Ecological clusters based on responses of soil microbial phylotypes to precipitation explain ecosystem functions
Graphical abstract
We constructed a 3-year experiment with nine levels of artificial precipitation (100–500 mm) in a typical semi-arid steppe. Ecological clusters based on the relationships between the relative abundance of phylotypes and dry and wet gradients were correlated with soil C or N mineralization rates; these ecological clusters explained 15–24% of the total variance in soil C and N mineralization rates. In contrast, soil C or N mineralization rates were not correlated with the commonly measured properties (e.g., biomass and diversity) of plant, soil bacterial, and soil fungal communities. Our findings indicate that the grouping of soil microorganisms into ecological clusters based on responses to precipitation gradients can provide insights into the relationships between soil organisms and ecosystem functions.
Introduction
In many terrestrial biomes, precipitation is the primary constraint of soil C and nutrient cycling and other ecosystem functions (Knapp and Smith, 2001; Bell et al., 2014; Liu et al., 2016). This is especially true for semi-arid ecosystems, which cover 17.7% of Earth's terrestrial surface (Ahlström et al., 2015). However, the responses of these ecosystems to shifts in precipitation regimes are difficult to predict because climate models suggest that most semi-arid regions will experience highly variable precipitation patterns and frequent extreme precipitation and drought events (Savo et al., 2016). It is well documented that alterations in precipitation may greatly affect aboveground net primary productivity (ANPP), plant diversity, and ecosystem C and N cycling in semi-arid regions (Knapp and Smith, 2001; Huxman et al., 2004). Furthermore, soils harbor highly diverse microbial communities that are crucial for regulating multiple ecosystem processes (Delgado-Baquerizo et al., 2018; Glassman et al., 2018; Saleem et al., 2019). Although past studied have increased our understanding of how alterations in precipitation affect soil microbial communities and thereby affect ecosystem processes (Bell et al., 2014; Zhou et al., 2018; Chen et al., 2019a), these past studies have seldom investigated the effects of precipitation on ecosystem processes based on ecological clusters (ECs) of soil microbial phylotypes (Singh et al., 2010; Fierer et al., 2012). The ECs have recently been used to reveal how environmental conditions influence the ecological properties of soil microorganisms (Philippot et al., 2010; Evans and Wallenstein, 2014; Delgado-Baquerizo et al., 2018). It may therefore be useful to determine whether assessment of ECs can increase our understanding of the responses of soil microbial communities to climate change and to the relationships between soil microbial communities and ecosystem processes (Fierer et al., 2007; Delgado-Baquerizo et al., 2018).
The responses of soil microbial communities to precipitation change remain highly uncertain. Several studies have shown that increased or decreased precipitation does not affect soil microbial communities (Angel et al., 2010; Santonja et al., 2017), but other studies indicate that soil microbial composition and structure are responsive to altered precipitation (Castro et al., 2010; Hawkes et al., 2011; De Vries et al., 2018). There are several reasons for this inconsistency. First, the response of soil microbial communities to environmental changes may be over- or underestimated depending on which method is used to assess the microbial communities (Lok, 2015; Delgado-Baquerizo et al., 2018). Second, understanding soil microbial responses to precipitation change is often difficult, in part because the effects of precipitation change on the microbial taxa can be taxon-specific and difficult to interpret when microorganisms are assessed only at the community level (Fierer et al., 2007; Singh et al., 2010; Lennon and Jones, 2011). Third, most previous research concerning the effects of precipitation on soil microbial communities has been conducted at a regional or continental scale along precipitation gradients (e.g., Angel et al., 2010; Hawkes et al., 2011; Maestre et al., 2015), which makes it difficult to tease apart the direct effect of precipitation from other coupled environmental variables. Fourth, most previous precipitation manipulation experiments have included only a few levels of precipitation; manipulation experiments that include multiple levels of precipitation (i.e., gradients) are needed to discern the effects of precipitation on soil biodiversity and ecosystem functioning (Kreyling et al., 2018).
The ecological responses to alteration in precipitation can be “symmetrical” (with similar responses to the precipitation gradient under drier and wetter conditions) or “asymmetrical” (with different responses to the precipitation gradient under drier and wetter conditions) (Kreyling et al., 2018; Zhou et al., 2018). Observational studies or manipulation experiments have indicated that the ANPP in semi-arid grasslands is more sensitive to increases in precipitation in wet years than dry years (Knapp and Smith, 2001) or under wet treatments than dry treatments (Wilcox et al., 2017), i.e., the responses are asymmetrical. Another study found an asymmetrical response, i.e., soil respiration was more sensitive to increases in precipitation at wet sites than at dry sites (Liu et al., 2016). Although ecologists have proposed that the sensitivities of ecosystem functions to changes in precipitation may be quite different under dry vs. wet conditions, whether the responses of soil microbial communities to precipitation are symmetrical or asymmetrical under dry vs. wet conditions has seldom been assessed (Castro et al., 2010; Zhou et al., 2018). Limited reports showed that the responses of soil microbial composition to altered precipitation are asymmetrical (Hawkes et al., 2011; Zhou et al., 2018). These asymmetrical changes in the compositions of soil fungal and bacterial communities may have strong effects on ecosystem functions (e.g., C and N cycling) (Fierer, 2017).
Understanding the ecological attributes of microbial phylotypes by identifying ECs could increase our ability to predict how soil processes will respond to precipitation change (Singh et al., 2010; Evans and Wallenstein, 2014; Delgado-Baquerizo et al., 2018). Bacterial taxa were divided into three life strategies after a dry-rewetting experiment (Evans and Wallenstein, 2014), and the possibility of predicting bacterial distribution at a global scale was verified by associating soil environment characteristics with bacterial taxa and by grouping these taxa into ECs (Fierer et al., 2007; Fierer et al., 2012; Delgado-Baquerizo et al., 2018). The identification of ECs was recently proposed as a way to more tightly link microbial communities to ecosystem functions (Fierer et al., 2007; Delgado-Baquerizo et al., 2018). The consideration of such ECs can increase our understanding of the relationships of microorganisms with soil and plant attributes (Fierer et al., 2007; Singh et al., 2010). The linking of microbial ECs to important soil functions such as soil C and N mineralization could be especially useful because microbial communities associated with soil mineralization are variable (Barnard et al., 2015; Chen et al., 2019a). Moreover, some studies that have linked microbial communities with soil mineralization suggest that only a subset of microbial taxa are correlated with or respond to substrate mineralization (Philippot et al., 2013; Banerjee et al., 2018), which once again suggests that the identification of soil microbial ECs could be useful for understanding the effects of soil microorganisms on soil ecosystem functions.
Here, we determined how soil bacterial and fungal communities responded to increases in precipitation under dry conditions (≤300 mm of precipitation per growing season) and wet conditions (≥300 mm of precipitation per growing season) and whether the responses are associated with ecosystem functions in a typical semi-arid steppe. We attempted to answer three questions: 1) How do the composition and structure of soil bacterial and fungal communities at different taxa levels respond to increases in precipitation under dry and wet conditions? 2) How is soil microbial community composition related to plant community composition under dry and wet conditions? and 3) If soil microorganisms are assigned to ECs based on their responses to increasing levels of precipitation under dry vs. wet conditions, are the clusters related to ecosystem functions (i.e., C or N mineralization rates)?
Section snippets
Study site and experimental design
A precipitation manipulation experiment was initiated at the Inner Mongolian Grassland Ecosystem Research Station (IMGERS, 43°38′N, 116°42′E, 1200 m a.s.l) in 2013. The station is located in a region with a typical semi-arid continental climate; over the last 40 years in the region, the mean annual precipitation (MAP) has been 334 mm, and the mean annual temperature (MAT) has been 0.9 °C. Data collected during the growing season at the IMGERS for a recent 31-year period (1982–2013) indicated
Effects of dry and wet gradients on the diversity of the soil microbial community
After extremely rare OTUs were filtered, the data set included 1565 bacterial and 774 fungal OTUs. The soil bacterial communities were dominated by the phyla Actinobacteria, Acidobacteria, Proteobacteria, Chloroflexi, and Bacteroidetes (Table S2). The soil fungal communities were dominated by the classes Sordariomycetes, Agaricomycetes, Dothideomycetes, and Eurotiomycetes (Table S2). The alpha diversity (indicated by the Shannon-Wiener index) of the soil bacterial community decreased as
Effects of simulated precipitation on the alpha diversity of soil microbial communities
Previous reports have documented that the effects of simulated precipitation on ANPP, net ecosystem exchange, and soil respiration were “asymmetrical” in that the effects differed under wet conditions vs. dry conditions; more specifically, the effects were greater under wet than dry conditions (Liu et al., 2016; Wilcox et al., 2017). The effects of simulated precipitation on soil bacterial and fungal communities, however, have not been previously compared under wet and dry conditions in a
Acknowledgements
We thank Huasong Chen for his help in soil analysis. We also thank editor and two anonymous reviewers for their valuable comments on the earlier version of this paper. This study was supported by the Chinese National Key Development Program for Basic Research (2016YFC0500804), the National Natural Science Foundation of China (31570450 and 31630010), and the Youth Innovation Promotion Association of the Chinese Academy of Sciences (2015061).
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