Linking cropland ecosystem services to microbiome taxonomic composition and functional composition in a sandy loam soil with 28-year organic and inorganic fertilizer regimes

Abstract The ability of soil microorganisms to uphold a variety of ecosystem services is of increasing interest, but our understanding of the linkage between cropland ecosystem services and the soil microbiome under long-term different fertilizer regimes is still limited. Here, we measured 15 response variables commonly used as indicators of cropland ecosystem services, and employed a shotgun metagenomic sequencing technology to determine microbiome taxonomic composition and functional composition in a sandy loam soil amended with organic and inorganic fertilizers for 28 years. Long-term application of fertilizers had overall positive effects on the variables that indicate soil C and nutrient status, organic material decomposition, nutrient transformation, and plant productivity, but the strength of these effects differed between organic and inorganic fertilization. In long term, organic fertilizers significantly increased the abundance of Sphingomonas and Acidobacteria as well as genes involved in C and N metabolism and degradation of aromatic organic compounds. The observed differences in the indicators of overall biological activity, litter decomposition, nutrient transformation, cropland fertility and productivity were associated with changes in taxonomic composition and functional composition of the soil microbiome. Network analysis revealed that soil organic C, total N, L-leucine aminopeptidase, phosphatase, microbial biomass C and N, and the multifunctionality index showed strong positive associations with Acidobacterium, Lysobacter and Nitrososphaera. These microbes are implicated in the decomposition of organic material, soil C and N transformation, and plant growth promotion. The present study deepens our understanding of the relationship between the soil microbiome and agro-ecosystem functioning, and provides support for the use of organic fertilization strategy to enhance multiple ecosystem services in croplands.

[1]  R. Fulthorpe,et al.  Seasonal variation of bacterial endophytes in urban trees , 2015, Front. Microbiol..

[2]  J. Domínguez,et al.  Short-term effects of organic and inorganic fertilizers on soil microbial community structure and function , 2013, Biology and Fertility of Soils.

[3]  P. Shannon,et al.  Cytoscape: a software environment for integrated models of biomolecular interaction networks. , 2003, Genome research.

[4]  Andreas Richter,et al.  Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil , 2011, Proceedings of the National Academy of Sciences.

[5]  N. Jehmlich,et al.  The active microbial diversity drives ecosystem multifunctionality and is physiologically related to carbon availability in Mediterranean semi‐arid soils , 2016, Molecular ecology.

[6]  Adam Godzik,et al.  Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences , 2006, Bioinform..

[7]  T. Wubet,et al.  Mineral vs. Organic Amendments: Microbial Community Structure, Activity and Abundance of Agriculturally Relevant Microbes Are Driven by Long-Term Fertilization Strategies , 2016, Front. Microbiol..

[8]  J. Kirkegaard,et al.  Network analysis reveals functional redundancy and keystone taxa amongst bacterial and fungal communities during organic matter decomposition in an arable soil , 2016 .

[9]  C. Pepe-Ranney,et al.  Dynamics of microbial community composition and soil organic carbon mineralization in soil following addition of pyrogenic and fresh organic matter , 2015, The ISME Journal.

[10]  H. Chu,et al.  High throughput sequencing analysis of biogeographical distribution of bacterial communities in the black soils of northeast China , 2014 .

[11]  D. Ercolini,et al.  Organic farming induces changes in soil microbiota that affect agro-ecosystem functions , 2016 .

[12]  Jia-bao Zhang,et al.  Mortierella elongata's roles in organic agriculture and crop growth promotion in a mineral soil , 2018 .

[13]  Bingzi Zhao,et al.  Bacterial community structure in maize stubble-amended soils with different moisture levels estimated by bar-coded pyrosequencing , 2015 .

[14]  G. Robertson,et al.  Nitrogen in Agriculture: Balancing the Cost of an Essential Resource , 2009 .

[15]  T. Urich,et al.  Metatranscriptomic Analysis of Arctic Peat Soil Microbiota , 2014, Applied and Environmental Microbiology.

[16]  Bingqiang Zhao,et al.  Soil microbial community structure and function are significantly affected by long-term organic and mineral fertilization regimes in the North China Plain , 2015 .

[17]  Xuewen Huang,et al.  Plant Species Richness and Ecosystem Multifunctionality in Global Drylands , 2012, Science.

[18]  J. Stolz,et al.  Nitrate and periplasmic nitrate reductases. , 2014, Chemical Society reviews.

[19]  V. Gupta,et al.  Soil microbial biomass: A key soil driver in management of ecosystem functioning. , 2018, The Science of the total environment.

[20]  Hong-bo Hu,et al.  Comparative genomic analysis of 26 Sphingomonas and Sphingobium strains: Dissemination of bioremediation capabilities, biodegradation potential and horizontal gene transfer. , 2017, The Science of the total environment.

[21]  Jiachao Zhang,et al.  Response of denitrifying genes coding for nitrite (nirK or nirS) and nitrous oxide (nosZ) reductases to different physico-chemical parameters during agricultural waste composting , 2015, Applied Microbiology and Biotechnology.

[22]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[23]  Y. Bromberg,et al.  Comparative genomic and physiological analysis provides insights into the role of Acidobacteria in organic carbon utilization in Arctic tundra soils. , 2012, FEMS microbiology ecology.

[24]  P. Brookes,et al.  Structural and functional differentiation of the root-associated bacterial microbiomes of perennial ryegrass , 2016 .

[25]  M. Grube,et al.  Differential sharing and distinct co‐occurrence networks among spatially close bacterial microbiota of bark, mosses and lichens‬‬ , 2017, Molecular ecology.

[26]  T. Lueders,et al.  Identification of Bacterial Micropredators Distinctively Active in a Soil Microbial Food Web , 2006, Applied and Environmental Microbiology.

[27]  G. Kowalchuk,et al.  Bio-fertilizer application induces soil suppressiveness against Fusarium wilt disease by reshaping the soil microbiome , 2017 .

[28]  M. Borodovsky,et al.  Ab initio gene identification in metagenomic sequences , 2010, Nucleic acids research.

[29]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[30]  E. Blagodatskaya,et al.  Maize phenology alters the distribution of enzyme activities in soil : Field estimates , 2018 .

[31]  Youzhi Feng,et al.  Long-term balanced fertilization decreases arbuscular mycorrhizal fungal diversity in an arable soil in North China revealed by 454 pyrosequencing. , 2012, Environmental science & technology.

[32]  Jason P. Kaye,et al.  Functional diversity in cover crop polycultures increases multifunctionality of an agricultural system , 2017 .

[33]  Changrong Yan,et al.  Long-term effect of chemical fertilizer, straw, and manure on soil chemical and biological properties in northwest China , 2010 .

[34]  Jian Wang,et al.  SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler , 2012, GigaScience.

[35]  J. Fuhrman General Distributions and the 'rare Biosphere' Microbial Community Structure and Its Functional Implications Review Insight , 2022 .

[36]  Jizhong Zhou,et al.  Soil genomics , 2009, Nature Reviews Microbiology.

[37]  Noah Fierer,et al.  Using network analysis to explore co-occurrence patterns in soil microbial communities , 2011, The ISME Journal.

[38]  Han Meng,et al.  A More Comprehensive Community of Ammonia-Oxidizing Archaea (AOA) Revealed by Genomic DNA and RNA Analyses of amoA Gene in Subtropical Acidic Forest Soils , 2017, Microbial Ecology.

[39]  Honghui Zhu,et al.  Metagenomic evidence of stronger effect of stylo (legume) than bahiagrass (grass) on taxonomic and functional profiles of the soil microbial community , 2017, Scientific Reports.

[40]  P. Reich,et al.  Microbial richness and composition independently drive soil multifunctionality , 2017 .

[41]  J. Postma,et al.  Diversity and Activity of Lysobacter Species from Disease Suppressive Soils , 2015, Front. Microbiol..

[42]  J. Prosser,et al.  Plant host habitat and root exudates shape soil bacterial community structure , 2008, The ISME Journal.

[43]  Jiabao Zhang,et al.  Effects of long-term (23 years) mineral fertilizer and compost application on physical properties of fluvo-aquic soil in the North China Plain , 2016 .

[44]  M. V. D. van der Heijden,et al.  Soil biodiversity and soil community composition determine ecosystem multifunctionality , 2014, Proceedings of the National Academy of Sciences.

[45]  Xiaoyuan Yan,et al.  Long-term manure and fertilizer effects on soil organic matter fractions and microbes under a wheat-maize cropping system in northern China , 2009 .

[46]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[47]  Jiabao Zhang,et al.  Yield, phosphorus use efficiency and balance response to substituting long-term chemical fertilizer use with organic manure in a wheat-maize system , 2017 .

[48]  M. J. Hensel,et al.  Biodiversity enhances ecosystem multifunctionality across trophic levels and habitats , 2015, Nature Communications.

[49]  E. Kandeler,et al.  Structure and function of the soil microbial community in a long-term fertilizer experiment , 2003 .

[50]  D. Geisseler,et al.  Long-term effects of mineral fertilizers on soil microorganisms – A review , 2014 .

[51]  Xin-ping Chen,et al.  Improving crop productivity and resource use efficiency to ensure food security and environmental quality in China. , 2012, Journal of experimental botany.

[52]  Investigating the relationship between biodiversity and ecosystem multifunctionality: challenges and solutions , 2013, 1305.1985.

[53]  Michael Mitzenmacher,et al.  Detecting Novel Associations in Large Data Sets , 2011, Science.

[54]  Alwyn Williams,et al.  The effects of 55 years of different inorganic fertiliser regimes on soil properties and microbial community composition , 2013 .

[55]  J. Blesh Functional traits in cover crop mixtures: Biological nitrogen fixation and multifunctionality , 2018 .

[56]  K. Tatsumi,et al.  Biodegradation of polycyclic aromatic hydrocarbons by Sphingomonas sp. enhanced by water-extractable organic matter from manure compost. , 2009, The Science of the total environment.

[57]  Y. Kuzyakov,et al.  Maize rhizosphere priming: field estimates using 13C natural abundance , 2016, Plant and Soil.

[58]  S. Hart,et al.  Meta-analysis reveals ammonia-oxidizing bacteria respond more strongly to nitrogen addition than ammonia-oxidizing archaea , 2016 .

[59]  Anne-Kristin Kaster,et al.  Methanogenic archaea: ecologically relevant differences in energy conservation , 2008, Nature Reviews Microbiology.

[60]  Marcel Martin Cutadapt removes adapter sequences from high-throughput sequencing reads , 2011 .

[61]  P. Reich,et al.  Relative importance of soil properties and microbial community for soil functionality: insights from a microbial swap experiment , 2016 .

[62]  Jia-bao Zhang,et al.  Bacterial Community Structure after Long-term Organic and Inorganic Fertilization Reveals Important Associations between Soil Nutrients and Specific Taxa Involved in Nutrient Transformations , 2017, Front. Microbiol..

[63]  M. Stieglmeier,et al.  Nitrososphaera viennensis gen. nov., sp. nov., an aerobic and mesophilic, ammonia-oxidizing archaeon from soil and a member of the archaeal phylum Thaumarchaeota , 2014, International journal of systematic and evolutionary microbiology.

[64]  Yuemao Shen,et al.  Bioactive natural products from Lysobacter. , 2012, Natural product reports.

[65]  Martin Schaefer,et al.  Land use intensification alters ecosystem multifunctionality via loss of biodiversity and changes to functional composition , 2015, Ecology letters.