Climatic factors have unexpectedly strong impacts on soil bacterial β-diversity in 12 forest ecosystems
Introduction
Unravelling the pattern of community assembly and its underlying mechanisms is important for a better understanding of biodiversity maintenance, community stability and ecosystem functioning (Hooper et al., 2002; Nemergut et al., 2013). Deterministic (niche-based) and stochastic (neutral) processes are regarded as two main forces in shaping community assembly and have been widely applied to interpret the community assembly processes of macro-organisms (Kraft et al., 2008; Ellwood et al., 2009). The niche-based theory states that deterministic factors, including environmental variables, biotic interactions and species traits, modulate the local microbial community. In this scenario, a community should be convergent towards a single pattern under similar environmental conditions and divergent under different environmental conditions (Zhou et al., 2013). The neutral theory, by contrast, assumes that many natural community patterns can be generated by ecological drift, which leads to dispersal-assembled communities mainly or solely due to dispersal (immigration) rather than adaptation to habitats (Hubbell, 2001; Alonso et al., 2006).
Soil bacteria rank among the most abundant and diverse groups of organisms on Earth and play key roles in biogeochemical cycling and ecosystem functioning. Despite the fact that bacterial cells have small sizes and short generation times, researchers are beginning to evaluate the relative importance of determinism and neutrality in structuring bacterial community assembly (i.e., Powell et al., 2015) with the help of molecular techniques to unravel their vast diversity. Previous studies have shown that the relative role of deterministic and stochastic processes in the assembly of soil bacterial communities is highly dependent on spatial scale (Caruso et al., 2011). For example, determinism plays a dominant role at a relatively larger geographic scale, whereas stochasticity dominates at a smaller scale. The study of Powell et al. (2015), which is based on the scale of Scotland, reported that soil bacterial communities were predominantly impacted by deterministic processes under reduced land-use intensity, such as semi-natural grasslands, woodlands, moors and bogs. However, the relative importance of determinism and stochasticity in shaping soil bacterial diversity along a much larger latitudinal gradient in natural forest ecosystems remains less understood.
Characterizing bacterial α-diversity (e.g., richness and/or phylogenetic diversity) and β-diversity (i.e., community composition/variation) is fundamental to understanding ecological functioning and the underlying mechanisms that generate, drive and maintain bacterial biodiversity in ecosystems (Legendre and De Cáceres, 2013; Reese et al., 2018). At a large scale, although the pattern of decreasing “macrobial” diversity from the tropics to the poles (i.e., latitudinal diversity gradient, LDG) has been documented for > 200 years (Amend et al., 2010; Kinlock et al., 2018), it remains less understood whether microbes exhibit a similar LDG (Fierer and Jackson, 2006; Zhou et al., 2016). Previous studies reported that microbial diversity patterns showed unimodal (Shi et al., 2014), monotonically decreasing (Fuhrman et al., 2008; Tedersoo et al., 2014), or nonlinear third-order polynomial (Tedersoo et al., 2014; Wang et al., 2016b) patterns with increasing latitude. No broad consensus is achieved for a microbial LDG pattern, and there is an urgent need to characterize the key drivers of microbial community across a large scale.
Previous studies have elucidated the distribution patterns of soil bacteria at large geographic scales but generated inconsistent results. For instance, across a broad range, some studies found that the soil bacterial β-diversity was significantly impacted by spatial variables (Martiny et al., 2011), soil pH and organic matter (Fierer and Jackson, 2006; Tian et al., 2018), whereas other studies reported that salinity and plant community composition were crucial environmental determinants of the bacterial community composition (Lozupone and Knight, 2007; Wang et al., 2016b; Reese et al., 2018). More importantly, the mean annual precipitation and temperature, rather than soil pH, have been recognized as the strongest predictors of microbial diversity and composition at the global (Tedersoo et al., 2014) and continental (Zhou et al., 2016) scales. Overall, bacterial diversity and/or community composition are influenced by different environmental factors, depending on ecosystem differences and spatial scales. Therefore, to elucidate the determinants that dominate bacterial community β-diversity, we need more empirical evidence from ecosystems that are less impacted by anthropogenic disturbances, such as natural and undisturbed forests. This knowledge can help us to better identify and compare the relative roles of neutral and niche processes in structuring soil bacterial community under the consistent ecosystem-type.
In this study, we examined the soil bacterial community in 12 undisturbed forests across a broad-scale latitudinal range in China (>4000 km, covering a latitude of 21.6°–50.8° N), using Illumina high-throughput sequencing. Unlike the available findings about microbial latitudinal diversity (e.g., Wang et al., 2016b; Tian et al., 2018), we first employed a neutral model approach to generate neutral predictions. The predicted community was subsequently analysed and compared to the observed β-diversity to achieve three possible outcomes: the observed β-diversity equals the neutral prediction or is greater (divergence) or smaller (convergence) than the neutral prediction. We aimed to reveal the soil bacterial LDG pattern and to decipher the relationships between the bacterial community diversity and the habitat turnover based on soil, plant and climatic properties. The key factors influencing the bacterial community assembly patterns were identified through multivariate statistical analysis. We hypothesized that: (H1) a clear deterministic pattern would be observed for the bacterial community assembly processes; (H2) the bacterial LDG pattern would be different from that of macro-organisms; (H3) in addition to soil pH, annual temperature and/or annual precipitation which represent the typical climatic characteristics across large spatial scales, will strongly shape the bacterial diversity.
Section snippets
Study sites and soil collection
This study was conducted in 12 permanent forest sites established by the Chinese Forest Biodiversity Monitoring Network (CForBio), ranging from the latitude of 21.6°N to 50.8°N in China (Supplementary Fig. S1). As shown in Fig. S1, the forest types included two tropical (seasonal) rain forests (XSBN and NG), four subtropical evergreen broad-leaf forests (DHS, HSD, GTS, and BDGS), one mixed evergreen broad-leaved and deciduous broad-leaved forest (TTS), two warm-temperate deciduous broad-leaved
High-throughput sequencing analysis
After quality control, we obtained a total of 11,975,634 quality filtered 16S rRNA gene sequences, which were clustered into 10,108 bacterial OTUs. After normalization, we obtained 9262 bacterial OTUs (1,455,840 reads), which were distributed in 43 phyla, 128 classes, and 182 orders. The dominant bacterial phyla were Proteobacteria (34.2%), Acidobacteria (27.8%), Verrucomicrobia (9.6%), Actinobacteria (9.3%), Bacteroidetes (5.1%), Planctomycetes (4.4%), Crenarchaeota (2.6%), and Chloroflexi
Divergence dominated bacterial community assembly
Previous studies documented that the assembly of bacterial communities depends largely on deterministic process (niche-based) driven by contemporary environmental characteristics, such as soil pH, temperature, salinity, and nutrients (Fierer and Jackson, 2006; Lozupone and Knight, 2007; Wang et al., 2016a). Meanwhile, the bacterial communities could also be driven by stochastic processes, such as geographical separation and dispersal limitation (Wang et al., 2013). However, the relative
Conclusions
A divergent pattern was found for soil bacterial community composition through a neutral model simulation approach. Our results demonstrated that deterministic processes influenced the outcome of bacterial community assembly via environmental variations along a large-scale latitudinal gradient. Previous studies in a variety of habitats have reported that soil pH, salinity and carbon content impacted the bacterial community (Fierer and Jackson, 2006; Lozupone and Knight, 2007; Delgado-Baquerizo
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We are grateful to staff of the CForBio for soil sample collection. We thank Ke-Ping Ma, Xiao-Jun Du, Wei-Guo Sang, Zhan-Qing Hao, Ming-Xi Jiang, Wan-Hui Ye, Min Cao, Xian-Kun Li, Guang-Ze Jin, Xiao-Yong Chen, and Bu-Hang Li for providing the plant information. We thank Dr. Liang Chen, Dr. Cheng Gao, and Dr. Jianjun Wang for their valuable suggestions on data analysis and organization of this manuscript. We also thank the editor and two anonymous reviewers whose insightful comments and
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