General statistical scaling laws for stability in ecological systems.

Ecological stability refers to a family of concepts used to describe how systems of interacting species vary through time and respond to disturbances. Because observed ecological stability depends on sampling scales and environmental context, it is notoriously difficult to compare measurements across sites and systems. Here, we apply stochastic dynamical systems theory to derive general statistical scaling relationships across time, space, and ecological level of organisation for three fundamental stability aspects: resilience, resistance, and invariance. These relationships can be calibrated using random or representative samples measured at individual scales, and projected to predict average stability at other scales across a wide range of contexts. Moreover deviations between observed vs. extrapolated scaling relationships can reveal information about unobserved heterogeneity across time, space, or species. We anticipate that these methods will be useful for cross-study synthesis of stability data, extrapolating measurements to unobserved scales, and identifying underlying causes and consequences of heterogeneity.

Spatiotemporal disturbance characteristics determine functional stability and collapse risk of simulated microbial ecosystems.

Terrestrial microbial ecosystems are exposed to many types of disturbances varying in their spatial and temporal characteristics. The ability to cope with these disturbances is crucial for maintaining microbial ecosystem functions, especially if disturbances recur regularly. Thus, understanding microbial ecosystem dynamics under recurrent disturbances and identifying drivers of functional stability and thresholds for functional collapse is important. Using a spatially explicit ecological model of bacterial growth, dispersal, and substrate consumption, we simulated spatially heterogeneous recurrent disturbances and investigated the dynamic response of pollutant biodegradation - exemplarily for an important ecosystem function. We found that thresholds for functional collapse are controlled by the combination of disturbance frequency and spatial configuration (spatiotemporal disturbance regime). For rare disturbances, the occurrence of functional collapse is promoted by low spatial disturbance fragmentation. For frequent disturbances, functional collapse is almost inevitable. Moreover, the relevance of bacterial growth and dispersal for functional stability also depends on the spatiotemporal disturbance regime. Under disturbance regimes with moderate severity, microbial properties can strongly affect functional stability and shift the threshold for functional collapse. Similarly, networks facilitating bacterial dispersal can delay functional collapse. Consequently, measures to enhance or sustain bacterial growth/dispersal are promising strategies to prevent functional collapses under moderate disturbance regimes.

Functional Resistance to Recurrent Spatially Heterogeneous Disturbances Is Facilitated by Increased Activity of Surviving Bacteria in a Virtual Ecosystem.

Bacterial degradation of organic compounds is an important ecosystem function with relevance to, e.g., the cycling of elements or the degradation of organic contaminants. It remains an open question, however, to which extent ecosystems are able to maintain such biodegradation function under recurrent disturbances (functional resistance) and how this is related to the bacterial biomass abundance. In this paper, we use a numerical simulation approach to systematically analyze the dynamic response of a microbial population to recurrent disturbances of different spatial distribution. The spatially explicit model considers microbial degradation, growth, dispersal, and spatial networks that facilitate bacterial dispersal mimicking effects of mycelial networks in nature. We find: (i) There is a certain capacity for high resistance of biodegradation performance to recurrent disturbances. (ii) If this resistance capacity is exceeded, spatial zones of different biodegradation performance develop, ranging from no or reduced to even increased performance. (iii) Bacterial biomass and biodegradation dynamics respond inversely to the spatial fragmentation of disturbances: overall biodegradation performance improves with increasing fragmentation, but bacterial biomass declines. (iv) Bacterial dispersal networks can enhance functional resistance against recurrent disturbances, mainly by reactivating zones in the core of disturbed areas, even though this leads to an overall reduction of bacterial biomass.

Mycelium-mediated transfer of water and nutrients stimulates bacterial activity in dry and oligotrophic environments.

Fungal-bacterial interactions are highly diverse and contribute to many ecosystem processes. Their emergence under common environmental stress scenarios however, remains elusive. Here we use a synthetic microbial ecosystem based on the germination of Bacillus subtilis spores to examine whether fungal and fungal-like (oomycete) mycelia reduce bacterial water and nutrient stress in an otherwise dry and nutrient-poor microhabitat. We find that the presence of mycelia enables the germination and subsequent growth of bacterial spores near the hyphae. Using a combination of time of flight- and nanoscale secondary ion mass spectrometry (ToF- and nanoSIMS) coupled with stable isotope labelling, we link spore germination to hyphal transfer of water, carbon and nitrogen. Our study provides direct experimental evidence for the stimulation of bacterial activity by mycelial supply of scarce resources in dry and nutrient-free environments. We propose that mycelia may stimulate bacterial activity and thus contribute to sustaining ecosystem functioning in stressed habitats.

Bacterial Dispersal Promotes Biodegradation in Heterogeneous Systems Exposed to Osmotic Stress.

Contaminant biodegradation in soils is hampered by the heterogeneous distribution of degrading communities colonizing isolated microenvironments as a result of the soil architecture. Over the last years, soil salinization was recognized as an additional problem especially in arid and semiarid ecosystems as it drastically reduces the activity and motility of bacteria. Here, we studied the importance of different spatial processes for benzoate biodegradation at an environmentally relevant range of osmotic potentials (ΔΨo) using model ecosystems exhibiting a heterogeneous distribution of the soil-borne bacterium Pseudomonas putida KT2440. Three systematically manipulated scenarios allowed us to cover the effects of (i) substrate diffusion, (ii) substrate diffusion and autonomous bacterial dispersal, and (iii) substrate diffusion and autonomous as well as mediated bacterial dispersal along glass fiber networks mimicking fungal hyphae. To quantify the relative importance of the different spatial processes, we compared these heterogeneous scenarios to a reference value obtained for each ΔΨo by means of a quasi-optimal scenario in which degraders were ab initio homogeneously distributed. Substrate diffusion as the sole spatial process was insufficient to counteract the disadvantage due to spatial degrader heterogeneity at ΔΨo ranging from 0 to -1 MPa. In this scenario, only 13.8-21.3% of the quasi-optimal biodegradation performance could be achieved. In the same range of ΔΨo values, substrate diffusion in combination with bacterial dispersal allowed between 68.6 and 36.2% of the performance showing a clear downwards trend with decreasing ΔΨo. At -1.5 MPa, however, this scenario performed worse than the diffusion scenario, possibly as a result of energetic disadvantages associated with flagellum synthesis and emerging requirements to exceed a critical population density to resist osmotic stress. Network-mediated bacterial dispersal kept biodegradation almost consistently high with an average of 70.7 ± 7.8%, regardless of the strength of the osmotic stress. We propose that especially fungal network-mediated bacterial dispersal is a key process to achieve high functionality of heterogeneous microbial ecosystems also at reduced osmotic potentials. Thus, mechanical stress by, for example, soil homogenization should be kept low in order to preserve fungal network integrity.

Mycelium-Like Networks Increase Bacterial Dispersal, Growth, and Biodegradation in a Model Ecosystem at Various Water Potentials.

Fungal mycelia serve as effective dispersal networks for bacteria in water-unsaturated environments, thereby allowing bacteria to maintain important functions, such as biodegradation. However, poor knowledge exists on the effects of dispersal networks at various osmotic (Ψo) and matric (Ψm) potentials, which contribute to the water potential mainly in terrestrial soil environments. Here we studied the effects of artificial mycelium-like dispersal networks on bacterial dispersal dynamics and subsequent effects on growth and benzoate biodegradation at ΔΨo and ΔΨm values between 0 and -1.5 MPa. In a multiple-microcosm approach, we used a green fluorescent protein (GFP)-tagged derivative of the soil bacterium Pseudomonas putida KT2440 as a model organism and sodium benzoate as a representative of polar aromatic contaminants. We found that decreasing ΔΨo and ΔΨm values slowed bacterial dispersal in the system, leading to decelerated growth and benzoate degradation. In contrast, dispersal networks facilitated bacterial movement at ΔΨo and ΔΨm values between 0 and -0.5 MPa and thus improved the absolute biodegradation performance by up to 52 and 119% for ΔΨo and ΔΨm, respectively. This strong functional interrelationship was further emphasized by a high positive correlation between population dispersal, population growth, and degradation. We propose that dispersal networks may sustain the functionality of microbial ecosystems at low osmotic and matric potentials.