Response of the Abundance of Key Soil Microbial Nitrogen-Cycling Genes to Multi-Factorial Global Changes

PLOS ONE, Dec 2019

Multiple co-occurring environmental changes are affecting soil nitrogen cycling processes, which are mainly mediated by microbes. While it is likely that various nitrogen-cycling functional groups will respond differently to such environmental changes, very little is known about their relative responsiveness. Here we conducted four long-term experiments in a steppe ecosystem by removing plant functional groups, mowing, adding nitrogen, adding phosphorus, watering, warming, and manipulating some of their combinations. We quantified the abundance of seven nitrogen-cycling genes, including those for fixation (nifH), mineralization (chiA), nitrification (amoA of ammonia-oxidizing bacteria (AOB) or archaea (AOA)), and denitrification (nirS, nirK and nosZ). First, for each gene, we compared its sensitivities to different environmental changes and found that the abundances of various genes were sensitive to distinct and different factors. Overall, the abundances of nearly all genes were sensitive to nitrogen enrichment. In addition, the abundances of the chiA and nosZ genes were sensitive to plant functional group removal, the AOB-amoA gene abundance to phosphorus enrichment when nitrogen was added simultaneously, and the nirS and nirK gene abundances responded to watering. Second, for each single- or multi-factorial environmental change, we compared the sensitivities of the abundances of different genes and found that different environmental changes primarily affected different gene abundances. Overall, AOB-amoA gene abundance was most responsive, followed by the two denitrifying genes nosZ and nirS, while the other genes were less sensitive. These results provide, for the first time, systematic insights into how the abundance of each type of nitrogen-cycling gene and the equilibrium state of all these nitrogen-cycling gene abundances would shift under each single- or multi-factorial global change.

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Response of the Abundance of Key Soil Microbial Nitrogen-Cycling Genes to Multi-Factorial Global Changes

et al. (2013) Response of the Abundance of Key Soil Microbial Nitrogen-Cycling Genes to Multi-Factorial Global Changes. PLoS ONE 8(10): e76500. doi:10.1371/journal.pone.0076500 Response of the Abundance of Key Soil Microbial Nitrogen-Cycling Genes to Multi-Factorial Global Changes Ximei Zhang 0 Wei Liu 0 Michael Schloter 0 Guangming Zhang 0 Quansheng Chen 0 Jianhui Huang 0 Linghao Li 0 James J. Elser 0 Xingguo Han 0 Mickael Desvaux, INRA Clermont-Ferrand Research Center, France 0 1 State Key Laboratory of Forest and Soil Ecology, Institute of Applied Ecology, Chinese Academy of Sciences , Shenyang , China , 2 State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences , Beijing , China , 3 State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences , Beijing, China, 4 Environmental Genomics , Helmholtz Center for Environmental Health , Oberschleissheim, Germany , 5 School of Life Sciences, Arizona State University , Tempe, Arizona , United States of America Multiple co-occurring environmental changes are affecting soil nitrogen cycling processes, which are mainly mediated by microbes. While it is likely that various nitrogen-cycling functional groups will respond differently to such environmental changes, very little is known about their relative responsiveness. Here we conducted four long-term experiments in a steppe ecosystem by removing plant functional groups, mowing, adding nitrogen, adding phosphorus, watering, warming, and manipulating some of their combinations. We quantified the abundance of seven nitrogen-cycling genes, including those for fixation (nifH), mineralization (chiA), nitrification (amoA of ammonia-oxidizing bacteria (AOB) or archaea (AOA)), and denitrification (nirS, nirK and nosZ). First, for each gene, we compared its sensitivities to different environmental changes and found that the abundances of various genes were sensitive to distinct and different factors. Overall, the abundances of nearly all genes were sensitive to nitrogen enrichment. In addition, the abundances of the chiA and nosZ genes were sensitive to plant functional group removal, the AOB-amoA gene abundance to phosphorus enrichment when nitrogen was added simultaneously, and the nirS and nirK gene abundances responded to watering. Second, for each single- or multifactorial environmental change, we compared the sensitivities of the abundances of different genes and found that different environmental changes primarily affected different gene abundances. Overall, AOB-amoA gene abundance was most responsive, followed by the two denitrifying genes nosZ and nirS, while the other genes were less sensitive. These results provide, for the first time, systematic insights into how the abundance of each type of nitrogen-cycling gene and the equilibrium state of all these nitrogen-cycling gene abundances would shift under each single- or multi-factorial global change. - Funding: This work was supported by the National Natural Science Foundation of China(30830026) and the State Key Basic Research Development Program of China (973 Program) (2009CB825103), Postdoctoral Science Foundation of China (2011M500440, 2012T50158), and the US National Science Foundation (DEB0925017). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Nitrogen (N) cycling is one of the most important ecosystem functions and most soil N-cycling processes are driven by microbes [14]. For example, N fixing microbes convert N2 into NH4+, providing most of the N ultimately used by organisms on Earth [5,6]. In turn, mineralizing microbes decompose organic N into NH4+, most of which will be reused by organisms [7], while nitrifying microbes oxidize NH4+ into NO2- and then NO3-, often a preferable N form for plants [8,9]. Denitrifying microbes reduce NO3- into NO, N2O and N2, returning N to the atmosphere and completing the entire N-cycling process [10,11]. As anthropogenic activities intensify, these microbe-mediated N-cycling processes are being affected by various environmental changes, often leading to undesirable consequences [1215]. For example, N fertilization/ deposition stimulates the production of excess NO3- by nitrifying microbes. This excess NO3- can be easily lost from soil by leaching, resulting in pollution of groundwater and eutrophication of lakes, estuaries, and coastal oceans [12,14]. Therefore, the influence of various environmental changes on each type of Ncycling functional group has been widely investigated during the past several decades [1619]. However, any given ecosystem can be disturbed by many kinds of environmental changes at the same time [8,12,20] and different environmental changes (and their concurrence) might have different influences on a given N-cycling functional group. F (...truncated)


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Ximei Zhang, Wei Liu, Michael Schloter, Guangming Zhang, Quansheng Chen, Jianhui Huang, Linghao Li, James J. Elser, Xingguo Han. Response of the Abundance of Key Soil Microbial Nitrogen-Cycling Genes to Multi-Factorial Global Changes, PLOS ONE, 2013, 10, DOI: 10.1371/journal.pone.0076500