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Microbial community response to hydration-desiccation cycles in desert soil

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ABSTRACT

Life in desert soil is marked by episodic pulses of water and nutrients followed by long periods of drought. While the desert flora and fauna flourish after rainfall the response of soil microorganisms remains unclear and understudied. We provide the first systematic study of the role of soil aqueous habitat dynamics in shaping microbial community composition and diversity. Detailed monitoring of natural microbial communities after a rainfall event revealed a remarkable decrease in diversity and a significant transition in community composition that were gradually restored to pre-rainfall values during soil desiccation. Modelling results suggest a critical role for the fragmented aqueous habitat in maintaining microbial diversity under dry soil conditions and diversity loss with wetting events that increase connectivity among habitats. This interdisciplinary study provides new insights into wetting and drying processes that promote and restore the unparalleled microbial diversity found in soil.

No MeSH data available.


A wetting-drying cycle was applied to the modified rough-surface patch model (RSPM) to observe its effect on bacterial diversity and the community composition.(A) The relative abundance dynamics of modelled bacterial classes are depicted. In the simulations, 40 virtual taxa (20 taxa growing aerobically and other 20 taxa growing anaerobically) were inoculated. For this figure, the virtual taxa were classified to 10 classes (5 aerobic groups shown in light colours and 5 anaerobic groups shown in dark colours) and the relative abundance dynamics of 10 independent simulations were averaged. (B) Shannon index of the simulated bacterial populations were compared with the field measurements suggesting that in both the diversity decreased rapidly after wetting and then recovered with drying. For this comparison, the field measurements and the simulation results were rescaled with the value at day 0 (dry soil) indicating the relative changes. Results from 10 individual simulations (with different inoculation of microbial cells and different soil structures with same pore size distribution and porosity) are averaged (red line) and shaded area (in pink) indicates the standard deviation (s.t.d.). Averaged values of measurements are presented with mean ± s.t.d. (black solid lines) calculated from three environmental replicates in 3 adjacent plots.
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f3: A wetting-drying cycle was applied to the modified rough-surface patch model (RSPM) to observe its effect on bacterial diversity and the community composition.(A) The relative abundance dynamics of modelled bacterial classes are depicted. In the simulations, 40 virtual taxa (20 taxa growing aerobically and other 20 taxa growing anaerobically) were inoculated. For this figure, the virtual taxa were classified to 10 classes (5 aerobic groups shown in light colours and 5 anaerobic groups shown in dark colours) and the relative abundance dynamics of 10 independent simulations were averaged. (B) Shannon index of the simulated bacterial populations were compared with the field measurements suggesting that in both the diversity decreased rapidly after wetting and then recovered with drying. For this comparison, the field measurements and the simulation results were rescaled with the value at day 0 (dry soil) indicating the relative changes. Results from 10 individual simulations (with different inoculation of microbial cells and different soil structures with same pore size distribution and porosity) are averaged (red line) and shaded area (in pink) indicates the standard deviation (s.t.d.). Averaged values of measurements are presented with mean ± s.t.d. (black solid lines) calculated from three environmental replicates in 3 adjacent plots.

Mentions: We applied a mechanistic model for microbial populations’ dynamics during changes in soil wetness (induced by the rainfall event). The model results were in qualitative agreement with field observations in terms of microbial diversity and the community composition changes. Figure 3 depicts the predicted effect of hydration dynamics on the soil microbial community. After soil wetting, the relative abundance of various taxa exhibited a dynamic response. Figure 3A shows the rise of anaerobic classes (marked with strong colours) from day 2 to day 7, replacing aerobic classes that were prevalent in the dry soil. The model results show the sharp decrease of anaerobes at between day 6 and day 7 as the soil became aerated again. While drying, air penetrates through the profile and shifts most of the domain back from anoxic to oxic conditions (corresponding to a water content of 0.1 [g/g]). Furthermore, in Fig. 3B, the relative changes in Shannon index was chosen as the key diversity index for a comparison with the field observations. The decrease in diversity indicates the rises of dominant taxa during wetting. This is driven by competitive interactions among individuals over a common substrate, in this case the carbon source. The connected aqueous habitats and the increased dispersal of cells allowed intense competition for the substrate thereby causing the changes in diversity. The recovery of diversity reflects the role of aqueous habitat fragmentation. As the degree of connectivity in the aqueous phase decreased, microbial interactions are spatially limited31. Essentially, the observed dynamics of community composition and diversity are the outcome of simultaneous effects of the competition over dissolved substrates and the temporary dominance of anaerobic taxa due the transition from oxic to anoxic conditions in some parts of the wet soil.


Microbial community response to hydration-desiccation cycles in desert soil
A wetting-drying cycle was applied to the modified rough-surface patch model (RSPM) to observe its effect on bacterial diversity and the community composition.(A) The relative abundance dynamics of modelled bacterial classes are depicted. In the simulations, 40 virtual taxa (20 taxa growing aerobically and other 20 taxa growing anaerobically) were inoculated. For this figure, the virtual taxa were classified to 10 classes (5 aerobic groups shown in light colours and 5 anaerobic groups shown in dark colours) and the relative abundance dynamics of 10 independent simulations were averaged. (B) Shannon index of the simulated bacterial populations were compared with the field measurements suggesting that in both the diversity decreased rapidly after wetting and then recovered with drying. For this comparison, the field measurements and the simulation results were rescaled with the value at day 0 (dry soil) indicating the relative changes. Results from 10 individual simulations (with different inoculation of microbial cells and different soil structures with same pore size distribution and porosity) are averaged (red line) and shaded area (in pink) indicates the standard deviation (s.t.d.). Averaged values of measurements are presented with mean ± s.t.d. (black solid lines) calculated from three environmental replicates in 3 adjacent plots.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC5382909&req=5

f3: A wetting-drying cycle was applied to the modified rough-surface patch model (RSPM) to observe its effect on bacterial diversity and the community composition.(A) The relative abundance dynamics of modelled bacterial classes are depicted. In the simulations, 40 virtual taxa (20 taxa growing aerobically and other 20 taxa growing anaerobically) were inoculated. For this figure, the virtual taxa were classified to 10 classes (5 aerobic groups shown in light colours and 5 anaerobic groups shown in dark colours) and the relative abundance dynamics of 10 independent simulations were averaged. (B) Shannon index of the simulated bacterial populations were compared with the field measurements suggesting that in both the diversity decreased rapidly after wetting and then recovered with drying. For this comparison, the field measurements and the simulation results were rescaled with the value at day 0 (dry soil) indicating the relative changes. Results from 10 individual simulations (with different inoculation of microbial cells and different soil structures with same pore size distribution and porosity) are averaged (red line) and shaded area (in pink) indicates the standard deviation (s.t.d.). Averaged values of measurements are presented with mean ± s.t.d. (black solid lines) calculated from three environmental replicates in 3 adjacent plots.
Mentions: We applied a mechanistic model for microbial populations’ dynamics during changes in soil wetness (induced by the rainfall event). The model results were in qualitative agreement with field observations in terms of microbial diversity and the community composition changes. Figure 3 depicts the predicted effect of hydration dynamics on the soil microbial community. After soil wetting, the relative abundance of various taxa exhibited a dynamic response. Figure 3A shows the rise of anaerobic classes (marked with strong colours) from day 2 to day 7, replacing aerobic classes that were prevalent in the dry soil. The model results show the sharp decrease of anaerobes at between day 6 and day 7 as the soil became aerated again. While drying, air penetrates through the profile and shifts most of the domain back from anoxic to oxic conditions (corresponding to a water content of 0.1 [g/g]). Furthermore, in Fig. 3B, the relative changes in Shannon index was chosen as the key diversity index for a comparison with the field observations. The decrease in diversity indicates the rises of dominant taxa during wetting. This is driven by competitive interactions among individuals over a common substrate, in this case the carbon source. The connected aqueous habitats and the increased dispersal of cells allowed intense competition for the substrate thereby causing the changes in diversity. The recovery of diversity reflects the role of aqueous habitat fragmentation. As the degree of connectivity in the aqueous phase decreased, microbial interactions are spatially limited31. Essentially, the observed dynamics of community composition and diversity are the outcome of simultaneous effects of the competition over dissolved substrates and the temporary dominance of anaerobic taxa due the transition from oxic to anoxic conditions in some parts of the wet soil.

View Article: PubMed Central - PubMed

ABSTRACT

Life in desert soil is marked by episodic pulses of water and nutrients followed by long periods of drought. While the desert flora and fauna flourish after rainfall the response of soil microorganisms remains unclear and understudied. We provide the first systematic study of the role of soil aqueous habitat dynamics in shaping microbial community composition and diversity. Detailed monitoring of natural microbial communities after a rainfall event revealed a remarkable decrease in diversity and a significant transition in community composition that were gradually restored to pre-rainfall values during soil desiccation. Modelling results suggest a critical role for the fragmented aqueous habitat in maintaining microbial diversity under dry soil conditions and diversity loss with wetting events that increase connectivity among habitats. This interdisciplinary study provides new insights into wetting and drying processes that promote and restore the unparalleled microbial diversity found in soil.

No MeSH data available.