The contrasting effects of fluctuating temperature on bacterial diversity and performances in temperate and subtropical soils.

The extremely high species diversity of soil bacterial community has fascinated and puzzled community ecologists. Although theory predicts that fluctuations in environments can facilitate diversity maintenance, the effects of fluctuating temperature on species diversity have rarely been investigated in species-rich microbial communities. Here, we examined whether fluctuating temperature had positive effects on species diversity relative to constant temperatures in soil bacterial communities, and investigated the effects of fluctuating temperature on bacterial performances (changes in relative abundance). We performed a temperature manipulation experiment with soils collected from temperate and subtropical zones, where the soils were subjected to constant high, low or fluctuating temperatures. We found that fluctuating temperatures showed significant positive effects on species diversity. The time-averaged effect of fluctuating temperatures (i.e., averaging out the differences between species in their environment-dependent performances) appeared to delay species loss in both the temperate and the subtropical communities. In addition, we found that the performances of temperature-responsive species at fluctuating temperatures significantly deviated from their time-weighted average performances at constant high and low temperatures, which was defined as fluctuation-dependent effects in our study. Intriguingly, fluctuation-dependent effects beyond time-averaged effect led to an opposite trend: differences in temperature-responsive species' performances decreased in the temperate communities, but increased in the subtropical communities. Our findings provide new insights into diversity maintenance in soil bacterial communities, and imply that the effects of fluctuating temperature on species diversity in soil bacterial community might vary across latitude.

Seasonal Climate Variations Promote Bacterial α-Diversity in Soil.

Ecological theory suggests that temporal environmental fluctuations can contribute greatly to diversity maintenance. Given bacteria's short generation time and rapid responses to environmental change, seasonal climate fluctuations are very likely to play an important role in maintaining the extremely high α-diversity of soil bacterial community, which has been unfortunately neglected in previous studies. Here, with in-depth analyses of two previously published soil bacterial datasets at global scale, we found that soil bacterial α-diversity was positively correlated with both seasonal variations of temperature and precipitation. Furthermore, piecewise structural equation models showed that seasonal variations of temperature or precipitation had weak but significant positive effect on soil bacterial α-diversity in each dataset. However, it is noteworthy that the importance of seasonal climate variations might be underestimated in the above analyses, due to the potential confounding factors (such as vegetation type) and the lack of sampling across seasons. As a supplement, we analyzed a previously published wheat cropland dataset with samples collected in both winter and the following summer across North China Plain. As expected, bacterial α-diversity was positively correlated with seasonal climate variations in the cropland dataset, and climate seasonality explained a larger proportion of variations in bacterial α-diversity. Collectively, these findings implied that fluctuation-dependent mechanisms of diversity maintenance presumably operate in soil bacterial communities. Based on existing evidence, we speculated that the storage effect may be the main mechanism responsible for diversity maintenance in soil bacterial community, but rigorous experimental tests are needed in the future.

Field experimental evidence that stochastic processes predominate in the initial assembly of bacterial communities.

To assess the relative importance of environmental selection, dispersal and stochastic processes in structuring ecological communities, we conducted a bacterial community assembly experiment using microcosms filled with sterile liquid medium under field conditions in the Inner Mongolian grasslands. Multiple replicate microcosms containing different carbon substrates were placed at nine locations across three spatial scales (10, 300 and 10 000 m distance between locations) in such a way that the environment of microcosms varies independently of the geographical distance. The operational taxonomic units within the experimental communities were assessed via the terminal restriction fragment length polymorphism techniques on the 10th and 17th days after the onset of the experiment. We found no evidence of distance decay in community similarity, and communities within a given location were more similar to each other regardless of environment than communities at other locations within the same spatial scale. Variance partitioning indicated that location explained more compositional variation in microbial communities than environment, particularly on the 17th day, despite that environment and location in combination could only explain less than half of the total variation. These results suggest that bacterial dispersal is not limited by distance in this experiment, and community assembly in microcosms is not environmentally determined but governed by stochastic processes.

Evolutionary rescue can be impeded by temporary environmental amelioration.

Rapid evolutionary adaptation has the potential to rescue from extinction populations experiencing environmental changes. Little is known, however, about the impact of short-term environmental fluctuations during long-term environmental deterioration, an intrinsic property of realistic environmental changes. Temporary environmental amelioration arising from such fluctuations could either facilitate evolutionary rescue by allowing population recovery (a positive demographic effect) or impede it by relaxing selection for beneficial mutations required for future survival (a negative population genetic effect). We address this uncertainty in an experiment with populations of a bacteriophage virus that evolved under deteriorating conditions (gradually increasing temperature). Periodic environmental amelioration (short periods of reduced temperature) caused demographic recovery during the early phase of the experiment, but ultimately reduced the frequency of evolutionary rescue. These experimental results suggest that environmental fluctuations could reduce the potential of evolutionary rescue.

Microbial biogeography of acid mine drainage sediments at a regional scale across southern China.

Investigations of microbial biogeography in extreme environments provide unique opportunities to disentangle the roles of environment and space in microbial community assembly. Here, we reported a comprehensive microbial biogeographic survey of 90 acid mine drainage (AMD) sediment samples from 18 mining sites of various mineral types across southern China. We found that environmental selection was strong in determining the AMD habitat species pool. However, microbial alpha diversity was primarily explained by mining sites rather than environmental factors, and microbial beta diversity correlated more strongly with geographic than environmental distance at both large and small spatial scales. Particularly, the presence/absence of widespread AMD habitat generalists was only correlated with geographic distance and independent of environmental variation. These distance-decay patterns suggested that spatial processes played a more important role in determining microbial compositional variation across space; which could be explained by the reinforced impacts of dispersal limitation in less fluid, spatially structured sediment habitat with diverse pre-existing communities. In summary, our findings suggested that the deterministic assembling and spatial constraints interact to shape microbial biogeography in AMD sediments; and provided implications that spatial processes should be considered when predicting microbial dynamics in response to severe environmental change across large spatial scales.

Local biotic interactions drive species-specific divergence in soil bacterial communities.

It is well accepted that environmental heterogeneity and dispersal are key factors determining soil bacterial community composition, yet little is known about the role of local biotic interactions. Here we address this issue with an abundance-manipulation experiment that was conducted in a semiarid grassland. We manually increased the abundance of six randomly chosen resident bacterial species in separate, closed, communities and allowed the communities to recover in situ for 1 year. The single episode of increase in the abundance of different species drove species-specific community divergence accompanied by a decline in local diversity. Four of the six added species caused a decrease in the abundance of their closely related species, suggesting an important role of interspecific competition in driving the observed community divergence. Our results also suggested a lack of effective population regulations to force the relative abundance of manipulated species to revert to original level, which would allow persistence of the divergence among soil bacterial communities. We concluded that biotic interactions were important in determining soil bacterial community composition, which could result in substantial variation in soil bacterial community composition in abiotically homogenous environment.

Stability of A Coevolving Host-parasite System Peaks at Intermediate Productivity.

Habitat productivity may affect the stability of consumer-resource systems, through both ecological and evolutionary mechanisms. We hypothesize that coevolving consumer-resource systems show more stable dynamics at intermediate resource availability, while very low-level resource supply cannot support sufficiently large populations of resource and consumer species to avoid stochastic extinction, and extremely resource-rich environments may promote escalatory arms-race-like coevolution that can cause strong fluctuations in species abundance and even extinction of one or both trophic levels. We tested these ideas by carrying out an experimental evolution study with a model bacterium-phage system (Pseudomonas fluorescens SBW25 and its phage SBW25Φ2). Consistent with our hypothesis, this system was most stable at intermediate resource supply (fewer extinction events and smaller magnitude of population fluctuation). In our experiment, the rate of coevolution between bacterial resistance and phage infectivity was correlated with the magnitude of population fluctuation, which may explain the different in stability between levels of resource supply. Crucially, our results are consistent with a suggestion that, among the two major modes of antagonistic coevolution, arms race is more likely than fluctuation selection dynamics to cause extinction events in consumer-resource systems. This study suggests an important role of environment-dependent coevolutionary dynamics for the stability of consumer-resource species systems, therefore highlights the importance to consider contemporaneous evolutionary dynamics when studying the stability of ecosystems, particularly those under environmental changes.

The role of late-acting self-incompatibility and early-acting inbreeding depression in governing female fertility in monkshood, Aconitum kusnezoffii.

Reduced seed yields following self-pollination have repeatedly been observed, but the underlying mechanisms remain elusive when self-pollen tubes can readily grow into ovaries, because pre-, post-zygotic late-acting self-incompatibility (LSI), or early-acting inbreeding depression (ID) can induce self-sterility. The main objective of this study was to differentiate these processes in Aconitum kusnezoffii, a plant lacking stigmatic or stylar inhibition of self-pollination. We performed a hand-pollination experiment in a natural population of A. kusnezoffii, compared seed set among five pollination treatments, and evaluated the distribution of seed size and seed set. Embryonic development suggested fertilization following self-pollination. A partial pre-zygotic LSI was suggested to account for the reduced seed set by two lines of evidence. The seed set of chase-pollination treatment significantly exceeded that of self-pollination treatment, and the proportion of unfertilized ovules was the highest following self-pollination. Meanwhile, early-acting ID, rather than post-zygotic LSI, was suggested by the findings that the size of aborted selfed seeds varied continuously and widely; and the selfed seed set both exhibited a continuous distribution and positively correlated with the crossed seed set. These results indicated that the embryos were aborted at different stages due to the expression of many deleterious alleles throughout the genome during seed maturation. No signature of post-zygotic LSI was found. Both partial pre-zygotic LSI and early-acting ID contribute to the reduction in selfed seed set in A. kusnezoffii, with pre-zygotic LSI rejecting part of the self-pollen and early-acting ID aborting part of the self-fertilized seeds.