Abstract
Anthropogenic nitrogen (N) input is known to alter the soil microbiome, but how N enrichment influences the abundance, alpha-diversity and community structure of N-cycling functional microbial communities in grasslands remains poorly understood. Here, we collected soils from plant communities subjected to up to 9 years of annual N-addition (10 g N m−2 per year using urea as a N-source) and from unfertilized plots (control) in 30 grasslands worldwide spanning a large range of climatic and soil conditions. We focused on three key microbial groups responsible for two essential processes of the global N cycle: N2 fixation (soil diazotrophs) and nitrification (AOA: ammonia-oxidizing archaea and AOB: ammonia-oxidizing bacteria). We targeted soil diazotrophs, AOA and AOB using Illumina MiSeq sequencing and measured the abundance (gene copy numbers) using quantitative PCR. N-addition shifted the structure of the diazotrophic communities, although their alpha-diversity and abundance were not affected. AOA and AOB responded differently to N-addition. The abundance and alpha-diversity of AOB increased, and their community structure shifted with N-addition. In contrast, AOA were not affected by N-addition. AOA abundance outnumbered AOB in control plots under conditions of low N availability, whereas N-addition favoured copiotrophic AOB. Overall, N-addition showed a low impact on soil diazotrophs and AOA while effects for AOB communities were considerable. These results reveal that long-term N-addition has important ecological implications for key microbial groups involved in two critical soil N-cycling processes. Increased AOB abundance and community shifts following N-addition may change soil N-cycling, as larger population sizes may promote higher rates of ammonia oxidation and subsequently increase N loss via gaseous and soil N-leaching. These findings bring us a step closer to predicting the responses and feedbacks of microbial-mediated N-cycling processes to long-term anthropogenic N-addition in grasslands.
| Original language | English |
|---|---|
| Article number | 108887 |
| Journal | Soil Biology and Biochemistry |
| Volume | 176 |
| DOIs | |
| State | Published - Jan 2023 |
Bibliographical note
Publisher Copyright:© 2022 The Authors
Funding
Dominance of AOA relative to AOB in the amoA gene pool, as we found here, has also been reported in grasslands and agricultural environments (He et al., 2007; Gubry-Rangin et al., 2011; Zhou et al., 2014; Sterngren et al., 2015). This could be attributed to a difference in the affinity for ammonia caused by the unique physiological characteristics and preferred habitat conditions of AOA and AOB (Prosser and Nicol, 2012). AOB are typically copiotrophic (Hatzenpichler, 2012) and are most abundant in soils that have a relatively high N content (Sterngren et al., 2015; Trivedi et al., 2019). AOA perform better in habitats with more acidic, organic matter-depleted soil conditions (Banning et al., 2015; Trivedi et al., 2019) which is strongly supported by our findings in some of the grassland soils (e.g. spin.us; sgs.us; kibber.in). AOA also appear to be less constrained by the availability of N substrates and prosper in oligotrophic environments (Martens-Habbena et al., 2009; Trivedi et al., 2019), and our results confirm this pattern. In addition, AOA have lower membrane permeability, smaller cell and genome size, and higher energy efficiency than AOB, which enables AOA to better adapt to and perform their physiological activities in nutrient-limited environments (Prosser and Nicol, 2012; Banning et al., 2015). Burton and Prosser (2001) suggested that AOB in contrast to AOA can produce urease and thus respond directly to urea addition which might be responsible for the stronger response of AOB compared to AOA to N-addition in our study. These and potentially other physiological or metabolic differences between AOA and AOB likely lead to niche differentiation between these two groups (Prosser and Nicol, 2012; Carey et al., 2016; Aigle et al., 2019), and therefore different responses to N-addition. Overall, our results suggest that AOB perform better in nutrient-rich environments than AOA when faced with an increased N input (H2).This work was conducted within the Nutrient Network (http://www.nutnet.org) experiment, which is funded at the site scale by individual researchers. The N-cycling microbial communities add-on study was funded by an internal competitive WSL grant (PSP 5233.00176.001.01) to B.F. and A.C.R. Coordination and data management have been supported by funding from the National Science Foundation Research Coordination Network (NSF-DEB-1042132) to E.T.B. and E.W.S. the Long-Term Ecological Research (LTER) programme (NSF-DEB-1234162), and the Institute on the Environment at the University of Minnesota (DG-0001-13). We also thank the Minnesota Supercomputer Institute for hosting project data, and the Institute on the Environment for hosting NutNet meetings. We are grateful to B. Stierli, S. Baumgartner and A. Dharmarajah for their help with sample processing and analyses. We also thank M. Dawes for her valuable contribution to the editing of this article. This work was conducted within the Nutrient Network ( http://www.nutnet.org ) experiment, which is funded at the site scale by individual researchers. The N-cycling microbial communities add-on study was funded by an internal competitive WSL grant (PSP 5233.00176.001.01) to B.F. and A.C.R. Coordination and data management have been supported by funding from the National Science Foundation Research Coordination Network (NSF-DEB-1042132) to E.T.B. and E.W.S., the Long-Term Ecological Research (LTER) programme (NSF-DEB-1234162), and the Institute on the Environment at the University of Minnesota (DG-0001-13). We also thank the Minnesota Supercomputer Institute for hosting project data, and the Institute on the Environment for hosting NutNet meetings. We are grateful to B. Stierli, S. Baumgartner and A. Dharmarajah for their help with sample processing and analyses. We also thank M. Dawes for her valuable contribution to the editing of this article.
| Funders | Funder number |
|---|---|
| Hawkesbury Institute for the Environment | |
| Long-Term Ecological Research | NSF-DEB-1234162 |
| U.S. Department of Energy Chinese Academy of Sciences Guangzhou Municipal Science and Technology Project Oak Ridge National Laboratory Extreme Science and Engineering Discovery Environment National Science Foundation National Energy Research Scientific Computing Center National Natural Science Foundation of China | 1042132 |
| Minnesota State University-Mankato | DG-0001-13 |
| National Science Foundation Research Coordination Network | NSF-DEB-1042132 |
Keywords
- Ammonia oxidizer
- Biogeography
- Diazotroph
- Grassland
- N-Fertilization
- N-cycling microbial community
- N-fixing bacteria
- Nutrient network (NutNet)
- Urea
- nifH
ASJC Scopus subject areas
- Microbiology
- Soil Science