High intensity perturbations induce an abrupt shift in soil microbial state

Abstract

Soil microbial communities play a pivotal role in regulating ecosystem functioning. But they are increasingly being shaped by human-induced environmental change, including intense "pulse" perturbations, such as droughts, which are predicted to increase in frequency and intensity with climate change. While it is known that soil microbial communities are sensitive to such perturbations and that effects can be long-lasting, it remains untested whether there is a threshold in the intensity and frequency of perturbations that can trigger abrupt and persistent transitions in the taxonomic and functional characteristics of soil microbial communities. Here we demonstrate experimentally that intense pulses of drought equivalent to a 30-year drought event (<15% WHC) induce a major shift in the soil microbial community characterised by significantly altered bacterial and fungal community structures of reduced complexity and functionality. Moreover, the characteristics of this transformed microbial community persisted after returning soil to its previous moisture status. As a result, we found that drought had a strong legacy effect on bacterial community function, inducing an enhanced growth rate following subsequent drought. Abrupt transitions are widely documented in aquatic and terrestrial plant communities in response to human-induced perturbations. Our findings demonstrate that such transitions also occur in soil microbial communities in response to high intensity pulse perturbations, with potentially deleterious consequences for soil health.

Fig. 1. Effects of drought on soil microbial community structure.

a–d Alpha diversity 6 months after drought (mean ± error of estimated values). e, f Community structure. The first two axes explained 17.3% (bacteria) and 5.4% (fungi) of the variance. g Percentage variance explained in PERMANOVA analyses including all the treatments (global) or just one drought intensity level and the control. h, i Relative abundance of microbial families. Data = mean (n = 4). sg subgroup. Significance of drought intensity (I), frequency (F), and time point (T) is shown (a–g): *p < 0.05, **p < 0.01, ***p < 0.001, or significance of drought treatment for each sampling time (h, i): ^-p > 0.05, *p < 0.05.

Fig. 2. Effects of drought on soil function.

a, b Resistance and resilience indexes. Asterisks indicate significant change (value ≠ 0, p < 0.05). c, d Functional structure of soils. Mean ± SE (n = 4). Significance of PERMANOVA analysis evaluating the effects of drought intensity (I) and frequency (F) is shown: *p < 0.05, **p < 0.01, ***p < 0.001. Differences in data dispersion (dd) among groups is also shown (^ns non-significant). GLC: β-glucosidase, CBH: cellobiohydrolase, XYL: xylosidase, NAG: N-acetylglocasiminidase, PHO: acid phosphatase, POX: phenoloxidase, PER: peroxidase, URE: urease, DOC: dissolved organic carbon, DON: dissolved organic nitrogen, TOP: total organic phosphorus, C_mic: microbial carbon, N_mic : microbial nitrogen, P_mic : microbial phosphorus. e–h Effects of drought on selected soil nutrients after drought, summarised by drought intensity and frequency (x1: 1 event, x2: 2 events, x3: 3 events) treatments. Significance of linear mixed models evaluating the effects of drought intensity (I) and frequency (F), with soil as random factor, is shown in each graph. Values = mean ± standard error, n = 4.

Fig. 3. Adaptation to drought of microbial community traits.

Growth responses to a further drying/rewetting cycle of soils with different drought history, one month after drought. a Cumulative bacterial growth, b bacterial lag period, c cumulative fungal growth, d cumulative respiration. Mean ± SD (n = 4). Significance of LME evaluating the effects of drought intensity (I) and frequency (F) is shown: *p < 0.05, **p < 0.01, ***p < 0.001.

Fig. 4. Drought threshold and potential shift to an alternative state in soil microbial communities.

a–d Drought threshold: microbial community diversity, composition and multifunctionality depending on minimum water holding capacity (WHC) experienced by soils. e Functional capacity of soils evaluated by principal non-metric multidimensional scaling (NMDS) analysis with schematic representation of a shift to an alternative state. Mild or intermediate drought (blue arrows) moved the system from the reference state (circle on the left), but they bounced back. Intense drought (red arrow) moved the system further away, crossing a threshold, into an alternative state (circle on the right). f–h Diagrammatic representations of the effects of drought on the system, represented as a ball moving up and out of the stability basin. Mild or intermediate drought do not push the ball far enough, bouncing back to the reference state (f), while intense drought pushes the ball out of the reference state into a different stability basin, an alternative state (g), with distinct functionality and microbial community composition (h).