Elsevier

Geoderma

Volume 285, 1 January 2017, Pages 19-26
Geoderma

Impact of elevated atmospheric CO2 on soil bacteria community in a grazed pasture after 12-year enrichment

https://doi.org/10.1016/j.geoderma.2016.09.015Get rights and content

Highlights

  • Quantitative PCR and pyrosequencing were used to assess soil bacterial communities.

  • Elevated CO2 (eCO2) led to differential responses of soil bacterial taxa.

  • The overall structures of soil bacteria communities remained largely unchanged.

  • The most notable difference was a 50% increase in phylum Planctomycetes at eCO2.

Abstract

This study was designed to compare soil bacterial communities under ambient (aCO2) and elevated (eCO2) carbon dioxide after 12 years of enrichment using Free Air Carbon Dioxide Enrichment (FACE) in a grazed grassland. Grazing animals can have profound effects on nutrient cycling through the return of nutrient in excreta and by their influence on plant community composition through diet selection. The abundance and composition of bacterial communities were evaluated by real-time quantitative Polymerase Chain Reaction (qPCR) and pyrosequencing based on the analysis of bacterial 16S rRNA genes. The results showed the overall bacterial community structure was not altered by the eCO2 treatment despite the substantial changes in soil functions, pools and fluxes under eCO2 documented at this site in previous studies. The dominant phyla in both treatments were Actinobacteria, Proteobacteria, Firmicutes, Actinobacteria, Bacteroidetes and Planctomycetes, accounting for 87% of the total microbial 16S rRNA sequence reads. At the phylum level, Planctomycetes and Bacteria incertae sedis increased and BRC, Cyanobateria and TM7 decreased significantly at eCO2. Most changes were observed at lower taxonomic levels where the abundance of 30 of the 200 most abundant OTUs were responsive to eCO2 however these changes were not sufficient to differentiate the overall communities. It remains uncertain whether these changes in the lower order taxa could be responsible for the observed changes in soil properties. These first data for a grazed ecosystem are broadly consistent with those from a range of other ecosystems where CO2 effects are confined to relatively few taxa.

Introduction

The CO2 concentration in the atmosphere has increased by over 30% since the industrial revolution due to anthropogenic interference and is predicted to reach 500 ppm by 2050 (Collins et al., 2013). Elevated CO2 (eCO2) not only leads to climate change but also has a direct impact on biological systems. While there is a consensus that eCO2 has a generally stimulatory effect on plant growth and primary productivity (Ainsworth and Long, 2005, Lukac et al., 2009, Luo et al., 2006, Rogers et al., 1994) there are varied reports of the effects of eCO2 on belowground microbial communities (Austin et al., 2009, Carney et al., 2007, Gruber and Galloway, 2008, Lesaulnier et al., 2008). For example, studies have reported that soil bacterial diversity increases (Janus et al., 2005, Jossi et al., 2006, Lesaulnier et al., 2008, Sonneman and Wolters, 2005, Liu et al., 2014, Lee et al., 2015), decreases (He et al., 2012, Chen et al., 2014) or remains unchanged (Austin et al., 2009, Ebersberger et al., 2004, Ge et al., 2010, Grüter et al., 2006, Lipson et al., 2006) under eCO2. This variation may reflect genuine differences among ecosystems or, perhaps, differences in methodology (He et al., 2012).

Recent studies in long-term Free Air Carbon Dioxide Enrichment (FACE) experiments have found changes in microbial communities in a sown biodiversity experiment (Deng et al., 2012, He et al., 2010, He et al., 2014) but few changes after 10 years of eCO2 in a grass/clover pasture (Staddon et al., 2014) or after 11 years enrichment of an aspen plantation (Dunbar et al., 2014). An omission in research on soil microbial responses to eCO2 is any data from grazed grasslands. This is a land use that covers 37% of the land surface, makes a major contribution to food production (O'Mara, 2012), is a potential source/sink for carbon (C) (McSherry and Ritchie, 2013), a source of emissions of nitrous oxide (N2O) (Oenema et al., 2005) and both a sink (in the soil) and source (from ruminants) of methane. The impacts of eCO2 on grazed grassland are thus of considerable importance. In this paper we present data on soil microbial communities gathered from the New Zealand FACE (NZ-FACE) experiment which is the only FACE experiment to consider eCO2 effects on grazed grassland (Newton et al., 2006, Newton et al., 2014).

Grazed pastures have characteristics that distinguish them from other ecosystems; in particular, nutrients are re-cycled through the animals and the return of these nutrients in dung and urine results in marked heterogeneity in nutrient availability; in addition, animals may prefer some plant species over other and this selection can result in changes in botanical composition. Both of these processes are likely to influence bacterial communities (Anderson et al., 2011, Garbeva et al., 2006, Thomson et al., 2010) and be influenced by eCO2 (Newton et al., 2001). In the NZ-FACE, Ross et al. (2013) have found significantly greater pools of soil C and N after 10-years continuous exposure to eCO2 and Rütting et al. (2010) have identified altered N transformations in the soil suggesting changes in microbial activity were occurring.

One g of soil contains an estimated 4 × 107 to 2 × 109 prokaryotic cells (Daniel, 2005) and our ability to culture these bacteria is generally considered to be poor (Curtis et al., 2002, Rappé and Giovannoni, 2003, Schloss and Handelsman, 2004, Zinder and Salyers, 2001). However, recent development of high-throughput sequencing technology has markedly advanced our ability to characterize soil microbial communities (Petrosino et al., 2009, Xia and Jia, 2014). Studies using this new technique have demonstrated how land use (Acosta-Martínez et al., 2008, Nacke et al., 2011), soil management history (Sugiyama et al., 2010), geography (Chu et al., 2010) and environment (Lauber et al., 2009, Yu et al., 2012) can lead to shift in microbial communities. In this study we use pyrosequencing-based soil metagenomics analysis of bacterial 16S rRNA gene to investigate soil microbial communities in the NZ-FACE experiment and provide the first data on the response of grazed grassland to long-term eCO2.

Section snippets

NZ-FACE experiment

The NZ-FACE experiment is on a pasture grazed by sheep on the west coast of the North Island of New Zealand (40°14′S, 175°16′E). The pasture contains about 25 species of C3 and C4 grasses, forbs and legumes. The experimental design pairs ambient CO2 (aCO2) and eCO2 rings into three blocks; each ring is 12 m in diameter and is fenced to contain sheep during the grazing periods. Enrichment, to 475 ppm, started in October 1997 and is continuous during the photoperiod. Until 2012 the rings were

Absolute abundance

The copy number of soil bacterial 16S rRNA genes ranged from 0.86 × 108 to 1.73 × 108 copies g 1 dry soil weight. The abundance of bacteria in eCO2 was lower than that in aCO2 but the difference was not statistically significant (P = 0.17).

Community diversity

After removing low quality sequences generated from pyrosequencing, a total of 17,912 high quality sequences were obtained with an average sequence number of 2985 sequences per sample (Table 1). The average read length was about 389 bp. Of these sequences, > 88% could

Discussion

These are the first published data on soil bacterial communities under eCO2 in a grazed grassland. Our findings that the absolute abundance of bacteria identified by qPCR, and microbial relative abundance, diversity and overall community structure identified through pyrosequencing were not changed by eCO2, are consistent with results from other ecosystems such as soybean (Pereira et al., 2013) and aspen stands (Dunbar et al., 2014). We observed few changes due to eCO2 at higher bacterial

Acknowledgment

The study was funded by the Startup Foundation for Introducing Talent of NUIST (S8113117001); the National Natural Science Foundation of China (41501267); the Livestock Emission and Abatement Network (LEARN) Fellowship Programme; the New Zealand Ministry of Business, Innovation and Employment (C10X0713); the NZ-China Scientist Exchange Program and the Ministry of Science and Technology of China (2010DFA22770). We are grateful to Dr. Siva Ganesh of AgResearch for the multivariate statistical

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