Spatiotemporal changes in arbuscular mycorrhizal fungal communities under different nitrogen inputs over a 5-year period in intensive agricultural ecosystems on the North China Plain

RESEARCH ARTICLE Spatiotemporal changes in arbuscular mycorrhizal fungal communities under different nitrogen inputs over a 5-year period in intensive agricultural ecosystems on the North China Plain Wei Liu1,2, Shanshan Jiang1, Yunlong Zhang1, Shanchao Yue1,3, Peter Christie1, Philip J. Murray4, Xiaolin Li1 & Junling Zhang1 1 Correspondence: Junling Zhang, College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, China. Tel.: +86 10 62732574; fax: +86 10 62731061; e-mail: Received 26 April 2014; revised 22 July 2014; accepted 1 August 2014. Final version published online 26 August 2014. MICROBIOLOGY ECOLOGY DOI: 10.1111/1574-6941.12405 Editor: Ian C. Anderson Keywords arbuscular mycorrhizal fungi; intensive agriculture; maize; nitrogen management; North China Plain. Abstract Appropriate nitrogen (N) management is important to minimize N losses from intensively managed agricultural ecosystems. Understanding the community structure of arbuscular mycorrhizal fungi (AMF) in response to N management can be of great ecological significance, particularly with the recent emphasis on the role of AMF in N cycling. A comprehensive study of both the vertical distribution of AMF in the soil profile and the temporal changes in community structure in maize roots was conducted over a 5-year period at a field site on the North China Plain. The N treatments consisted of zero N, conventional farming practice, and optimum N based on an in-season soil Nmin test. Terminal restriction fragment length polymorphism and clone sequencing were used to analyse the AMF community. Optimum N mitigated the decline in richness of AMF in the conventional N treatment in the surface soil. Diverse and species-rich AMF communities occurred deep in the soil profile. A significant difference in AMF community structure was observed between the control and fertilizer N treatments but not between the two N application strategies. AMF communities deeper in the soil profile were subsets of those richer communities in the surface soil and the loss of AMF taxa was mostly due to the absence of rare taxa. Soil pH and Nmin contents were major soil properties affecting the soil AMF communities among the N treatments while vertical distribution was influenced mainly by soil electrical conductivity. Crop phenology had a stronger influence than N treatment on the temporal shifts in AMF communities in maize roots. Our results provide evidence for the importance of N management in maintaining AMF diversity. Changes in soil chemical properties due to N fertilization, in particular declining soil pH, should be integrated in N management strategies to reduce the negative impacts on AMF communities induced by N fertilization. Excessive N inputs induced significant changes in soil physicochemical properties, especially soil acidification, and may have negative impacts on AMF communities. Introduction The application of inorganic fertilizers to agricultural soils and especially N fertilizers has increased greatly in China in recent decades. Large inputs of synthetic N fertilizers ª 2014 Federation of European Microbiological Societies. Published by John Wiley & Sons Ltd. All rights reserved lead to serious environmental problems including eutrophication, nitrate leaching, gaseous N emissions and other forms of air pollution. It is clear that microbial processes, notably nitrification and denitrification, are responsible for high rates of nitrate leaching (Kramer FEMS Microbiol Ecol 90 (2014) 436–453 College of Resources and Environmental Sciences, China Agricultural University, Beijing, China; 2College of Landscape and Art, Jiangxi Agricultural University, Nanchang, China; 3State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Northwest A&F University, Yangling, China; and 4Sustainable Soil and Grassland System, Rothamsted Research, Okehampton, Devon, UK AMF community changes and N management in intensive agriculture FEMS Microbiol Ecol 90 (2014) 436–453 et al., 2014). Large differences in AMF communities between soils and roots (Hempel et al., 2007; Chen et al., 2014) have been due to the seasonal nature of AMF communities (Liu et al., 2009) but may also be related to the phenological development and nutrient requirements of the crop (Tian et al., 2011, 2013). Therefore, more systematic investigations into AMF communities in soils and roots in response to N fertilization might allow us to better understand the potential functioning of mycorrhizal fungal species and communities. In the present study we have undertaken a comprehensive comparison of the vertical distribution of the AMF community in soil and its temporal structure in maize roots under different N management treatments over a 5-year period at a field experimental site located in an intensive agricultural area on the North China Plain. This is an important agricultural production region in China which provides more than 75% of the national wheat crop and 35% of the maize (CAY, 2009) and it is one of the most intensively managed agricultural regions in the country. From 1949 to 2009 the wheat and maize yields here increased from 0.6 and 0.7 t ha1 to 5.4 and 5.6 t ha1, respectively. However, the average amount of N applied for the winter wheat–summer maize doublecropping system has increased from 143 kg N ha1 in 1967 to about 384 kg N ha1 in 1988 and 670 kg N ha1 in 2000 (a 368.5% increase from 1967 to 2000; Zhen et al., 2006). The annual N application rate for typical wheat–maize rotation systems varies from 500 to 600 kg N ha1 year1 but the crop requirements are only 200–300 kg N ha1 year1 (Cui et al., 2010). As a consequence of excessive fertilizer N application, the partial factor productivity from applied N (PFPn) decreased from 46 kg kg1 in 1978 to 21 kg kg1 in 1998. Furthermore, a number of environmental problems occur, including groundwater pollution by NO 3 -N (Zhu & Chen, 2002; Ju et al., 2006), air pollution due to N deposition (Liu et al., 2003) and soil acidification (Guo et al., 2010). An in-season N management strategy based on the soil Nmin test has been developed during the last decade to solve the problem of excessive N application in intensive agricultural systems in this region (Liu et al., 2003; Chen et al., 2006). N fertilizer is applied twice or three times during the crop growing season and the optimum N rate is determined based on target soil N values and actual soil nitrate-N values in the root zone at different growth stages (Cui et al., 2008). The results show that 79% of fertilizer N can be saved without a significant reduction in crop yields compared with conventional farming practice (Zhao et al., 2006). A number of studies based on spore inventories (Oehl et al., 2004, 2005; Tian et al., 2011) and molecular ª 2014 Federation of European Microbiological Societies. Published by John Wiley & Sons Ltd. All rights reserved et al., 2006) or gaseous N (...truncated)