Little environmental adaptation and high stability of bacterial communities in rhizosphere rather than bulk soils in rice fields

Highlights

• Bacterial communities in the rhizosphere and bulk soils had significant differences.

• Bacterial communities in rhizosphere had higher stability than those in bulk soils.

• Communities in bulk soils were more environmentally constrained than rhizosphere.

• Available potassium was decisive in regulating the bacterial community assemblies.

Abstract

The rhizosphere harbors complex bacterial communities, which are critical for plant growth and health. Significant differences exist between bacterial communities in the rhizosphere and bulk soils, however, limited research has explored co-occurrence patterns, environmental adaptations, and assembly mechanisms of rhizosphere bacterial communities. Using 16S rRNA high-throughput sequencing, we investigated the taxonomic and phylogenetic diversity of bacterial communities in both rhizosphere and bulk soils from a rice cropping experimental system in China. In addition to investigating differences in bacterial composition, we examined co-occurrence patterns, estimated environmental breadth and phylogenetic signals, and analyzed community assembly processes in these environments. Significant differences were observed between rhizosphere composition and bulk soil (p < 0.05) even some bacteria in the rice rhizosphere may come from the bulk soil around roots. The distribution patterns and ecological functions between communities in the rice rhizosphere and bulk soil were also significantly different. Lower β-diversity values among bacterial communities in the rice rhizosphere indicated that they had a higher stability than those in the bulk soils. In addition, rice rhizosphere communities had a wider phylogenetic diversity and lower functional redundancy when compared with bulk soils. Moreover, the results of environmental breadth analysis revealed that communities in bulk soils were more environmentally constrained than rhizosphere communities. Our null model revealed that deterministic processes drove community assembly in bulk soils (59.57%), whereas stochastic processes determined those in the rice rhizosphere (53.85%). Available potassium was decisive in determining the balance between stochasticity and determinism in both communities. Our study provides insights on the mechanisms underlying the assembly and maintenance of bacterial diversity in rice cropping soils, in response to environmental changes.

Introduction

The soil bacterial community, an integral component of agricultural ecosystems, drives critical biogeochemical cycles and maintains soil productivity (Zhou et al., 2019). The relationship between soil communities and crop growth and health has been extensively investigated in recent years (Niu et al., 2017; She et al., 2017). Exudations from crop roots alter the biogeochemistry and communities of surrounding soils, resulting in a unique and complex ecological rhizosphere zone (Turner et al., 2013). Significantly different bacterial community compositions have been identified between rhizosphere and bulk soils in multiple real-agricultural systems (Donn et al., 2015; Fan et al., 2017). Bacterial diversity varies along environmental gradients, and with nutrient availability (D. Shen et al., 2018; Huber et al., 2020). Equally, differences in nutrient uptake and environmental stress adaptations of species also lead to bacterial growth heterogeneity and abundance (Salcher et al., 2013). These factors also can result in an inhomogeneous distribution of bacterial community between rhizosphere and bulk soil in a local agricultural field (Cheng et al., 2019; Qin et al., 2019). Therefore, deciphering these bacterial communities in rhizosphere and bulk soils is vital for our understanding of microbe-driven ecological processes and functions in agricultural ecosystems.

Microbial communities efficiently regulate nutrient-use to manage imbalanced resources (Guo et al., 2018). Previous studies have investigated agricultural soil bacterial communities at relatively high taxonomic levels, e.g. phylum or class, as responses to environmental changes at these levels are easier to predict (Cederlund et al., 2014; Chen et al., 2016; Philippot et al., 2010). However, ecological functions and environmental stress adaptations of species in the same high taxonomic group are not always consistent. Therefore, it is important to investigate bacterial community responses to environmental changes at a higher resolution. Recently, network analyses have explored the co-occurrence patterns of bacterial species in different environments (Berry and Widder, 2014; Ma et al., 2016), thereby deciphering the structures and assemblies of such complex communities (Faust and Raes, 2012). In agricultural ecosystems, Mendes et al. (2014) demonstrated that the rhizosphere community was a subset of the bulk soil community based on co-occurrence networks. In addition, Fan et al. (2018) observed that the wheat rhizosphere harbored a less complex and more stable microbial co-occurrence pattern than bulk soil. Although some valuable findings have been reported, differences in ecological functions and bacterial co-occurrence patterns between rhizosphere and bulk soils have not been fully understood yet.

Disentangling the contribution of different ecological processes towards community assembly is key to microbial ecology (Stegen et al., 2016). Bacterial community assembly is influenced by both selective and non-selective processes, which are governed by two complementary mechanisms; niche- and neutral-based theories (Hubbell, 2001; Bahram et al., 2015). The former asserts that deterministic processes, induced by abiotic (temperature and salinity) and biotic factors (predation and competition), shape bacterial communities (Liu et al., 2015; Wei et al., 2016). In contrast, the latter proposes that bacterial communities are shaped by stochastic processes, such as birth, death, immigration, limited dispersal, and drift (Sloan et al., 2006; Chen et al., 2019). Naturally, environmental factors have important roles in balancing these processes (Jiao and Lu, 2020a), e.g., dissolved oxygen in eutrophic lakes mediate deterministic and stochastic governance in bacterioplankton community assembly (Wan et al., 2021). In addition, pH is a main factor influencing the relative importance of these processes across successional soils (Tripathi et al., 2018). Currently, many studies have focused on comparisons of composition and function of bacterial communities between the rhizosphere and bulk soils (Fonseca et al., 2018; Pascual et al., 2018; Yang et al., 2013). However, the assembly dynamics of these communities and their relationships with environmental variables in the rhizosphere and bulk soil of agricultural crops remain unclear.

Here, we used rice field experiments to characterize differences in composition, function, and bacterial community interactions between the rhizosphere and bulk soils. We also determined the ecological processes that shaped community assembly. Our aims were to: (i) decipher bacterial co-occurrence patterns in the rhizosphere and bulk soils; (ii) explore potential relationships between bacterial clustering patterns, community functions, and environmental variables; and (iii) investigate the major environmental variables influencing the assembly process of bacterial communities between the rhizosphere and bulk soils. To achieve these goals, we performed high-throughput sequencing based on 16S rRNA in rhizosphere versus bulk soils in 27 rice fields, in relation to 16 environmental variables. Our findings will enhance our understanding of bacterial community structuring processes in rice systems and improve management strategies for agricultural ecosystems.