Microbial community structure and functional metabolic diversity are associated with organic carbon availability in an agricultural soil
LI Juan, LI Yan-ting, YANG Xiang-dong, ZHANG Jian-jun, LIN Zhi-an, ZHAO Bing-qiang
Key Laboratory of Plant Nutrition and Fertilizer, Ministry of Agriculture/Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
摘要 Exploration of soil environmental characteristics governing soil microbial community structure and activity may improve our understanding of biogeochemical processes and soil quality. The impact of soil environmental characteristics especially organic carbon availability after 15-yr different organic and inorganic fertilizer inputs on soil bacterial community structure and functional metabolic diversity of soil microbial communities were evaluated in a 15-yr fertilizer experiment in Changping County, Beijing, China. The experiment was a wheat-maize rotation system which was established in 1991 including four different fertilizer treatments. These treatments included: a non-amended control (CK), a commonly used application rate of inorganic fertilizer treatment (NPK); a commonly used application rate of inorganic fertilizer with swine manure incorporated treatment (NPKM), and a commonly used application rate of inorganic fertilizer with maize straw incorporated treatment (NPKS). Denaturing gradient gel electrophoresis (DGGE) of the 16S rRNA gene was used to determine the bacterial community structure and single carbon source utilization profiles were determined to characterize the microbial community functional metabolic diversity of different fertilizer treatments using Biolog Eco plates. The results indicated that long-term fertilized treatments significantly increased soil bacterial community structure compared to CK. The use of inorganic fertilizer with organic amendments incorporated for long term (NPKM, NPKS) significantly promoted soil bacterial structure than the application of inorganic fertilizer only (NPK), and NPKM treatment was the most important driver for increases in the soil microbial community richness (S) and structural diversity (H). Overall utilization of carbon sources by soil microbial communities (average well color development, AWCD) and microbial substrate utilization diversity and evenness indices (H’ and E) indicated that long-term inorganic fertilizer with organic amendments incorporated (NPKM, NPKS) could significantly stimulate soil microbial metabolic activity and functional diversity relative to CK, while no differences of them were found between NPKS and NPK treatments. Principal component analysis (PCA) based on carbon source utilization profiles also showed significant separation of soil microbial community under long-term fertilization regimes and NPKM treatment was significantly separated from the other three treatments primarily according to the higher microbial utilization of carbohydrates, carboxylic acids, polymers, phenolic compounds, and amino acid, while higher utilization of amines/amides differed soil microbial community in NPKS treatment from those in the other three treatments. Redundancy analysis (RDA) indicated that soil organic carbon (SOC) availability, especially soil microbial biomass carbon (Cmic) and Cmic/SOC ratio are the key factors of soil environmental characteristics contributing to the increase of both soil microbial community structure and functional metabolic diversity in the long-term fertilization trial. Our results showed that long-term inorganic fertilizer and swine manure application could significantly improve soil bacterial community structure and soil microbial metabolic activity through the increases in SOC availability, which could provide insights into the sustainable management of China’s soil resource.
Abstract Exploration of soil environmental characteristics governing soil microbial community structure and activity may improve our understanding of biogeochemical processes and soil quality. The impact of soil environmental characteristics especially organic carbon availability after 15-yr different organic and inorganic fertilizer inputs on soil bacterial community structure and functional metabolic diversity of soil microbial communities were evaluated in a 15-yr fertilizer experiment in Changping County, Beijing, China. The experiment was a wheat-maize rotation system which was established in 1991 including four different fertilizer treatments. These treatments included: a non-amended control (CK), a commonly used application rate of inorganic fertilizer treatment (NPK); a commonly used application rate of inorganic fertilizer with swine manure incorporated treatment (NPKM), and a commonly used application rate of inorganic fertilizer with maize straw incorporated treatment (NPKS). Denaturing gradient gel electrophoresis (DGGE) of the 16S rRNA gene was used to determine the bacterial community structure and single carbon source utilization profiles were determined to characterize the microbial community functional metabolic diversity of different fertilizer treatments using Biolog Eco plates. The results indicated that long-term fertilized treatments significantly increased soil bacterial community structure compared to CK. The use of inorganic fertilizer with organic amendments incorporated for long term (NPKM, NPKS) significantly promoted soil bacterial structure than the application of inorganic fertilizer only (NPK), and NPKM treatment was the most important driver for increases in the soil microbial community richness (S) and structural diversity (H). Overall utilization of carbon sources by soil microbial communities (average well color development, AWCD) and microbial substrate utilization diversity and evenness indices (H’ and E) indicated that long-term inorganic fertilizer with organic amendments incorporated (NPKM, NPKS) could significantly stimulate soil microbial metabolic activity and functional diversity relative to CK, while no differences of them were found between NPKS and NPK treatments. Principal component analysis (PCA) based on carbon source utilization profiles also showed significant separation of soil microbial community under long-term fertilization regimes and NPKM treatment was significantly separated from the other three treatments primarily according to the higher microbial utilization of carbohydrates, carboxylic acids, polymers, phenolic compounds, and amino acid, while higher utilization of amines/amides differed soil microbial community in NPKS treatment from those in the other three treatments. Redundancy analysis (RDA) indicated that soil organic carbon (SOC) availability, especially soil microbial biomass carbon (Cmic) and Cmic/SOC ratio are the key factors of soil environmental characteristics contributing to the increase of both soil microbial community structure and functional metabolic diversity in the long-term fertilization trial. Our results showed that long-term inorganic fertilizer and swine manure application could significantly improve soil bacterial community structure and soil microbial metabolic activity through the increases in SOC availability, which could provide insights into the sustainable management of China’s soil resource.
This research was funded by the National Natural Science Foundation of China (NSFC, 31301843) and the National Nonprofit Institute Research Grant of Chinese Academy of Agricultural Sciences (IARRP-202-5).
LI Juan, LI Yan-ting, YANG Xiang-dong, ZHANG Jian-jun, LIN Zhi-an, ZHAO Bing-qiang .
2015.
Microbial community structure and functional metabolic diversity are associated with organic carbon availability in an agricultural soil. Journal of Integrative Agriculture, 14(12): 2500-2511.
Allison S D, Martiny J B H. 2008. Resistance, resilience, andredundancy in microbial communities. Proceedings of theNational Academy of Sciences of the United States ofAmerica, 105, 11512-11519
Balser T C, Firestone M K. 2005. Linking microbial communitystructure and soil processes in a California annual grasslandand mixed-conifer forest. Biogeochemistry, 73, 395-415
Bastian F, Bouziri L, Nicolardot B, Ranjard L. 2009. Impactof wheat straw decomposition on successional patternsof soil microbial community structure. Soil Biology andBiochemistry, 41, 262-275
Beauregard M S, Hamel C, St-Arnaud M. 2010. Long-termphosphorus fertilization impacts soil fungal and bacterialdiversity but not AM fungal community in alfalfa. MicrobialEcology, 59, 379-389
Chu H, Fujii T, Morimoto S, Lin X, Yagi K, Hu J, Zhang J.2007. Community structure of ammonia-oxidizing bacteriaunder long-term application of mineral fertilizer and organicmanure in a sandy loam soil. Applied and EnvironmentalMicrobiology, 73, 485-491
Cocolin L, Aggio D, Manzano M, Cantoni C, Comi G. 2002.An application of PCR-DGGE analysis to profile the yeastpopulations in raw milk. International Dairy Journal, 12,407-411
Cookson W R, Abaye D A, Marschner P, Murphy D V, StockdaleE A, Goulding K W. 2005. The contribution of soil organicmatter fractions to carbon and nitrogen mineralization andmicrobial community size and structure. Soil Biology andBiochemistry, 37, 1726-1737
Cookson W R, Murphy D V, Roper M M. 2008. Characterizingthe relationships between soil organic matter componentsand microbial function and composition along a tillagedisturbance gradient. Soil Biology and Biochemistry, 40,763-777
Degens B P, Schipper L A, Sparling G P, Vojvodic-Vukovich M.2000. Decreases in organic C reserves in soils can reducethe metabolic diversity of soil microbial communities. SoilBiology and Biochemistry, 32, 189-196
Drenovsky R E V D, Graham K J, Scow K M. 2004.Soil water content and organic carbon availabilityare major determinants of soil microbial communitycomposition. Microbial Ecology, 48, 424-430
Eilers K G, Lauber C L, Knight R, Fierer N. 2010. Shifts inbacterial community structure associated with inputs of lowmolecular weight carbon compounds to soil. Soil Biologyand Biochemistry, 42, 896-903
Elfstrand S, Hedlund K, Martensson A. 2007. Soil enzymeactivities, microbial community composition and functionafter 47 years of continuous green manuring. Applied SoilEcology, 35, 610-621
Enwall K, Philippot L, Hallin S. 2005. Activity and compositionof the denitrifying bacterial community respond differently to long-term fertilization. Applied Environmental Microbiology,71, 8335-8343Fan F, Li Z, Wakelin S A, Yu W, Liang Y
2012. Mineral fertilizeralters cellulolytic community structure and suppressessoil cellobiohydrolase activity in a long-term fertilizationexperiment. Soil Biology and Biochemistry, 55, 70-77
Franco W, Frank R, Martin H, Andreas F. 2006. Communitystructures and substrate utilization of bacteria in soils fromorganic and conventional farming systems of the DOK longtermfield experiment. Applied Soil Ecology, 33, 294-307
Garland J L, Mills A L. 1991. Classification and characterizationof heterotrophic microbial communities on basis of pattersof community level sole-carbon-source utilization. AppliedEnvironmental Microbiology, 57, 2351-2359
Ge Y, Zhang J B, Zhang L M, Yang M, He J Z. 2008. Long-termfertilization regimes affect bacterial community structure anddiversity of an agricultural soil in northern China. Journal ofSoils and Sediments, 8, 43-50
Geisseler D, Scow K M. 2014. Long-term effects of mineralfertilizers on soil microorganisms - A review. Soil Biologyand Biochemistry, 75, 54-63
Giacometti C, Demyan M S, Cavani L, Marzadori C, Ciavatta C,Kandeler E. 2013. Chemical and microbiological soil qualityindicators and their potential to differentiate fertilizationregimes in temperate agroecosystems. Applied SoilEcology, 64, 32-48
Gong W, Yan X Y, Wang J Y, Hu T X, Gong Y B. 2009. Longtermmanure and fertilizer effects on soil organic matterfractions and microbes under a wheat-maize croppingsystem in northern China. Geoderma, 149, 318-324
Gu Y, Zhang X, Tu S, Lindström K. 2009. Soil microbial biomass,crop yields, and bacterial community structure as affectedby long-term fertilizer treatments under wheat-rice cropping.European Journal of Soil Biology, 45, 239-246
Hallin S, Jones C M, Schloter M, Philippot L. 2009. Relationshipbetween N-cycling communities and ecosystem functioningin a 50-year-old fertilization experiment. The ISMEJournal, 3, 597-605
Haynes R J. 2005. Labile organic matter fractions as centralcomponents of the quality of agricultural soils: anoverview. Advances in Agronomy, 85, 221-268
He J Z, Shen J P, Zhang L M, Zhu Y G, Zheng Y M, Xu M G,Di H. 2007. Quantitative analyses of the abundance andcomposition of ammonia-oxidizing bacteria and ammoniaoxidizingarchaea of a Chinese upland red soil under longtermfertilization practices. Environmental Microbiology, 9,2364-2374
Kong W D, Zhu Y G, Fu B J, Han X Z, Zhang L, He J Z. 2008.Effect of long-term application of chemical fertilizers onmicrobial biomass and functional diversity of a blacksoil. Pedosphere, 18, 801-808
Larkin R P, Honeycutt C W. 2006. Effects of different 3-yearcropping systems on soil microbial communities andRhizoctonia diseases of potato. Phytopathology, 96, 68-79
Lejon D P, Sebastia J, Lamy I, Chaussod R, Ranjard L.2007. Relationships between soil organic status andmicrobial community density and genetic structure in twoagricultural soils submitted to various types of organicmanagement. Microbial Ecology, 53, 650-663
Levy-Booth D J, Prescott C E, Grayston S J. 2014. Microbialfunctional genes involved in nitrogen fixation, nitrificationand denitrification in forest ecosystems. Soil Biology andBiochemistry, 75, 11-25
Li C, Yan K, Tang L, Jia Z, Li Y. 2014. Change in deep soilmicrobial communities due to long-term fertilization. SoilBiology and Biochemistry, 75, 264-272
Li F, Liu M, Li Z, Jiang C, Han F, Che Y. 2013. Changes in soilmicrobial biomass and functional diversity with a nitrogengradient in soil columns. Applied Soil Ecology, 64, 1-6
Li J, Zhao B Q, Li X Y, Jiang R B, So H B. 2008. Effects oflong-term combined application of organic and mineralfertilizers on microbial biomass, soil enzyme activities andsoil fertility. Agricultural Sciences in China, 7, 336-343
Li J, Cooper J M, Lin Z A, Li Y, Yang X, Zhao B. 2015. Soilmicrobial community structure and function are significantlyaffected by long-term organic and mineral fertilizationregimes in the North China Plain. Applied Soil Ecology, 96,75-87
Lipson D A, Schmidt S K, Monson R K. 2000. Carbon availabilityand temperature control the post-snowmelt decline in alpinesoil microbial biomass. Soil Biology and Biochemistry, 32,441-448
Liu B, Gumpertz M L, Hu S, Ristaino J B. 2007. Long-termeffects of organic and synthetic soil fertility amendments onsoil microbial communities and the development of southernblight. Soil Biology and Biochemistry, 39, 2302-2316
Liu M, Hu F, Chen X, Huang Q, Jiao J, Zhang B, Li H. 2009.Organic amendments with reduced chemical fertilizerpromote soil microbial development and nutrient availabilityin a subtropical paddy field: the influence of quantity, typeand application time of organic amendments. Applied SoilEcology, 42, 166-175
Lu R K. 2000. The Analysis Method of Soil AgriculturalChemistry. Chinese Agricultural Sciences and TechnologyPress. (in Chinese)
Marschner P, Kandeler E, Marschner B. 2003. Structure andfunction of the soil microbial community in a long-termfertilizer experiment. Soil Biology and Biochemistry, 35,453-461
Moffett B F, Nicholson F A, Uwakwe N C, Chambers B J, HarrisJ A, Hill T C J. 2003. Zinc contamination decreases thebacterial diversity of agricultural soil. FEMS MicrobiologyEcology, 43, 13-19
Muyzer G, De Waal E C, Uitterlinden A G. 1993. Profilingof complex microbial populations by denaturing gelelectrophoresis analysis of polymerase chain reactionamplifiedgenes coding for 16S rRNA. Applied EnvironmentalMicrobiology, 59, 695-700
Nelson P N, Dictor M C, Soulas, G. 1994. Availability of organiccarbon in soluble and particle-size fractions from a soilprofile. Soil Biology and Biochemistry, 26, 1549-1555
Ogilvie L A, Hirsch P R, Johnston A W B. 2008. Bacterial diversity of the broadbalk ‘classical’ winter wheat experimentin relation to long-term fertilizer inputs. Microbial Ecology,56, 525-537
O’Donnell A G, Seasman M, Macrae A, Waite I, Davies J T.2001. Plants and fertilizers as drivers of change in microbialcommunity structure and function in soils. Plant and Soil,232, 135-145
Orr C H, James A, Leifert C, Cooper J M, Cummings S P. 2011.Diversity and activity of free-living nitrogen-fixing bacteriaand total bacteria in organic and conventionally managedsoils. Applied and Environmental Microbiology, 77,911-919
Rademaker J L W, Louws F J, Rossbach U, Vinuesa P, DeBruijn F J. 1999. Computer-assisted pattern analysis ofmolecular fingerprints and database construction. MolecularMicrobial Ecology Manual, 7, 1-33
Sarathchandra S U, Ghani A, Yeates G W, Burch G, Cox NR. 2001. Effect of nitrogen and phosphate fertilisers onmicrobial and nematode diversity in pasture soils. SoilBiology and Biochemistry, 33, 953-964
Sharma S K, Ramesh A, Sharma M P, Joshi O P, GovaertsB, Steenwerth K L, Karlen D L. 2011. Microbial communitystructure and diversity as indicators for evaluating soilquality. In: Biodiversity, Biofuels, Agroforestry andConservation Agriculture. Springer Netherland. pp. 317-358Shen J P, Zhang L M, Guo J F, Ray J L, He J Z
2010. Impactof long-term fertilization practices on the abundance andcomposition of soil bacterial communities in NortheastChina. Applied Soil Ecology, 46, 119-124
Sikora L J, McCoy J L. 1990. Attempts to determine availablecarbon in soils. Biology and Fertility of Soils, 9, 19-24
Su J Q, Ding L J, Xue K, Yao H Y, Quensen J, Bai S J, Wei WX, Wu J S, Zhou J Z, Tiedje J M, Zhu Y G. 2015. Long-termbalanced fertilization increases the soil microbial functionaldiversity in a phosphorus-limited paddy soil. MolecularEcology, 24, 136-150
Sun R, Zhang X X, Guo X, Wang D, Chu H. 2015. Bacterialdiversity in soils subjected to long-term chemical fertilizationcan be more stably maintained with the addition of livestockmanure than wheat straw. Soil Biology and Biochemistry,88, 9-18
Sradnick A, Murugan R, Oltmanns M, Raupp J, Joergensen RG. 2013. Changes in functional diversity of the soil microbialcommunity in a heterogeneous sandy soil after long-termfertilization with cattle manure and mineral fertilizer. AppliedSoil Ecology, 63, 23-28
Vance E D, Brookes P C, Jenkinson D S. 1987. An extractionmethod for measuring soil microbial biomass C. Soil Biologyand Biochemistry, 19, 703-707
Vineela C, Wani S P, Srinivasarao C, Padmaja B, Vittal KP R. 2008. Microbial properties of soils as affected bycropping and nutrient management practices in severallong-term manurial experiments in the semi-arid tropics ofIndia. Applied Soil Ecology, 40, 165-173
Watts D B, Torbert H A, Feng Y, Prior S A. 2010. Soil microbialcommunity dynamics as influenced by composted dairymanure, soil properties, and landscape position. SoilScience, 175, 474-486
Wessén E, Nyberg K, Jansson J K, Hallin S. 2010. Responsesof bacterial and archaeal ammonia oxidizers to soil organicand fertilizer amendments under long-term management.Applied Soil Ecology, 45, 193-200.Wu M, Qin H, Chen Z, Wu J, Wei W. 2011. Effect of long-termfertilization on bacterial composition in rice paddy soil.Biology and Fertility of Soils, 47, 397-405
Yu C, Hu X M, Deng W, Li Y, Xiong C, Ye C H, Han G M, Li,X. 2015. Changes in soil microbial community structureand functional diversity in the rhizosphere surroundingmulberry subjected to long-term fertilization. Applied SoilEcology, 86, 30-40
Zhao J, Ni T, Li Y, Xiong W, Ran W, Shen B, Shen Q R, ZhangR F. 2014. Responses of bacterial communities in arablesoils in a rice-wheat cropping system to different fertilizerregimes and sampling times. PLOS ONE, 9, e85301.
Zhong W, Gu T, Wang W, Zhang B, Lin X, Huang Q, Shen W.2010. The effects of mineral fertilizer and organic manure onsoil microbial community and diversity. Plant and Soil, 326,511-522
Zhong W H, Cai Z C. 2007. Long-term effects of inorganicfertilizers on microbial biomass and community functionaldiversity in a paddy soil derived from quaternary redclay. Applied Soil Ecology, 36, 84-91
Zhou J, Bruns M A, Tiedje J M. 1996. DNA recovery from soils ofdiverse composition. Applied Environmental Microbiology,62, 316-322