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. 2015 Mar 17;112(11):E1326-32.
doi: 10.1073/pnas.1414261112. Epub 2015 Mar 2.

Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession

Francisco Dini-Andreote  1 , James C Stegen  2 , Jan Dirk van Elsas  3 , Joana Falcão Salles  3
Affiliations

Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession

"V体育安卓版" Francisco Dini-Andreote et al. Proc Natl Acad Sci U S A. .

Abstract

Ecological succession and the balance between stochastic and deterministic processes are two major themes within microbial ecology, but these conceptual domains have mostly developed independent of each other. Here we provide a framework that integrates shifts in community assembly processes with microbial primary succession to better understand mechanisms governing the stochastic/deterministic balance. Synthesizing previous work, we devised a conceptual model that links ecosystem development to alternative hypotheses related to shifts in ecological assembly processes. Conceptual model hypotheses were tested by coupling spatiotemporal data on soil bacterial communities with environmental conditions in a salt marsh chronosequence spanning 105 years of succession VSports手机版. Analyses within successional stages showed community composition to be initially governed by stochasticity, but as succession proceeded, there was a progressive increase in deterministic selection correlated with increasing sodium concentration. Analyses of community turnover among successional stages--which provide a larger spatiotemporal scale relative to within stage analyses--revealed that changes in the concentration of soil organic matter were the main predictor of the type and relative influence of determinism. Taken together, these results suggest scale-dependency in the mechanisms underlying selection. To better understand mechanisms governing these patterns, we developed an ecological simulation model that revealed how changes in selective environments cause shifts in the stochastic/deterministic balance. Finally, we propose an extended--and experimentally testable--conceptual model integrating ecological assembly processes with primary and secondary succession. This framework provides a priori hypotheses for future experiments, thereby facilitating a systematic approach to understand assembly and succession in microbial communities across ecosystems. .

Keywords: community assembly; evolutionary niche conservatism; neutral theory; niche theory; simulation model V体育安卓版. .

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Three-phase conceptual model composed of alternative hypotheses related to changes in the strength and type of ecological selection during primary succession. Ecological selection is weak in the center of the vertical axis and is stronger toward both extremes. In phase 1, the initial establishment of microbial communities is expected to be dominated by stochasticity such that turnover in community composition shows little deviation from the null expectation. In phase 2, changes in environmental conditions progressively increase the strength of selection leading to scenarios 1a and 1b; if the environmental factors that change through time do not impose selection, stochastic factors are expected to remain dominant such that the system will remain ecologically neutral [sensu Hubbell (5)] as in scenario 1c. When succession is associated with increasing spatial heterogeneity in selective pressures the variable selection (VS) scenario (1a) is expected; spatial environmental heterogeneity causes turnover in community composition to be greater than the null expectation. In contrast, a spatially homogeneous environment and directional changes—across successional stages—toward increasingly extreme selective conditions lead to the homogeneous selection (HS) scenario (1b); spatial environmental homogeneity causes turnover in community composition to be lower than the null expectation. In phase 3, if succession eventually leads to relatively stable environmental conditions, a relatively stable balance between stochastic/deterministic processes is expected.
Fig. 2.
Fig. 2.
Patterns of βNTI and stochasticity. (A) Box plots of βNTI distributions across successional stages showing the median (thick black line), the first quartile (lower box bound), the third quartile (upper box bound), the range of data values that deviate from the box no more than 1.5 times the height of the box (vertical dashed lines), and outliers (open circles). Horizontal dashed lines indicate upper and lower significance thresholds at βNTI = +2 and −2, respectively. (B) The estimated relative influence of stochasticity as a function of log-transformed Na concentration per gram of soil. The solid line is the linear regression model, and statistics are provided on the panel.
Fig. 3.
Fig. 3.
βNTI patterns from empirical comparisons and simulated ecological scenarios. (A) βNTI for all pairwise community comparisons—within and between successional stages—as a function of the change in log-transformed soil organic matter (SOM) concentration between communities, presented as the fold change in SOM. The linear regression model is shown as the green line; statistics are provided on the panel. Horizontal dashed lines indicate the upper (+2) and lower (−2) significance thresholds. Boxes laid over the βNTI data represent our conceptual interpretation of how simulation model outputs (summarized in B) align with the empirical relationship between βNTI and changes in SOM. (B) βNTI distributions obtained from simulated ecological scenarios (see Fig. S3 for a detailed description).
Fig. 4.
Fig. 4.
Hypothesized conceptual model linking primary and secondary succession to the stochastic/deterministic balance. Phase 3 is the final phase of primary succession and is consistent with phase 3 in Fig. 1; vertical axis is as in Fig. 1. Following a disturbance event the relative influence of stochastic factors can shift in ways that are dependent on both the outcome of primary succession and the type of disturbance. In scenario 2a (red line), primary succession has resulted in strong variable selection. A significant shift away from strong variable selection—following disturbance—is expected if the environment is homogenized; the system may become dominated by strong homogeneous selection (not displayed) or become neutral if the resulting environmental condition does or does not, respectively, impose strong selection. In scenario 2b (purple line), a strong influence of stochastic factors has been maintained throughout primary succession, and the disturbance itself imposes a strong and spatially homogeneous selective pressure similar to patterns observed in soil microbial communities following fire (20). In scenarios 2c and 2d (blue lines), primary succession has resulted in strong homogeneous selection as in our field system. In scenario 2c, disturbance removes the strong selective pressure that developed over the course of primary succession; in our field system this could occur if shifts in topography lead to an increased frequency of tidal inundation at an older part of the chronosequence, thereby causing a decline in Na concentration. In scenario 2d, disturbance does not impact the primary selective pressure such that strong homogeneous selection is expected to be maintained; in our field system this could occur if SOM was artificially added to the later successional stages—high Na concentrations in late primary successional stages impose a dominant selective pressure that would not be alleviated by the addition of SOM.
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References

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