27–34.
Badri D V, Vivanco J M. 2010. Regulation and function of root exudates. Plant Cell & Environment, 32, 666–681.
Brolsma K M, Vonk J A, Mommer L, Van Ruijven J, Hoffland E, De Goede R G M. 2017. Microbial catabolic diversity in and beyond the rhizosphere of plant species and plant genotypes. Pedobiologia, 61, 43–49.
Campbell C D, Chapman S J, Cameron C M, Davidson M S, Potts J M. 2003. A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Applied and Environmental Microbiology, 69, 3593–3599.
Chapman S J, Campbell C D, Artz R R E. 2007. Assessing CLPPs using MicroRespTM. A comparison with Biolog and multi-SIR. Journal of Soils and Sediments, 7, 406–410.
Cheng H G, Hill P W, Bastami M S, Jones D L. 2017. Biochar stimulates the decomposition of simple organic matter and suppresses the decomposition of complex organic matter in a sandy loam soil. Global Change Biology Bioenergy, 9, 1110–1121.
Chodak M, Go??biewski M, Morawska-P?oskonka J, Kuduk K, Niklińska M. 2013. Diversity of microorganisms from forest soils differently polluted with heavy metals. Applied Soil Ecology, 64, 7–14
Choi J H, Kang H, Park S S. 2009. Comparison of enzyme activities in vegetated and nonvegetated sediments. Journal of Environmental Engineering, 135, 299–305.
Derrien D, Marol C, Balesdent J. 2004. The dynamics of neutral sugars in the rhizosphere of wheat. An approach by 13C pulse-labelling and GC/C/IRMS. Plant and Soil, 267, 243−253.
Dippold M A, Kuzyakov Y. 2013. Biogeochemical transformations of amino acids in soil assessed by position-specific labeling. Plant and Soil, 373, 385–401.
Downie, P M, Crosky A. 2009. Characteristics of biochar physical and structural properties. In: Lehmann J, Joseph S, eds., Biochar for Environmental Management, Science and Technology. Earthscan, London. pp. 13–29.
Franzluebbers A J. 2010. Achieving soil organic carbon sequestration with conservation agricultural systems in the southeastern United States. Soil Science Society of America Journal, 74, 347−357.
Franzluebbers A J, Stuedemann J A. 2010. Surface soil changes during twelve years of pasture management in the southern piedmont USA. Soil Science Society of America Journal, 74, 2131–2141.
Gao X Z, Ma W Q, Ma C B, Zhang F S, Wang Y H. 2002. Analysis on the current status of utilization of crop straw in China. Journal of Huazhong Agricultural University, 21, 242–247. (in Chinese).
Ge T, Chen X, Yuan H, Li B, Zhu H, Peng P, Li K, Jones D L, Wu J. 2013. Microbial biomass, activity, and community structure in horticultural soils under conventional and organic management strategies. European Journal of Soil Biology, 58, 122−128.
Ge T, Li B, Zhu Z, Hu Y, Yuan H, Dorodnikov M, Jones D L, Wu J, Kuzyakov Y. 2017. Rice rhizodeposition and its utilization by microbial groups depends on N fertilization. Biology and Fertility of Soils, 53, 37−48.
Ge T, Yuan H, Zhu H, Wu X, Nie S, Liu C, Tong C, Wu J, Brookes P. 2012. Biological carbon assimilation and dynamics in a flooded rice-soil system. Soil Biology and Biochemistry, 48, 39−49.
Hagemann N, Joseph S, Schmidt H P, Kammann C I, Harter J, Borch T, Young R B, Varga K, Taherymoosavi S, Wade Elliott K, McKenna A, Albu M, Mayrhofer C, Obst M, Conte P, Dieguez-Alonso A, Orsetti S, Subdiaga E, Behrense S, Andreas K. 2017. Organic coating on biochar explains its nutrient retention and stimulation of soil fertility. Nature Communications, 8, 1089.
Hansen V, Muller-Stover D, Munkholm L J, Peltre C, Hauggaard-Nielsen H, Jensen L S. 2016. The effect of straw and wood gasification biochar on carbon sequestration, selected soil fertility indicators and functional groups in soil: An incubation study. Geoderma, 269, 99−107.
Harvey O R, Kuo L J, Zimmerman A R, Louchouarn P, Amonette J E, Herbert B E. 2012. An index-based approach to assessing recalcitrance and soil carbon sequestration potential of engineered black carbons (biochars). Environmental Science & Technology, 46, 1415–1421.
Hofrichter M, Scheibner K, Schneegass I, Fritsche W. 1998. Enzymatic combustion of aromatic and aliphatic compounds by manganese peroxidase from Nematoloma frowardii. Applied and Environmental Microbiology, 64, 399–404.
Huang X, Wang C, Liu Q, Zhu Z, Lynn T M, Shen J, Whiteley A S, Kumaresan D, Ge T, Wu J. 2018. Abundance of microbial CO2-fixing genes during the late rice season in long-term management paddy field amended with straw and straw-derived biochar. Canadian Journal of Soil Science, 98, 306–316.
Islam M R, Chauhan P S, Kim Y, Kim M, Sa T. 2011. Community level functional diversity and enzyme activities in paddy soils under different long-term fertilizer management practices. Biology and Fertility of Soils, 47, 599–604.
Jones D L, Nguyen C, Finlay R D. 2009. Carbon flow in the rhizosphere: Carbon trading at the soil-root interface. Plant and Soil, 321, 5–33.
Kandeler E, Kampichler C, Joergensen R G, Mölter K. 1999. Effects of mesofauna in a spruce forest on soil microbial communities and n cycling in field mesocosms. Soil Biology & Biochemistry, 31 , 1783–1792.
Keeney D R, Nelson D W. 1982. Nitrogen inorganic forms. In: Page A L, Miller R H, Keeney D R, eds., Methods of Soil Analysis. 2nd. American Society of Agronomy, Madison, WI. pp. 643–698.
Klimek B, Chodak M, Ja?wa M, Solak A, Tarasek A, Niklińska M. 2016. The relationship between soil bacteria substrate utilisation patterns and the vegetation structure in temperate forests. European Journal of Forest Research, 135, 179–189.
Knox SH, Sturtevant C, Matthes JH, Koteen L, Verfaillie J, Baldocchi D. 2015. Agricultural peatland restoration: effects of land-use change on greenhouse gas (CO2 and CH4) fluxes in the Sacramento-San Joaquin Delta. Global Change Biology, 21, 750–765.
Kögel-Knabner I, Guggenberger G, Kleber M, Kandeler E, Kalbitz K, Scheu S, Eusterhues K, Leinweber P. 2008. Organo-mineral associations in temperate soils: Integrating biology, integralogy, and organic matter chemistry. Journal of Soil Science and Plant Nutrition, 171, 61–82.
Kuzyakov Y, Blagodatskaya E, Blagodatsky S. 2009. The biology of the regulatory gate: Comments on the paper by Kemmitt et al. (2008) ‘Mineralization of native soil organic matter is not regulated by the size, activity or composition of the soil microbial biomass - a new perspective. Soil Biology & Biochemistry, 41, 435–439.
Kuzyakov Y, Bogomolova I. 2015. Microbial hotspots and hot moments in soil: Concept & review. Soil Biology & Biochemistry, 83,184–199.
Kuzyakov Y, Bogomolova I, Glaser B. 2014. Biochar stability in soil: Decomposition during eight years and transformation as assessed by compound-specific 14C analysis. Soil Biology & Biochemistry, 70, 229–236.
Kuzyakov Y, Friedel J K, Stahr K. 2000. Review of mechanisms and quantification of priming effects. Soil Biology & Biochemistry, 32, 1485–1498.
Kuzyakov Y, Xu X L. 2013. Competition between roots and microorganisms for nitrogen: Mechanisms and ecological relevance. New Phytologist, 198, 656–669.
Lal R. 2008. Carbon sequestration. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 363, 815–830.
Lazdovica K, Kampars V, Liepina L, Vilka M. 2017. Comparative study on thermal pyrolysis of buckwheat and wheat straws by using TGA-FTIR and Py-GC/MS methods. Journal of Analytical and Applied Pyrolysis, 124, 1–15.
Lehmann J, Gaunt J, Rondon M. 2006. Biochar sequestration in terrestrial ecosystems - a review. Mitigation and Adaptation Strategies for Global Change, 11, 395–419.
Li M, Liu M, Li Z P, Jiang C Y, Wu M. 2016. Soil N transformation and microbial community structure as affected by adding biochar to a paddy soil of subtropical China. Journal of Integrative Agriculture, 15, 201–219.
Liang B Q, Lehmann J, Sohi S P, Thies J E, O’Neill B, Trujillo L, Gaunt J, Solomon D, Grossman J, Neves EG, Luizao F J. 2010. Black carbon affects the cycling of non-black carbon in soil. Organic Geochemistry, 41, 206–213.
Liu X Y, Zheng J F, Zhang D X, Cheng K, Zhou H M, Zhang A, Li L Q, Joseph S, Smith P, Crowley D, Kuzyakov Y, Pan G X. 2016. Biochar has no effect on soil respiration across Chinese agricultural soils. Science of the Total Environment, 554–555, 259–265.
Loeppmann S, Biagodatskaya E, Pausch J, Kuzyakov Y. 2016. Enzyme properties down the soil profile - A matter of substrate quality in rhizosphere and detritusphere. Soil Biology & Biochemistry, 103, 274–283.
Macdonald C A, Thomas N, Robinson L, Tate K R, Ross D J, Dando J, Singh B K. 2009. Physiological, biochemical and molecular responses of the soil microbial community after afforestation of pastures with Pinus radiata. Soil Biology & Biochemistry, 41, 1642–1651.
Maestrini B, Herrmann A M, Nannipieri P, Schmidt M W, Abiven S. 2014. Ryegrass-derived pyrogenic organic matter changes organic carbon and nitrogen mineralization in a temperate forest soil. Soil Biology & Biochemistry, 69, 291–301.
Marschner P, Kandeler E, Marschner B. 2003. Structure and function of the soil microbial community in a long-term fertilizer experiment. Soil Biology & Biochemistry, 35, 453–461.
Manzoni S, Taylor P, Richter A, Porporato A, Ågren G I. 2012. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytologist, 196, 79–91.
Nannipieri P, Ascher J, Ceccherini M T. 2003. Microbial diversity and soil functions. European Journal of Soil Science, 54, 655–670.
Pan F, Li Y, Chapman S J, Khan S, Yao H. 2016. Microbial utilization of rice straw and its derived biochar in a paddy soil. Science of the Total Environment, 559, 15–23.
Paterson E, Gebbing T, Abel C, Sim A, Telfer G. 2007. Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytologist, 173, 600–610.
Peng C J, Lai S S, Luo X S, Lu J W, Huang Q Y, Chen W L. 2016. Effects of long-term rice straw application on the microbial communities of rapeseed rhizosphere in a paddy-upland rotation system. Science of the Total Environment, 557, 231–239.
Philippot L, Spor A, Hénault C, Bru D, Bizouard F, Jones C M, Sarr A, Maron P A. 2013. Loss in microbial diversity affects nitrogen cycling in soil. ISME Journal, 7, 1609–1619.
Razanamalala K, Razafimbelo T, Maron P, Ranjard L, Chemidlin N, Lelievre M, Dequiedt S, Ramaroson V H, Marsden C, Becquer T, Trap J, Blanchart E, Bernard L. 2017. Soil microbial diversity drives the priming effect along climate gradients, a case study in Madagascar. ISME Journal, 12, 451–462.
Romaniuk R, Giuffré L, Costantini A, Nannipieri P. 2011. Assessment of soil microbial diversity measurements as indicators of soil functioning in organic and conventional horticulture systems. Ecological Indicators, 11, 1345–1353.
Rui J, Peng J, Lu Y. 2009. Succession of bacterial populations during plant residue decomposition in rice field soil. Applied and Environmental Microbiology, 75, 4879–4886.
Rutgers M, Wouterse M, Drost S M, Breure A M, Mulder C, Stone D, Creamer R E, Winding A, Bloem J. 2016. Monitoring soil bacteria with community-level physiological profiles using Biolog™ Eco-plates in the Netherlands and Europe. Applied Soil Ecology, 97, 23–35.
Samad M S, Johns C, Richards K G, Lanigan G J, de Klein C A M, Clough T J, Morales S E. 2017. Response to nitrogen addition reveals metabolic and ecological strategies of soil bacteria. Molecular Ecology, 26, 5500–5514.
Shaharoona B, Naveed M, Arshad M, Zahir Z A. 2008. Fertilizer-dependent efficiency of Pseudomonads for improving growth, yield, and nutrient use efficiency of wheat (Triticum aestivum L.). Applied Microbiology and Biotechnology, 79, 147–155
Shen J, Tang H, Liu J, Wang C, Li Y, Ge T, Jones D L, Wu J. 2014. Contrasting effects of straw and straw-derived biochar amendments on greenhouse gas emissions within double rice cropping systems. Agriculture Ecosystems & Environment, 188, 264–274.
Smith J L, Collins H P, Bailey V L. 2010. The effect of young biochar on soil respiration. Soil Biology & Biochemistry, 42, 2345–2347.
Sparling G P, Schipper L A, Hewitt A E, Degens B P. 2000. Resistance to cropping pressure of two New Zealand soils with contrasting mineralogy. Australian Journal of Soil Research, 38, 85–100.
Swallow M J B, Quideau S A. 2015. A method for determining community level physiological profiles of organic soil horizons. Soil Science Society of America Journal, 79, 536–542.
Tian J, Wang J Y, Dippold M, Gao Y, Blagodatskaya E, Kuzyakov Y. 2016. Biochar affects soil organic matter cycling and microbial functions but does not alter microbial community structure in a paddy soil. Science of the Total Environment, 556, 89–97.
Vance E D, Brookes P C, Jenkinson D S. 1987. Microbial biomass measurements in forest soils, determination of kc values and tests of hypotheses to explain the failure of the chloroform fumigation-incubation method in acid soils. Soil Biology & Biochemistry, 19, 689–696.
Wang J, Xiong Z, Kuzyakov Y. 2016. Biochar stability in soil, meta-analysis of decomposition and priming effects. Global Change Biology Bioenergy, 8, 512–523.
Wichern F, Mayer J, Joergensen R G, Muller T. 2007. Release of C and N from roots of peas and oats and their availability to soil microorganisms. Soil Biology & Biochemistry, 39, 2829–2839.
Woolf D, Amonette J E, Street-Perrott F A, Lehmann J, Joseph S. 2010. Sustainable biochar to mitigate global climate change. Nature Communication, 1, 1−9.
Wu J, Joergensen R G, Pommerening B, Chaussod R, Brookes P C. 1990. Measurement of soil microbial biomass C by fumigation-extraction - an automated procedure. Soil Biology & Biochemistry, 22, 1167–1169.
Yang W H, Zhang T X, Lin S, Ni W Z. 2017. Distance-dependent varieties of microbial community structure and metabolic functions in the rhizosphere of Sedum alfredii Hance during phytoextraction of a cadmium-contaminated soil. Environmental Science and Pollution Research, 24, 14234–14248.
Ye R Z, Doane T A, Morris J, Horwath W R. 2015. The effect of rice straw on the priming of soil organic matter and methane production in peat soils. Soil Biology & Biochemistry, 81, 98–107.
Yuan H, Ge T, Zhou P, Liu S, Roberts P, Zhu H, Tong C, Wu J. 2013. Soil microbial biomass and bacterial and fungal community structures responses to long-term fertilization in paddy soils. Journal of Soils and Sediments, 13, 877–886.
Yuan Y S, Zhao W Q, Xiao J, Zhang Z L, Qiao M F, Liu Q, Yin H J. 2017. Exudate components exert different influences on microbially mediated C losses in simulated rhizosphere soils of a spruce plantation. Plant and Soil, 419, 127–140.
Zak J C, Willig M R, Moorhead D L, Wildman H G. 1994. Functional diversity of microbial communities, a quantitative approach. Soil Biology & Biochemistry, 26, 1101–1108.
Zhang A F, Bian R J, Pan G X, Cui L Q, Hussain Q, Li L Q, Zheng J W, Zheng J F, Zhang X H, Han X J, Yu X Y. 2012. 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 Crops Research, 127, 153–160.
Zhu Z, Ge T, Hu Y, Zhou P g Wang T, Shibistova O, Guggenberger G, Su Y, Wu J. 2017. Fate of rice shoot and root residues, rhizodeposits, and microbial assimilated carbon in paddy soil-part 2: turnover and microbial utilization. Plant and Soil, 416, 243–257.
Zhu Z, Ge T, Luo Y, Liu S, Xu X, Tong C, Shibistova O, Guggenberger G, Wu J. 2018. Microbial stoichiometric flexibility regulates rice straw mineralization and its priming effect in paddy soil. Soil Biology & Biochemistry, 121, 67–76.
Zimmerman A R, Gao B, Ahn M Y. 2011. Positive and negative carbon mineralization priming effects among a variety of biochar-amended soils. Soil Biology & Biochemistry, 43, 1169–1179.
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