Diversity patterns of the rhizosphere and bulk soil microbial communities along an altitudinal gradient in an alpine ecosystem of the eastern Tibetan Plateau
Graphical abstract
Introduction
Alpine ecosystems represent one of the most important components of the terrestrial system and provide many ecological services (Li et al., 2018). Climate, vegetation and soil properties in alpine ecosystems vary greatly over short spatial distances and altitudinal gradients (McCain, 2010). These changes will strongly affect the structures and functions of soil microbial communities (Shen et al., 2013; Lin et al., 2015). For example, geographic distance, soil pH, the carbon:nitrogen (C:N) ratio and vegetation type have been generally reported as the key drivers of the distributional patterns of soil microbes (Chen et al., 2017b; Li et al., 2018). Soil microorganisms play important roles in regulating biogeochemical cycles and maintaining ecosystem functions (Chen et al., 2017b). Also, soil microorganisms are more sensitive than plants and animals to environmental change (Shen et al., 2015). A better understanding of the patterns of geographic distribution and drivers of community assembly along environmental gradients of alpine ecosystems is therefore important for elucidating microbial processes, and for improving our predictions of the functions of alpine ecosystem in a changing climate.
The rhizosphere, as a focus of microbial activity, plays an important role in microbial assembly because microbial-plant interactions and genetic exchanges are frequent there (Tkacz et al., 2015; Cui et al., 2018; Duan et al., 2018). Bacterial diversity is generally lower in the rhizosphere than the bulk soil (Marilley and Aragno, 1999), and microbial-community compositions differ greatly due to the strongly selective environment of rhizospheres (Kielak et al., 2010; Ai et al., 2012). Bulk soil has relatively oligotrophic conditions, with low rates of nutrient transformation and microbial activity, unlike the more active rhizosphere environment (Ai et al., 2012). Most studies of microbial communities in the alpine ecosystems, however, have focused on bulk soil (Shen et al., 2013; Chen et al., 2017b; Li et al., 2018). Microbial communities in alpine ecosystems have more stable habitats than communities in agricultural ecosystems with more annually variable conditions (Ai et al., 2012; Tkacz et al., 2015). These differences in physicochemical and biological properties suggest distinct differences in microbial communities between rhizosphere and bulk soil, and the responses of microbial communities to the rhizosphere conditions in alpine ecosystems may differ greatly from the responses in other ecosystems. The distributional patterns and drivers of microbial communities may consequently differ between rhizosphere and bulk soil in alpine ecosystems.
In addition to the influences of external conditions on microbial communities, the distinct responses of microbial taxa (bacteria, archaea and fungi) to environmental factors would lead to the variation of patterns of geographic distribution and differences in the drivers of community assembly (Zhang et al., 2017). Mounting evidences suggest that soil pH is a key regulator shaping the structures of bacterial and archaeal communities (J.T. Wang et al., 2015; Hu et al., 2016), but that plant diversity determines the structures of soil fungal communities over broad geographic scales (Chen et al., 2017a). Fungal diversity and richness decrease as altitude increases in alpine ecosystems such as the Tibetan Plateau (Margesin et al., 2009). These studies indicated that bacteria, archaea and fungi responded differently to environmental conditions. All these studies notably focused on a complete or large-scale altitudinal gradient, with relatively large elevational intervals and different vegetation types (Shen et al., 2013; Chen et al., 2017b; Li et al., 2018). The scale over which biodiversity is sampled will strongly influence the patterns observed (Green and Bohannan, 2006), so the effects of environmental factors on structuring microbial communities in a consistent ecosystem within a small-scale altitudinal gradient remain poorly known.
Metabolic characteristics differ greatly between bacteria and archaea, and both bacteria and archaea are very abundant and functionally important in terrestrial ecosystems. For example, ammonia-oxidizing archaea have unique mechanisms for nitrification, better adaptation to low-pH pressures, and strikingly lower ammonia requirements compared with ammonia-oxidizing bacteria (He et al., 2012; Hu et al., 2013). Fungal breakdown of plant materials rich in lignin and cellulose (i.e. lignocellulose) is centrally important to the cycling of terrestrial C due to the abundance of lignocellulose in above- and belowground systems (Meier et al., 2010). These differences in metabolic processes among bacteria, archaea and fungi and their important ecological functions (Nemergut et al., 2010; Meier et al., 2010), indicate that further understanding of the responses of bacterial, archaeal and fungal taxa to environmental conditions in small-scale altitudinal gradients with the same vegetation type is necessary for accurately assessing the altitudinal patterns of distribution and drivers of community assembly in alpine ecosystems and can improve the resolution and precision of our knowledge.
Mount Gongga is the highest mountain on the eastern boundary of the Tibetan Plateau. It has steep slopes, distinct vegetation and relatively low environmental temperature (He and Tang, 2008). We previously reported that the soil of this area has abundant organic matter and sources of available N and phosphorus (P), with a C:N:P ratio of 556:22:1 for the O horizon (Bing et al., 2016), which provide abundant energy and nutrients for the local microorganisms and plants. These conditions provide a natural platform for identifying geographic distributional patterns and drivers of community assembly along an altitudinal gradient. These conditions are also helpful for assessing potential microbial responses to climate change, with a strategy of space-for-time substitution. We investigated the altitudinal distributional patterns and driving factors of the bacterial, archaeal and fungal communities in the rhizosphere and bulk soil along an altitudinal gradient from 2800 to 3500 m a.s.l. containing the same vegetation type (Abies fabri Mast.) on Mount Gongga. We hypothesized that: (1) the pattern of microbial-community diversity would not vary significantly along the small-scale altitudinal gradient in an A. fabri community due to the small spatial scale and consistent vegetation, (2) the microbial communities would not distinctly vary between the rhizosphere and bulk soil because of the low environmental temperature and sufficient resources in the alpine ecosystems, and (3) the driving factors of the bacterial, archaeal and fungal taxa would differ due to the differences in their metabolic processes, even within a short distance.
Section snippets
Study area and soil sampling
The study area was in the Hailuogou catchment of Mount Gongga (29°30′–30°20′N, 101°30′–102°15′E; 2800–3500 m a.s.l.) (Fig. 1). The mountain is in the transition zone of the Tibetan Plateau frigid zone and the warm-humid subtropical monsoon zone and is the highest mountain in the Hengduan Mountains. The climate in the area is mainly controlled by the Asian monsoon. Mean annual temperature and precipitation are 4.2 °C and 1947 mm, respectively (Wu et al., 2013). The soil has mainly developed from
Soil characteristics along the altitudinal gradient
Most soil parameters differed significantly between the rhizosphere and bulk soil along the altitudinal gradient (Tables S2 and S3). The two-way ANOVAs indicated that the SOC, DOC and NH4+-N contents, the C:P and N:P ratios and soil temperature were significantly higher at 2800 and 3000 m than at 3200 and 3500 m (P < 0.05). The NO3−-N, NH4+-N and TP contents and the C:N and C:P ratios were strongly affected by both altitude and location and their interaction (P < 0.05). The Pearson correlation
Differences in microbial alpha diversity and community structure along the altitudinal gradient
Our results indicated that the alpha diversities and community structures of the soil microbes on Mount Gongga varied markedly along an altitudinal gradient containing the same type of vegetation, which did not support our first hypothesis. The soil properties and spatial attributes associated with altitude greatly affected the composition of the belowground communities. Other studies have also reported variations of microbial communities along altitudinal gradients (Yang et al., 2014; Guo et
Conclusions
This study provides insights into the distributional patterns and drivers of microbial communities in rhizosphere and bulk soil along an altitudinal gradient containing the same vegetation type and improves our understanding of microbial ecology in alpine ecosystems. We found significant differences in microbial alpha diversity and microbial-community structure along the gradient but not between the rhizosphere and bulk soil. Environmental factors (explaining 14.6–44% of the variance) and
Acknowledgements
This work was financially supported by the National Natural Science Foundation of China (41571314 and 41630751), CAS “Light of West China” Program (XAB2016A03) and State Key Research & Development Plan Project (2017YFC0504504).
References (53)
- et al.
Responses of extracellular enzyme activities and microbial community in both the rhizosphere and bulk soil to long-term fertilization practices in a fluvo-aquic soil
Geoderma
(2012) - et al.
Plant diversity represents the prevalent determinant of soil fungal community structure across temperate grasslands in Northern China
Soil Biol. Biochem.
(2017) - et al.
Ecoenzymatic stoichiometry and microbial nutrient limitation in rhizosphere soil in the arid area of the northern Loess Plateau, China
Soil Biol. Biochem.
(2018) - et al.
Reveal the response of enzyme activities to heavy metals through in situ zymography
Ecotoxicol. Environ. Saf.
(2018) - et al.
Detection of arbuscular mycorrhizal fungal spores in the air across different biomes and ecoregions
Fungal Ecol.
(2014) - et al.
Spatial scaling of microbial biodiversity
Trends Ecol. Evol.
(2006) - et al.
Fungal endophyte and tall fescue cultivar interact to differentially affect bulk and rhizosphere soil processes governing C and N cycling
Soil Biol. Biochem.
(2016) - et al.
Soil development along primary succession sequences on moraines of Hailuogou Glacier, Gongga Mountain, Sichuan, China
Catena
(2008) - et al.
Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils
Soil Biol. Biochem.
(2012) - et al.
Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil
Soil Biol. Biochem.
(2006)
Bacterial community structure and function change in association with colonizer plants during early primary succession in a glacier forefield
Soil Biol. Biochem.
Soil properties and tree species drive β-diversity of soil bacterial communities
Soil Biol. Biochem.
Phylogenetic diversity of bacterial communities differing in degree of proximity of Lolium perenne and Trifolium repens roots
Appl. Soil Ecol.
Fungal growth on a common wood substrate across a tropical elevation gradient: temperature sensitivity, community composition, and potential for above-ground decomposition
Soil Biol. Biochem.
Plot-scale manipulations of organic matter inputs to soils correlate with shifts in microbial community composition in a lowland tropical rain forest
Soil Biol. Biochem.
Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain
Soil Biol. Biochem.
Soil bacterial and fungal diversity differently correlated with soil biochemistry in alpine grassland ecosystems in response to environmental changes
Sci. Rep.
Stoichiometric variation of carbon, nitrogen, and phosphorus in soils and its implication for nutrient limitation in alpine ecosystem of Eastern Tibetan Plateau
J. Soils Sediments
A consideration of the relative contributions of different microbial subpopulations to the soil N cycle
Front. Microbiol.
Nitrogen-total
Microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity
Proc. Natl. Acad. Sci. U. S. A.
Distinct microbial communities in the active and permafrost layers on the Tibetan Plateau
Mol. Ecol.
Fungal symbionts. Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism
Science
ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts
Mol. Ecol.
Diversity and distribution of autotrophic microbial community along environmental gradients in grassland soils on the Tibetan Plateau
Appl. Microbiol. Biotechnol.
Signaling in the arbuscular mycorrhizal symbiosis
Annu. Rev. Microbiol.
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These authors contributed equally to this work.