Soil pH mediates the balance between stochastic and deterministic assembly of bacteria

The ISME Journal (2018) 12:1072–1083 https://doi.org/10.1038/s41396-018-0082-4 ARTICLE Soil pH mediates the balance between stochastic and deterministic assembly of bacteria Binu M. Tripathi1 James C. Stegen ● 2 ● Mincheol Kim1 Ke Dong3 Jonathan M. Adams4 Yoo Kyung Lee1 ● ● ● 1234567890();,: Received: 30 March 2017 / Revised: 1 February 2018 / Accepted: 5 February 2018 / Published online: 7 March 2018 © The Author(s) 2018. This article is published with open access Abstract Little is known about the factors affecting the relative influences of stochastic and deterministic processes that govern the assembly of microbial communities in successional soils. Here, we conducted a meta-analysis of bacterial communities using six different successional soil datasets distributed across different regions. Different relationships between pH and successional age across these datasets allowed us to separate the influences of successional age (i.e., time) from soil pH. We found that extreme acidic or alkaline pH conditions lead to assembly of phylogenetically more clustered bacterial communities through deterministic processes, whereas pH conditions close to neutral lead to phylogenetically less clustered bacterial communities with more stochasticity. We suggest that the influence of pH, rather than successional age, is the main driving force in producing trends in phylogenetic assembly of bacteria, and that pH also influences the relative balance of stochastic and deterministic processes along successional soils. Given that pH had a much stronger association with community assembly than did successional age, we evaluated whether the inferred influence of pH was maintained when studying globally distributed samples collected without regard for successional age. This dataset confirmed the strong influence of pH, suggesting that the influence of soil pH on community assembly processes occurs globally. Extreme pH conditions likely exert more stringent limits on survival and fitness, imposing strong selective pressures through ecological and evolutionary time. Taken together, these findings suggest that the degree to which stochastic vs. deterministic processes shape soil bacterial community assembly is a consequence of soil pH rather than successional age. Introduction These authors contributed equally: Binu M. Tripathi and James C. Stegen. Electronic supplementary material The online version of this article (https://doi.org/10.1038/s41396-018-0082-4) contains supplementary material, which is available to authorized users. * Jonathan M. Adams j.m.adams@cranfield.ac.uk * Yoo Kyung Lee 1 Korea Polar Research Institute, Incheon 21990, Republic of Korea 2 Pacific Northwest National Laboratory, 902 Battelle Boulevard, P. O. Box 999, Richland, WA 99352, USA 3 Department of Biological Sciences, College of Natural Sciences, Seoul National University, 1 Gwanak-ro, Gwanak-gu, Seoul 08826, Republic of Korea 4 School of Water, Energy and Environment, Cranfield University, Cranfield MK43 0AL, UK Understanding the fundamental ecological processes that shape the assembly of microbial communities is a major challenge in microbial ecology [1]. The assembly of microbial species in a local community is influenced by two types of ecological processes, namely deterministic and stochastic [2, 3]. Deterministic processes include ecological selection imposed by abiotic and biotic factors, which influence organismal fitness and thereby determine the composition and relative abundance of species [4, 5]. Stochastic processes, in contrast, involve random birth, death, and dispersal events that result in patterns of species composition indistinguishable from those produced by random chance alone [6, 7]. Both deterministic and stochastic processes act concurrently to regulate the assembly of ecological communities [8–11]. However, variation in strength of ecological selection and rates of dispersal influence the relative importance of deterministic and stochastic processes across time, space, and from one system to another [12–14]. Soil pH mediates the balance between stochastic and deterministic assembly of bacteria… An open question is the degree to which differences in the balance between stochastic and deterministic processes are driven by differences between environments rather than time itself. Successional soils represent a series of soils of different ages with varying abiotic and biotic characteristics [15]. The pedogenesis (soil development) processes along successional soils results in directional change in nutrient content and often, but not always, lead to declines in pH [16–19]. Over the past decade, several studies have characterized the shifts in soil microbial communities along successional soils—on both shorter [20–25] and longer [26, 27] time scales. However, relatively little is known about the underlying ecological processes that govern the assembly of microbial communities in successional soils [13, 21, 28]. One limitation is that in any single dataset or system, environmental conditions often vary systematically with time such that these variables are confounded. Bringing together a set of successional systems that differ in the relationship between soil age and environmental properties is ideal for disentangling the relative contributions of the environment vs. time. Recent studies have indicated that in early successional soils, bacterial community assembly is largely governed by stochastic processes, with the relative importance of deterministic processes increasing progressively in later successional soils [13, 28]. However, it is still not clear what underlying environmental factors or community processes may be changing between early and late successional soils to produce this increased importance of determinism. For instance, it is well known that soil pH is very important in determining variation in bacterial community structure and diversity [29–33]. As pH often changes along successional soils [17], this could be the main cause of the observed trends in bacterial community assembly and also influence the relative importance of stochastic and deterministic processes across successional soils. Alternatively, time itself could be the driver wherein biological interactions change through time to alter the balance between stochastic and deterministic processes. To examine whether differences in soil pH (and other environmental variables) or time were the primary drivers of shifts in the stochastic-deterministic balance, we carried out a meta-analysis across a range of different successional soils, not all of which show the same trend in soil pH over time. This is a powerful design whereby successional age does not consistently co-vary with pH. Because successional age and pH do not confound each other, their relative influences can be evaluated. We applied an ecological null modeling approach to analyze the community assembly processes with the following questions: 1. Are there a pre (...truncated)