Mercè Berga

Fundamentals of microbial community resistance and resilience.

Microbial communities are at the heart of all ecosystems, and yet microbial community behavior in disturbed environments remains difficult to measure and predict. Understanding the drivers of microbial community stability, including resistance (insensitivity to disturbance) and resilience (the rate of recovery after disturbance) is important for predicting community response to disturbance. Here, we provide an overview of the concepts of stability that are relevant for microbial communities. First, we highlight insights from ecology that are useful for defining and measuring stability. To determine whether general disturbance responses exist for microbial communities, we next examine representative studies from the literature that investigated community responses to press (long-term) and pulse (short-term) disturbances in a variety of habitats. Then we discuss the biological features of individual microorganisms, of microbial populations, and of microbial communities that may govern overall community stability. We conclude with thoughts about the unique insights that systems perspectives – informed by meta-omics data – may provide about microbial community stability.

Temporal variation of β-diversity and assembly mechanisms in a bacterial metacommunity

The turnover of community composition across space, β-diversity, is influenced by different assembly mechanisms, which place varying weight on local habitat factors, such as environmental conditions and species interactions, and regional factors such as dispersal and history. Several assembly mechanisms may function simultaneously; however, little is known about how their importance changes over time and why. Here, we implemented a field survey where we sampled a bacterial metacommunity consisting of 17 rock pools located at the Swedish Baltic Sea coast at 11 occasions during 1 year. We determined to which extent communities were structured by different assembly mechanisms using variation partitioning and studied changes in β-diversity across environmental gradients over time. β-Diversity was highest at times of high overall productivity and environmental heterogeneity in the metacommunity, at least partly due to species sorting, that is, selection of taxa by the prevailing environmental conditions. In contrast, dispersal-driven assembly mechanisms were primarily detected at times when β-diversity was relatively low. There were no indications for strong and persistent differences in community composition or β-diversity between permanent and temporary pools, indicating that the physical disturbance regime is of relatively minor importance. In summary, our study clearly suggests that there are temporal differences in the relative importance of different assembly mechanisms related to abiotic factors and shows that the temporal variability of those factors is important for a more complete understanding of bacterial metacommunity dynamics.

Effects of Disturbance Intensity and Frequency on Bacterial Community Composition and Function

Disturbances influence community structure and ecosystem functioning. Bacteria are key players in ecosystems and it is therefore crucial to understand the effect of disturbances on bacterial communities and how they respond to them, both compositionally and functionally. The main aim of this study was to test the effect of differences in disturbance strength on bacterial communities. For this, we implemented two independent short-term experiments with dialysis bags containing natural bacterial communities, which were transplanted between ambient and ‘disturbed’ incubation tanks, manipulating either the intensity or the frequency of a salinity disturbance. We followed changes in community composition by terminal restriction fragment analysis (T-RFLP) and measured various community functions (bacterial production, carbon substrate utilization profiles and rates) directly after and after a short period of recovery under ambient conditions. Increases in disturbance strength resulted in gradually stronger changes in bacterial community composition and functions. In the disturbance intensity experiment, the sensitivity to the disturbance and the ability of recovery differed between different functions. In the disturbance frequency experiment, effects on the different functions were more consistent and recovery was not observed. Moreover, in case of the intensity experiment, there was also a time lag in the responses of community composition and functions, with functional responses being faster than compositional ones. To summarize, our study shows that disturbance strength has the potential to change the functional performance and composition of bacterial communities. It further highlights that the overall effects, rates of recovery and the degree of congruence in the response patterns of community composition and functioning along disturbance gradients depend on the type of function and the character of the disturbance.

Mechanisms determining the fate of dispersed bacterial communities in new environments

Recent work has shown that dispersal has an important role in shaping microbial communities. However, little is known about how dispersed bacteria cope with new environmental conditions and how they compete with local resident communities. To test this, we implemented two full-factorial transplant experiments with bacterial communities originating from two sources (freshwater or saline water), which were incubated, separately or in mixes, under both environmental conditions. Thus, we were able to separately test for the effects of the new environment with and without interactions with local communities. We determined community composition using 454-pyrosequencing of bacterial 16S rRNA to specifically target the active fraction of the communities, and measured several functional parameters. In absence of a local resident community, the net functional response was mainly affected by the environmental conditions, suggesting successful functional adaptation to the new environmental conditions. Community composition was influenced both by the source and the incubation environment, suggesting simultaneous effects of species sorting and functional plasticity. In presence of a local resident community, functional parameters were higher compared with those expected from proportional mixes of the unmixed communities in three out of four cases. This was accompanied by an increase in the relative abundance of generalists, suggesting that competitive interactions among local and immigrant taxa could explain the observed ‘functional overachievement’. In summary, our results suggest that environmental filtering, functional plasticity and competition are all important mechanisms influencing the fate of dispersed communities.

The spatial structure of bacterial communities is influenced by historical environmental conditions

The spatial structure of ecological communities, including that of bacteria, is often influenced by species sorting by contemporary environmental conditions. Moreover, historical processes, i.e., ecological and evolutionary events that have occurred at some point in the past, such as dispersal limitation, drift, priority effects, or selection by past environmental conditions, can be important, but are generally investigated much less. Here, we conducted a field study using 16 rock pools, where we specifically compared the importance of past vs. contemporary environmental conditions for bacterial community structure by correlating present differences in bacterial community composition among pools to environmental conditions measured on the same day, as well as to those measured 2, 4, 6, and 8 d earlier. The results prove that selection by past environmental conditions exists, since we were able to show that bacterial communities are, to a greater extent, an imprint of past compared to contemporary environmental conditions. We suggest that this is the result of a combination of different mechanisms, including priority effects that cause rapid adaptation to new environmental conditions of taxa that have been initially selected by past environmental conditions, and slower rates of turnover in community composition compared to environmental conditions.

Combined effects of zooplankton grazing and dispersal on the diversity and assembly mechanisms of bacterial metacommunities

Effects of dispersal and the presence of predators on diversity, assembly and functioning of bacterial communities are well studied in isolation. In reality, however, dispersal and trophic interactions act simultaneously and can therefore have combined effects, which are poorly investigated. We performed an experiment with aquatic metacommunities consisting of three environmentally different patches and manipulated dispersal rates among them as well as the presence or absence of the keystone species Daphnia magna. Daphnia magna reduced both local and regional diversity, whereas dispersal increased local diversity but decreased beta-diversity having no net effect on regional diversity. Dispersal modified the assembly mechanisms of bacterial communities by increasing the degree of determinism. Additionally, the combination of the D. magna and dispersal increased the importance of deterministic processes, presumably because predator-tolerant taxa were spread in the metacommunity via dispersal. Moreover, the presence of D. magna affected community composition, increased community respiration rates but did not affect bacterial production or abundance, whereas dispersal slightly increased bacterial production. In conclusion, our study suggests that predation by a keystone species such as D. magna and dispersal additively influence bacterial diversity, assembly processes and ecosystem functioning.

Effects of Dispersal and Initial Diversity on the Composition and Functional Performance of Bacterial Communities.

Natural communities are open systems and consequently dispersal can play an important role for the diversity, composition and functioning of communities at the local scale. It is, however, still unclear how effects of dispersal differ depending on the initial diversity of local communities. Here we implemented an experiment where we manipulated the initial diversity of natural freshwater bacterioplankton communities using a dilution-to-extinction approach as well as dispersal from a regional species pool. The aim was further to test whether dispersal effects on bacterial abundance and functional parameters (average community growth rates, respiration rates, substrate utilisation ability) differ in dependence of the initial diversity of the communities. First of all, we found that both initial diversity and dispersal rates had an effect on the recruitment of taxa from a regional source, which was higher in communities with low initial diversity and at higher rates of dispersal. Higher initial diversity and dispersal also promoted higher levels of richness and evenness in local communities and affected, both, separately or interactively, the functional performance of communities. Our study therefore suggests that dispersal can influence the diversity, composition and functioning of bacterial communities and that this effect may be enhanced if the initial diversity of communities is depleted.

Contribution of different bacterial dispersal sources to lakes : Population and community effects in different seasons

Summary The diversity and composition of lake bacterial communities are driven by the interplay between local contemporary environmental conditions and dispersal of cells from the surroundings, i.e. the metacommunity. Still, a conceptual understanding of the relative importance of the two types of factors is lacking. For instance, it is unknown which sources of dispersal are most important and under which circumstances. Here, we investigated the seasonal variation in the importance of dispersal from different sources (mixing, precipitation, surface runoff and sediment resuspension) for lake bacterioplankton community and population dynamics. For that purpose, two small forest lakes and their dispersal sources were sampled over a period of 10 months. The influence of dispersal on communities and populations was determined by 454 sequencing of the 16S rRNA gene and SourceTracker analysis. On the community level direct effects of dispersal were questionable from all sources. Instead we found that the community of the preceding sampling occasion, representing growth of resident bacteria, was of great importance. On the population level, however, dispersal of individual taxa from the inlet could be occasionally important even under low water flow. The effect of sediment resuspension and precipitation appeared small.

Contribution of different dispersal sources to the metabolic response of lake bacterioplankton following a salinity change

Dispersal can modify how bacterial community composition (BCC) changes in response to environmental perturbations, yet knowledge about the functional consequences of dispersal is limited. Here we hypothesized that changes in bacterial community production in response to a salinity disturbance depend on the possibility to recruit cells from different dispersal sources. To investigate this, we conducted an in situ mesocosm experiment where bacterial communities of an oligotrophic lake were exposed to different salinities (0, 18, 36 psu) for 2 weeks and subjected to dispersal of cells originating from sediments, air (mesocosms open to air deposition), both or none. BCC was determined using 454 pyrosequencing of the 16S rRNA gene and bacterial production was measured by 3 H leucine uptake. Bacterial production differed significantly among salinity treatments and dispersal treatments, being highest at high salinity. These changes were associated with changes in BCC and it was found that the identity of the main functional contributors differed at different salinities. Our results further showed that after a salinity perturbation, the response of bacterial communities depended on the recruitment of taxa, including marine representatives (e.g., Alphaproteobacteria Loktanella, Erythrobacter and the Gammaproteobacterium Rheiheimera) from dispersal sources, in which atmospheric deposition appeared to play a major role.

Functional and Compositional Stability of Bacterial Metacommunities in Response to Salinity Changes

Disturbances and environmental change are important factors determining the diversity, composition, and functioning of communities. However, knowledge about how natural bacterial communities are affected by such perturbations is still sparse. We performed a whole ecosystem manipulation experiment with freshwater rock pools where we applied salinity disturbances of different intensities. The aim was to test how the compositional and functional resistance and resilience of bacterial communities, alpha- and beta-diversity and the relative importance of stochastic and deterministic community assembly processes changed along a disturbance intensity gradient. We found that bacterial communities were functionally resistant to all salinity levels (3, 6, and 12 psu) and compositionally resistant to a salinity increase to 3 psu and resilient to increases of 6 and 12 psu. Increasing salinities had no effect on local richness and evenness, beta-diversity and the proportion of deterministically vs. stochastically assembled communities. Our results show a high functional and compositional stability of bacterial communities to salinity changes of different intensities both at local and regional scales, which possibly reflects long-term adaptation to environmental conditions in the study system.