Impact of elevated atmospheric CO2 on soil bacteria community in a grazed pasture after 12-year enrichment
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
References (92)
- et al.
Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use
Soil Biol. Biochem.
(2008) - et al.
Short and long-term effects of elevated CO2 on Lolium perenne rhizodeposition and its consequences on soil organic matter turnover and plant N yield
Soil Biol. Biochem.
(2006) - et al.
Changes in the fungal-to-bacterial respiratory ratio and microbial biomass in agriculturally managed soils under free-air CO2 enrichment (FACE) —a six-year survey of a field study
Soil Biol. Biochem.
(2011) - et al.
Assessment of 10 years of CO2 fumigation on soil microbial communities and function in a sweetgum plantation
Soil Biol. Biochem.
(2009) - et al.
Surface soil fungal and bacterial communities in aspen stands are resilient to eleven years of elevated CO2 and O3
Soil Biol. Biochem.
(2014) - et al.
Short-term responses of microbial community and functioning to experimental CO2 enrichment and warming in a Chinese paddy field
Soil Biol. Biochem.
(2014) A rapid method for the determination of organic carbon in soil
Anal. Chim. Acta
(1960)- et al.
Plant responses to atmospheric CO2 enrichment with emphasis on roots and the rhizosphere
Environ. Pollut.
(1994) - et al.
Impact of a low level of CO2 enrichment on soil carbon and nitrogen pools and mineralization rates over ten years in a seasonally dry, grazed pasture
Soil Biol. Biochem.
(2013) Enumeration of 16S rDNA of Desulfotomaculum lineage 1 in rice field soil by real-time PCR with SybrGreen™ detection
J. Microbiol. Methods
(2002)
Shifts in microbial community function and structure along the successional gradient of coastal wetlands in Yellow River Estuary
Eur. J. Soil Biol.
What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2
New Phytol.
Increased quantity and quality of coarse soil organic matter fraction at elevated CO2 in a grazed grassland are a consequence of enhanced root growth rate and turnover
Plant Soil
Diversity of Planctomycetes in soil in relation to soil history and environmental heterogeneity
Appl. Environ. Microbiol.
Catenulispora acidiphila gen. Nov., sp. Nov., a novel, mycelium-forming actinomycete, and proposal of Catenulisporaceae fam. Nov.
Int. J. Syst. Evol. Microbiol.
Altered soil microbial community at elevated CO2 leads to loss of soil carbon
Proc. Natl. Acad. Sci. USA.
Non-parametric estimation of the number of classes in a population
Scand. J. Stat.
Responses of soil microbial activity to cadmium pollution and elevated CO2
SCI. REP.-UK
Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes
Environ. Microbiol.
Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine
PLoS One
Long-term climate change: projections, commitments and irreversibility
Soils and agriculture of Flock House, Bulls, Manawatu
Fertiliser Recommendations for Pasture and Crops in New Zealand
Estimating prokaryotic diversity and its limits
Proc. Natl. Acad. Sci. USA
Changes in bacterial denitrifier community abundance over time in an agricultural field and their relationship with denitrification activity
Appl. Environ. Microbiol.
The metagenomics of soil
Nat. Rev. Microbiol.
Elevated carbon dioxide alters the structure of soil microbial communities
Appl. Environ. Microbiol.
Novel bacterial lineages at the (sub)division level as detected by signature nucleotide-targeted recovery of 16S rRNA genes from bulk soil and rice roots of flooded rice microcosms
Appl. Environ. Microbiol.
Common bacterial responses in six ecosystems exposed to 10 years of elevated atmospheric carbon dioxide
Environ. Microbiol.
Effects of long term CO2 enrichment on microbial community structure in calcareous grassland
Plant Soil
Search and clustering orders of magnitude faster than BLAST
Bioinformatics
The influence of sex, handedness, and washing on the diversity of hand surface bacteria
Proc. Natl. Acad. Sci. USA
The Planctomycetes: emerging models for microbial ecology, evolution and cell biology
Microbiology
Effect of above-ground plant species on soil microbial community structure and its impact on suppression of Rhizoctonia solani AG3
Environ. Microbiol.
The spatial factor, rather than elevated CO2, controls the soil bacterial community in a temperate forest ecosystem
Appl. Environ. Microbiol.
An earth-system perspective of the global nitrogen cycle
Nature
Influence of plant diversity and elevated atmospheric carbon dioxide levels on belowground bacterial diversity
BMC Microbiol.
Effects of elevated atmospheric CO2 on microbial community structure at the plant-soil interface of young beech trees (Fagus sylvatica L.) grown at two sites with contrasting climatic conditions
Microb. Ecol.
Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex
Nat. Methods
Changes in the microbial community structure of bacteria, archaea and fungi in response to elevated CO2 and warming in an Australian native grassland soil
Environ. Microbiol.
The phylogenetic composition and structure of soil microbial communities shifts in response to elevated carbon dioxide
ISME. J.
Distinct responses of soil microbial communities to elevated CO2 and O3 in a soybean agro-ecosystem
ISME. J.
Metagenomic analysis reveals a marked divergence in the structure of belowground microbial communities at elevated CO2
Ecol. Lett.
Complete genome sequence of Haliangium ochraceumtype strain (SMP-2T)
Stand. Genomic Sci.
Coordinated surface activities in Variovorax paradoxus EPS
BMC Microbiol.
Elevated atmospheric CO2 alters soil microbial communities associated with trembling aspen (Populus tremuloides) roots
Microb. Ecol.
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