Does microbial habitat or community structure drive the functional stability of microbes to stresses following re-vegetation of a severely degraded soil?

Re-vegetation of eroded soil restores organic carbon concentrations and improves the physical stability of the soil, which may then extend the range of microhabitats and influence soil microbial activity and functional stability through its effects on soil bacterial community structure. The objectives of this study were (i) to evaluate the restorative effect of re-vegetation on soil physical stability, microbial activity and bacterial community structure; (ii) to examine the effects of soil physical microhabitats on bacterial community structure and diversity and on soil microbial functional stability. Soil samples were collected from an 18-year-old eroded bare soil restored with either Cinnamomum camphora (“Eroded Cc”) or Lespedeza bicolour (“Eroded Lb”). An uneroded soil planted with Pinus massoniana (“Uneroded Pm”) and an eroded bare soil served as references. The effect of microhabitats was assessed by physical destruction with a wet shaking treatment. Soil bacterial community structure and diversity were measured using a terminal restriction fragment length polymorphism (T-RFLP) approach, while soil microbiological stability (resistance and resilience) was determined by measuring short-term (28 days) decomposition rate of added barley (Hordeum vulgare) powder following copper and heat perturbations. The results demonstrated that re-vegetation treatment affected the recovery of physical and biological stability, microbial decomposition and the bacterial community structure. Although the restored soils overshot the Uneroded Pm sample in physical stability, they had lower microbial decomposition and less resilience to copper and heat perturbations than the Uneroded Pm samples. Soil physical destruction by shaking had the same effect on soil physical stability, but different effects on soil microbial functional stability. There were significant effects of vegetation treatment and perturbation type, and interactive effects among vegetation treatment, shaking and perturbation type on bacterial community structure. The destruction of aggregate structure increased resilience of the Eroded Lb sample and also altered its bacterial community structure. Both copper and heat perturbations resulted in significantly different community structure from the unperturbed controls, with a larger effect of copper than heat perturbation. Bacterial diversity (Shannon index) increased following the perturbations, with a more profound effect in the Uneroded Pm sample than in the restored soils. The interactive effects of vegetation treatment and shaking on microbial community and stability suggest that soil aggregation may contribute to the generation of bacterial community structure and mediation of biological stability via the protection afforded by soil organic carbon. Differential effects of re-vegetation treatment suggest that the long-term effects are mediated through changes in the quality and quantity of C inputs to soil.     

Functional resilience of soil microbial communities depends on both soil structure and microbial community composition

The effects of soil structure and microbial community composition on microbial resistance and resilience to stress were found to be interrelated in a series of experiments. The initial ability of Pseudomonas fluorescens to decompose added plant residues immediately after a copper or heat stress (resistance) depended significantly on which of 26 sterile soils it was inoculated into. Subsequent studies showed that both the resistance and subsequent recovery in the ability of P. fluorescens to decompose added plant residues over 28 days after stress (resilience) varied significantly between a sandy and a clay-loam soil. Sterile, sandy and clay-loam soil was then inoculated with a complex microbial community extracted from either of the soils. The resulting microbial community structure depended on soil type rather than the source of inoculum, whilst the resistance and resilience of decomposition was similarly governed by the soil and not the inoculum source. Resilience of the clay-loam soil to heat stress did not depend on the water content of the soil at the time of stress, although the physical condition of the soil when decomposition was measured did affect the outcome. We propose that soil functional resilience is governed by the physico-chemical structure of the soil through its effect on microbial community composition and microbial physiology.     

Exotic annuals reduce soil heterogeneity in coastal sage scrub soil chemical and biological characteristics

Exotic plant invasions alter ecosystem structure and function above- and below-ground through plant–soil feedbacks. The resistance of ecosystems to invasion can be measured by the degree of change in microbial communities and soil chemical pools and fluxes, whereas their resilience can be measured by the ability to recover following restoration. Coastal sage scrub (CSS) is one of the most highly invaded ecosystems in the US but the response of CSS soils to exotic plant invasion is little known. We examined resistance and resilience of CSS soil chemical and biological characteristics following invasion of exotic annual grasses and forbs and restoration of the native plant community. We hypothesized that invasion of exotic plant species would change biological and chemical characteristics of CSS soils by altering soil nutrient inputs. Additionally, we expected that if exotic plants were controlled and native plants were restored, native soil characteristics would recover. We sampled two locations with invaded, restored and native CSS for plant community composition, soil chemistry and microbial communities, and phospholipid fatty acid (PLFA) profiles. Communities invaded by exotic annuals were resistant to some measured parameters but not others. Extractable nitrogen pools decreased, nitrogen cycling rates increased, and microbial biomass and fungal:bacterial ratios were altered in invaded soils, and these effects were mediated by the phenological stage of the dominant plant species. The largest impact of invasion on soils was an overall reduction of spatial heterogeneity in soil nutrients, nutrient cycling and microbial communities. Restored plots tended to recover in most biotic and chemical parameters including increased resource heterogeneity compared to invaded plots, suggesting that CSS soils are resilient but not resistant to invasion.     

Physical resilience of soil to field compaction and the interactions with plant growth and microbial community structure

Soil compaction has deleterious effects on soil physical properties, which can affect plant growth, but some soils are inherently resilient, whereby they may recover following removal of the stress. We explored aspects of soil physical resilience in a field‐based experiment. We subjected three soils of different texture, sown with winter wheat or remaining fallow, to a compaction event. We then monitored soil strength, as a key soil physical property, over the following 16 months. We were also interested in the associated interactions with crop growth and the microbial community. Compaction had a considerable and sustained effect in a sandy loam and a sandy clay loam soil, resulting in an increase in strength and decreased crop yields. By contrast compaction had little effect on a clay soil, perhaps due initially to the buoyancy effect of pore water pressure. Fallow clay soil did have a legacy of the compaction event at depth, however, suggesting that it was the actions of the crop, and rooting in particular, that maintained smaller strengths in the cropped clay soil rather than other physical processes. Compaction generally did not affect microbial communities, presumably because they occupy pores smaller than those affected by compaction. That the clay soil was able to supply the growing crop with sufficient water whilst remaining weak enough for root penetration was a key finding. The clay soil was therefore deemed to be much more resilient to the compaction stress than the sandy loam and sandy clay loam soils.     

Rhizosphere effects on functional stability of microbial communities in conventional and organic soils following elevated temperature treatment

The resistance and resilience of soil function may be increased through selection of crops and organic matter inputs. Soil from paired organic or conventional plots was left unplanted or used to grow barley. Substrate induced respiration (SIR) and community level physiological profiles (CLPP) were significantly different in both planted and unplanted systems and in conventional and organically-managed farming systems with no interaction; planted and organic systems had higher SIR. Following heat treatment (30 min at 70 °C), CLPP of planted and unplanted soils in both farming systems changed; a small short-lived decline in SIR only occurred in the planted soils. Differences in the response of these microbial communities to stress may be related to the relative proportions of active and dormant organisms; an increase in functional diversity did not necessarily reflect changed soil function.     

Experimental warming effects on the microbial community of a temperate mountain forest soil

Soil microbial communities mediate the decomposition of soil organic matter (SOM). The amount of carbon (C) that is respired leaves the soil as CO₂ (soil respiration) and causes one of the greatest fluxes in the global carbon cycle. How soil microbial communities will respond to global warming, however, is not well understood. To elucidate the effect of warming on the microbial community we analyzed soil from the soil warming experiment Achenkirch, Austria. Soil of a mature spruce forest was warmed by 4 °C during snow-free seasons since 2004. Repeated soil sampling from control and warmed plots took place from 2008 until 2010. We monitored microbial biomass C and nitrogen (N). Microbial community composition was assessed by phospholipid fatty acid analysis (PLFA) and by quantitative real time polymerase chain reaction (qPCR) of ribosomal RNA genes. Microbial metabolic activity was estimated by soil respiration to biomass ratios and RNA to DNA ratios. Soil warming did not affect microbial biomass, nor did warming affect the abundances of most microbial groups. Warming significantly enhanced microbial metabolic activity in terms of soil respiration per amount of microbial biomass C. Microbial stress biomarkers were elevated in warmed plots. In summary, the 4 °C increase in soil temperature during the snow-free season had no influence on microbial community composition and biomass but strongly increased microbial metabolic activity and hence reduced carbon use efficiency.     

Decreases in microbial functional diversity do not result in corresponding changes in decomposition under different moisture conditions

This study compares the functional capability of soils with differing microbial diversity. Soil microbial diversity was modified by either fumigation with reinoculation by unfumigated soil or fumigation with no reinoculation. Functional capability was assessed by following wheat straw decomposition in these soils and in an unfumigated control soil at three matric potentials (−5, −125 and −800 kPa). The changes in diversity after fumigation were compared with the effects of disturbance treatments (slow air-drying, rapid oven-drying, 2 mm sieving and 0.5 mm sieving) by studying patterns of in situ catabolic potential (ISCP) at 1 and 8 weeks. Five weeks after the fumigation treatments, the functional and phenotypic diversity of the soil microbial community, as revealed by patterns of ISCP and phospholipid fatty acid (PLFA) profiles, respectively, were greatly different from that in unfumigated soil. The effects of the fumigation reinoculation treatment on functional diversity were comparable with those caused by rapid oven-drying, but were greater than the effects of 0.5 mm sieving. These disturbance treatments caused persistent changes in functional diversity, whereas slow air-drying and 2 mm sieving had little influence on diversity. Rates of straw decomposition were initially greater in the fumigated reinoculated soil than in the unfumigated soil at all moisture potentials. In contrast, straw mineralisation rates in the fumigated uninoculated soil generally exceeded rates in unfumigated soil for a period after 14 d, which was shorter at greater moisture potentials. These rates resulted in total straw mineralisation in fumigated reinoculated soil exceeding that in unfumigated soil at all moisture potentials. Compared with the unfumigated soils, total straw mineralisation in fumigated uninoculated soil was less at −5 kPa, similar at −125 kPa and greater at −800 kPa. The results indicated that the decomposition function of soil with reduced functional diversity can be diminished under optimum moisture conditions, but is not invariably reduced when assessed under suboptimal moisture conditions. This indicated that decreases in the functional diversity of soil microbial communities may not consistently result in declines in soil functioning.     

Organic nitrogen cycling microbial communities are abundant in a dry Australian agricultural soil

Some microbial nitrogen (N) cycling processes continue under low soil moisture levels in drought-adapted ecosystems. These processes are of particular importance in winter cropping systems, where N availability during autumn sowing informs fertilizer practices and impacts crop productivity. We evaluated the organic and inorganic N-cycling communities in a key cropping soil (Vertosol), using a controlled-environment incubation study that was designed to model the autumn break in south Australian grain growing regions. Soils from wheat, lucerne, and green manure (disced-in vetch) rotations of the Sustainable Cropping Rotations in Mediterranean Environments trial (Victoria, Australia) were collected during the summer when soil moisture was low. Microbial community structure and functional capacity were measured both before and after wetting (21, 49, and 77 days post-wetting) using terminal restriction fragment length polymorphism measures of bacterial and fungal communities, and quantitative PCR of nitrogen cycling genes. Quantified genes included those associated with organic matter decomposition (laccase, cellobiohydrolase), mineralization of N from organic matter (peptidases) and nitrification (bacterial and archaeal ammonia monooxygenase and nitrite oxidoreductase). In general, the N cycling functional capacity decreased with soil wetting, and there was an apparent shift from organic-N cycling dominance to autotrophic mineral-N cycling dominance. Soil nitrate levels were best predicted by laccase and neutral peptidase genes under drought conditions, but by neutral peptidase and bacterial ammonia monooxygenase genes under moist conditions. Rotation history affected both the structural and functional resilience of the soil microbial communities to changing soil moisture. Discing in green manure (vetch) residues promoted a resilient microbial community, with a high organic-N cycling capacity in dry soils. Although this was a small-scale microcosm study, our results suggest that management strategies could be developed to control microbial organic-N processing during the summer fallow period and thus improve crop-available N levels at sowing.     

Development of pollution-induced community tolerance is linked to structural and functional resilience of a soil bacterial community following a five-year field exposure to copper

Copper (Cu) is accumulating in agricultural soils worldwide creating concern for adverse impacts on soil microbial communities and associated ecosystem services. In order to evaluate the structural and functional resilience of soil microbial communities to increasing Cu levels, we compared a Cu-adapted and a corresponding non-adapted soil microbial community for their abilities to resist experimental Cu pollution. Laboratory soil microcosms were set-up with either High-Cu soil from Cu-amended field plots (63 g Cu m⁻²) or with Low-Cu control soil from the same five-year field experiment. Laboratory treatments consisted of Cu amendments in the presence or absence of pig manure. Microbial activities (soil respiration, substrate-induced respiration, [³H]leucine incorporation), bacterial community structure (terminal restriction fragment length polymorphism, T-RFLP), community-level physiological profiles, and pollution-induced bacterial community tolerance (PICT detected using the [³H]leucine incorporation technique) were monitored for 12 weeks. The High-Cu and Low-Cu soil microbial communities initially exhibited almost identical structure and function and could only be distinguished from each other by their differential Cu tolerance. Experimental Cu pollution inhibited microbial activities, affected bacterial community structure, and induced further bacterial community tolerance to Cu. However, Low-Cu and High-Cu soil microbial communities showed essentially identical responses. Manure amendment did not protect against Cu toxicity and slightly increased Cu bioavailability as measured by a Cu-specific whole-cell bacterial biosensor. Our results indicate convergence of bacterial community structure and function in the High-Cu and Low-Cu soils during the five-year field experiment. We conclude that soil bacterial communities can exhibit structural and functional resilience to a five-year Cu exposure by virtue of their ability to develop Cu tolerance without affecting overall community structure. The observed increased Cu tolerance may involve phenotypic adaptation or selection at the micro-diversity level, for example an increased proportion of Cu-resistant strains within each bacterial species, which go undetected by T-RFLP community fingerprinting. Finally, our results indicate that Cu-dissolved organic matter complexes contribute to microbial toxicity in manure-amended soils implying that free Cu may comprise a poor predictor of metal toxicity.     

Biological and physical resilience of soil amended with heavy metal-contaminated sewage sludge

Stability and resilience of a variety of soil properties and processes are emerging as key components of soil quality. We applied recently developed measures of biological and physical resilience to soils from an experimental site treated with metal‐contaminated sewage sludge. Soils treated with cadmium‐, copper‐ or zinc‐contaminated, digested or undigested sewage sludge were studied. Biological stability and resilience indices were: (i) the time‐dependent effects of either a transient stress (heating to 40°C for 18 hours) or a persistent stress (amendment with CuSO₄) on decomposition, and (ii) the mineralization of dissolved organic carbon (DOC) released by drying–rewetting cycles. Physical stability and resilience measures were: (i) compression and expansion indices of the soils, and (ii) resistance to prolonged wetting and structural regeneration through drying–rewetting cycles. Soil total carbon and DOC levels were greater in the sludge‐amended soils, but there were no differential effects due to metal contamination of the sewage sludge. Effects of metals on physical resilience were greater than effects on soil C, there being marked reductions in the expansion indices with Cd‐ and Cu‐contaminated sludge, and pointed to changes in soil aggregation. The rate of mineralization of DOC released by drying and wetting was reduced by Zn contamination, while biological resilience was increased in the Zn‐contaminated soil and reduced by Cd contamination. We argue that physical and biological resilience are potentially coupled through the microbial community. This needs to be tested in a wider range of soils, but demonstrates the benefits from a combined approach to the biological and physical resilience of soils.