Microbial population dynamics and evolutionary outcomes under extreme energy limitation.

Microorganisms commonly inhabit energy-limited ecosystems where cellular maintenance and reproduction is highly constrained. To gain insight into how individuals persist under such conditions, we derived demographic parameters from a collection of 21 heterotrophic bacterial taxa by censusing 100 populations in an effectively closed system for 1,000 d. All but one taxon survived prolonged resource scarcity, yielding estimated times to extinction ranging over four orders of magnitude from 100 to 105 y. Our findings corroborate reports of long-lived bacteria recovered from ancient environmental samples, while providing insight into mechanisms of persistence. As death rates declined over time, lifespan was extended through the scavenging of dead cells. Although reproduction was suppressed in the absence of exogenous resources, populations continued to evolve. Hundreds of mutations were acquired, contributing to genome-wide signatures of purifying selection as well as molecular signals of adaptation. Consistent ecological and evolutionary dynamics indicate that distantly related bacteria respond to energy limitation in a similar and predictable manner, which likely contributes to the stability and robustness of microbial life.

Optimal dormancy strategies in fluctuating environments given delays in phenotypic switching.

Organisms have evolved different mechanisms in response to periods of environmental stress, including dormancy - a reversible state of reduced metabolic activity. Transitions to and from dormancy can be random or induced by changes in environmental conditions. Prior theoretical work has shown that stochastic transitioning between active and dormant states at the individual level can maximize fitness at the population level. However, such theories of 'bet-hedging' strategies typically neglect certain physiological features of transitions to dormancy, including time lags to gain protective benefits. Here, we construct and analyze a dynamic model that couples stochastic changes in environmental state with the population dynamics of organisms that can initiate dormancy after an explicit time delay. Stochastic environments are simulated using a multi-state Markov chain through which the mean and variance of environmental residence time can be adjusted. In the absence of time lags (or in the limit of very short lags), we find that bet-hedging strategy transition probabilities scale inversely with the mean environmental residence times, consistent with prior theory. We also find that increasing delays in dormancy decreases optimal transitioning probabilities, an effect that can be influenced by the correlations of environmental noise. When environmental residence times - either good or bad - are uncorrelated, the maximum population level fitness is obtained given low levels of transitioning between active and dormant states. However when environmental residence times are correlated, optimal dormancy initiation and termination probabilities increase insofar as the mean environmental persistent time is longer than the delay to reach dormancy. We also find that bet hedging is no longer advantageous when delays to enter dormancy exceed the mean environmental residence times. Altogether, these results show how physiological limits to dormancy and environmental dynamics shape the evolutionary benefits and even viability of bet hedging strategies at population scales.

Molecular Evolutionary Dynamics of Energy Limited Microorganisms.

Microorganisms have the unique ability to survive extended periods of time in environments with extremely low levels of exploitable energy. To determine the extent that energy limitation affects microbial evolution, we examined the molecular evolutionary dynamics of a phylogenetically diverse set of taxa over the course of 1,000 days. We found that periodic exposure to energy limitation affected the rate of molecular evolution, the accumulation of genetic diversity, and the rate of extinction. We then determined the degree that energy limitation affected the spectrum of mutations as well as the direction of evolution at the gene level. Our results suggest that the initial depletion of energy altered the direction and rate of molecular evolution within each taxon, though after the initial depletion the rate and direction did not substantially change. However, this consistent pattern became diminished when comparisons were performed across phylogenetically distant taxa, suggesting that although the dynamics of molecular evolution under energy limitation are highly generalizable across the microbial tree of life, the targets of adaptation are specific to a given taxon.

Microbial and Environmental Processes Shape the Link between Organic Matter Functional Traits and Composition.

Dissolved organic matter (DOM) is a large and complex mixture of molecules that fuels microbial metabolism and regulates biogeochemical cycles. Individual DOM molecules have unique functional traits, but how their assemblages vary deterministically under global change remains poorly understood. Here, we examine DOM and associated bacteria in 300 aquatic microcosms deployed on mountainsides that span contrasting temperatures and nutrient gradients. Based on molecular trait dimensions of reactivity and activity, we partition the DOM composition into labile-active, recalcitrant-active, recalcitrant-inactive, and labile-inactive fractions and quantify the relative influences of deterministic and stochastic processes governing the assembly of each. At both subtropical and subarctic study sites, the assembly of labile or recalcitrant molecules in active fractions is primarily governed by deterministic processes, while stochastic processes are more important for the assembly of molecules within inactive fractions. Surprisingly, the importance of deterministic selection increases with global change gradients for recalcitrant molecules in both active and inactive fractions, and this trend is paralleled by changes in the deterministic assembly of microbial communities and environmental filtering, respectively. Together, our results highlight the shift in focus from potential reactivity to realized activity and indicate that active and inactive fractions of DOM assemblages are structured by contrasting processes, and their recalcitrant components are consistently sensitive to global change. Our study partitions the DOM molecular composition across functional traits and links DOM with microbes via a shared ecological framework of assembly processes. This integrated approach opens new avenues to understand the assembly and turnover of organic carbon in a changing world.

Stabilising role of seed banks and the maintenance of bacterial diversity.

Coexisting species often exhibit negative frequency dependence due to mechanisms that promote population growth and persistence when rare. These stabilising mechanisms can maintain diversity through interspecific niche differences, but also through life-history strategies like dormancy that buffer populations in fluctuating environments. However, there are few tests demonstrating how seed banks contribute to long-term community dynamics and the maintenance of diversity. Using a multi-year, high-frequency time series of bacterial community data from a north temperate lake, we documented patterns consistent with stabilising coexistence. Bacterial taxa exhibited differential responses to seasonal environmental conditions, while seed bank dynamics helped maintain diversity over less-favourable winter periods. Strong negative frequency dependence in rare, but metabolically active, taxa suggested a role for biotic interactions in promoting coexistence. Together, our results provide field-based evidence that niche differences and seed banks contribute to recurring community dynamics and the long-term maintenance of diversity in nature.

Resuscitation of the microbial seed bank alters plant-soil interactions.

While microorganisms are recognized for driving belowground processes that influence the productivity and fitness of plant populations, the vast majority of bacteria and fungi in soil belong to a seed bank consisting of dormant individuals. However, plant performance may be affected by microbial dormancy through its effects on the activity, abundance, and diversity of soil microorganisms. To test how microbial seed banks influence plant-soil interactions, we purified recombinant resuscitation promoting factor (Rpf), a bacterial protein that terminates dormancy. In a factorially designed experiment, we then applied the Rpf to soil containing field mustard (Brassica rapa), an agronomically important plant species. Plant biomass was ~33% lower in the Rpf treatment compared to plants grown with an unmanipulated microbial seed bank. In addition, Rpf reduced soil respiration, decreased bacterial abundance, and increased fungal abundance. These effects of Rpf on plant performance were accompanied by shifts in bacterial community composition, which may have diluted mutualists or resuscitated pathogens. Our findings suggest that changes in microbial seed banks may influence the magnitude and direction of plant-soil feedbacks in ways that affect above- and belowground biodiversity and function.

Peatland microbial community responses to plant functional group and drought are depth-dependent.

Peatlands store one-third of Earth's soil carbon, the stability of which is uncertain due to climate change-driven shifts in hydrology and vegetation, and consequent impacts on microbial communities that mediate decomposition. Peatland carbon cycling varies over steep physicochemical gradients characterizing vertical peat profiles. However, it is unclear how drought-mediated changes in plant functional groups (PFGs) and water table (WT) levels affect microbial communities at different depths. We combined a multiyear mesocosm experiment with community sequencing across a 70-cm depth gradient, to test the hypotheses that vascular PFGs (Ericaceae vs. sedges) and WT (high vs. low) structure peatland microbial communities in depth-dependent ways. Several key results emerged. (i) Both fungal and prokaryote (bacteria and archaea) community structure shifted with WT and PFG manipulation, but fungi were much more sensitive to PFG whereas prokaryotes were much more sensitive to WT. (ii) PFG effects were largely driven by Ericaceae, although sedge effects were evident in specific cases (e.g., methanotrophs). (iii) Treatment effects varied with depth: the influence of PFG was strongest in shallow peat (0-10, 10-20 cm), whereas WT effects were strongest at the surface and middle depths (0-10, 30-40 cm), and all treatment effects waned in the deepest peat (60-70 cm). Our results underline the depth-dependent and taxon-specific ways that plant communities and hydrologic variability shape peatland microbial communities, pointing to the importance of understanding how these factors integrate across soil profiles when examining peatland responses to climate change.

Microbial community assembly in a multi-layer dendritic metacommunity.

A major goal of metacommunity ecology is to infer the local- and regional-scale processes that underlie community assembly. In dendritic ecological networks, branching patterns and directional flow can alter the balance between local and regional factors during assembly. Vertical habitat structure may further affect community assembly in dendritic metacommunities. In this study, we analyzed the bacterial metacommunity of a fifth-order mountain stream network to assess differences in community assembly (1) between planktonic and benthic habitats, (2) across spatial scales, and (3) between headwater and downstream regions of the network. Using taxonomic and phylogenetic null modeling, we found habitat-specific spatial patterns of community assembly across the dendritic network. Compositional differences between planktonic and benthic communities were maintained by variable selection, but we also found evidence of local dispersal limitation between the two habitats. Planktonic community assembly was scale dependent, transitioning from homogeneous selection at local scales to variable selection at regional scales, while benthic community assembly was less scale dependent. Variable selection structured headwaters in both habitat types, but downstream communities were primarily structured by homogeneous selection, especially in sediments. Taken together, our results show that vertical habitat structure contributes to the scale-dependent processes of community assembly across the dendritic metacommunity.

Trait-based approach to bacterial growth efficiency.

Bacterial growth efficiency (BGE) is the proportion of assimilated carbon that is converted into biomass and reflects the balance between growth and energetic demands. Often measured as an aggregate property of the community, BGE is highly variable within and across ecosystems. To understand this variation, we first identified how species identity and resource type affect BGE using 20 bacterial isolates belonging to the phylum Proteobacteria that were enriched from north temperate lakes. Using a trait-based approach that incorporated genomic and phenotypic information, we characterized the metabolism of each isolate and tested for predicted trade-offs between growth rate and efficiency. A substantial amount of variation in BGE could be explained at broad (i.e., order, 20%) and fine (i.e., strain, 58%) taxonomic levels. While resource type was a relatively weak predictor across species, it explained >60% of the variation in BGE within a given species. A metabolic trade-off (between maximum growth rate and efficiency) and genomic features revealed that BGE may be a species-specific metabolic property. Our study suggests that genomic and phylogenetic information may help predict aggregate microbial community functions like BGE and the fate of carbon in ecosystems.

Low costs of adaptation to dietary restriction.

Dietary restriction (DR) is the most successful and widespread means of extending organismal lifespan. However, the evolutionary basis of life extension under DR remains uncertain. The traditional evolutionary explanation is that when organisms experience DR, they allocate endogenous resources to survival and postpone reproduction until conditions improve. However, this life-extension strategy should be maladaptive if DR continues for multiple generations due to trade-offs between longevity and reproduction. To test this prediction, we subjected the budding yeast Saccharomyces cerevisiae to 1800 generations of evolution on restricted versus non-restricted diets. Adaptation to a non-restricted diet improved reproductive fitness by 57%, but provided a much smaller (14%) advantage on a restricted diet. By contrast, adaptation to DR resulted in an approximately 35% increase in reproductive fitness on both restricted and non-restricted diets. Importantly, the life-extending effect of DR did not decrease following long-term evolution on the restricted diet. Thus, contrary to theoretical expectations, we found no evidence that the life-extending DR response became maladaptive during multigenerational DR. Together, our results suggest that the DR response has a low cost and that this phenomenon may have evolved as part of a generalist strategy that extends beyond the benefits of postponing reproduction.

Nutrient stoichiometry shapes microbial coevolution.

Coevolution is a force contributing to the generation and maintenance of biodiversity. It is influenced by environmental conditions including the scarcity of essential resources, which can drive the evolution of defence and virulence traits. We conducted a long-term chemostat experiment where the marine cyanobacterium Synechococcus was challenged with a lytic phage under nitrogen (N) or phosphorus (P) limitation. This manipulation of nutrient stoichiometry altered the stability of host-parasite interactions and the underlying mode of coevolution. By assessing the infectivity with > 18 000 pairwise challenges, we documented directional selection for increased phage resistance, consistent with arms-race dynamics while phage infectivity fluctuated through time, as expected when coevolution is driven by negative frequency-dependent selection. The resulting infection networks were 50% less modular under N- versus P-limitation reflecting host-range contraction and asymmetric coevolutionary trajectories. Nutrient stoichiometry affects eco-evolutionary feedbacks in ways that may alter the dynamics and functioning of environmental and host-associated microbial communities.

A Residence Time Theory for Biodiversity.

From microorganisms to the largest macroorganisms, much of Earth's biodiversity is subject to forces of physical turnover. Residence time is the ratio of an ecosystem's size to its rate of flow and provides a means for understanding the influence of physical turnover on biological systems. Despite its use across scientific disciplines, residence time has not been integrated into the broader understanding of biodiversity, life history, and the assembly of ecological communities. Here we propose a residence time theory for the growth, activity, abundance, and diversity of traits and taxa in complex ecological systems. Using thousands of stochastic individual-based models to simulate energetically constrained life-history processes, we show that our predictions are conceptually sound and mutually compatible and that they support ecological relationships that underpin much of biodiversity theory. We discuss the importance of residence time across the ecological hierarchy and propose how residence time can be integrated into theories ranging from population genetics to macroecology.

Dormancy in Metacommunities.

Although metacommunity ecology has improved our understanding of how dispersal affects community structure and dynamics across spatial scales, it has yet to adequately account for dormancy. Dormancy is a reversible state of reduced metabolic activity that enables temporal dispersal within the metacommunity. Dormancy is also a metacommunity-level process because it can covary with spatial dispersal and affect diversity across spatial scales. We develop a framework to integrate dispersal and dormancy, focusing on the covariation they exhibit, to predict how dormancy modifies the importance of species interactions, dispersal, and historical contingencies in metacommunities. We used empirical and modeling approaches to demonstrate the utility of this framework. We examined case studies of microcrustaceans in ephemeral ponds, where dormancy underlies metacommunity dynamics, and identified constraints on the dispersal and dormancy strategies of bromeliad-dwelling invertebrates. Using simulations, we showed that dormancy can alter classic metacommunity patterns of diversity in ways that depend on dispersal-dormancy covariation and spatiotemporal environmental variability. We propose that dormancy may also facilitate evolution-mediated priority effects if locally adapted seed banks prevent colonization by more dispersal-limited species. Last, we present testable predictions for the implications of dormancy in metacommunities, some of which may fundamentally alter our understanding of metacommunity ecology.

Scaling laws predict global microbial diversity.

Scaling laws underpin unifying theories of biodiversity and are among the most predictively powerful relationships in biology. However, scaling laws developed for plants and animals often go untested or fail to hold for microorganisms. As a result, it is unclear whether scaling laws of biodiversity will span evolutionarily distant domains of life that encompass all modes of metabolism and scales of abundance. Using a global-scale compilation of ∼35,000 sites and ∼5.6⋅10(6) species, including the largest ever inventory of high-throughput molecular data and one of the largest compilations of plant and animal community data, we show similar rates of scaling in commonness and rarity across microorganisms and macroscopic plants and animals. We document a universal dominance scaling law that holds across 30 orders of magnitude, an unprecedented expanse that predicts the abundance of dominant ocean bacteria. In combining this scaling law with the lognormal model of biodiversity, we predict that Earth is home to upward of 1 trillion (10(12)) microbial species. Microbial biodiversity seems greater than ever anticipated yet predictable from the smallest to the largest microbiome.

A trait-based approach to bacterial biofilms in soil.

A trait-based approach focuses on attributes of taxa that influence the structure and function of communities. Biofilm production is a common trait among microorganisms in a wide range of environmental, engineered, and host-associated ecosystems. Here, we used Pseudomonas aeruginosa to link biofilm production to moisture availability, a common stressor for microorganisms in soil. First, we demonstrate that biofilm production is a response trait that influences the desiccation phenotype by increasing survivorship, shifting the niche space, and reducing the minimum water potential needed to sustain a net-positive growth rate (Ψ*). Although the allocation of resources to biofilms is thought to be costly, we found no evidence for a trade-off between fitness and biofilm production along a soil moisture gradient. Second, we demonstrated that biofilm production is an effect trait. Specifically, biofilm production increased water retention in soils that were exposed to a series of drying and rewetting cycles. Although this form of niche construction should affect species interactions, we found no evidence that the benefits of biofilm production were extended to another co-occurring soil bacterium. Together, our results support the view that biofilm production is an important trait that may contribute to the distribution, abundance, and functioning of microorganisms in soils.

Species sorting along a subsidy gradient alters bacterial community stability.

The movement of resources between terrestrial and aquatic habitats has strong effects on ecological processes in recipient ecosystems. Allochthonous inputs modify the quality and quantity of the available resource pool in ways that may alter the composition and stability of recipient communities. Inputs of terrestrial dissolved organic carbon (tDOC) into aquatic ecosystems represent a large influx of resources that has the potential to affect local communities, especially microorganisms. To evaluate the effects of terrestrial inputs on aquatic bacterial community composition and stability, we manipulated the supply rate of tDOC to a set of experimental ponds. Along the tDOC supply gradient, we measured changes in diversity and taxon-specific changes in relative abundance and activity. We then determined community stability by perturbing each pond using a pulse of inorganic nutrients and measuring changes in composition and activity (i.e., responsiveness) along the gradient. Terrestrial DOC supply significantly altered the composition of the active bacterial community. The composition of the active bacterial community changed via decreases in richness and evenness as well as taxon-specific changes in relative abundance and activity indicating species sorting along the gradient. Likewise, the responsiveness of the active bacterial community decreased along the gradient, which led to a more stable active community. We did not, however, observe these changes in diversity and stability in the total community (i.e., active and inactive organisms), which suggests that tDOC supply modifies bacterial community stability through functional not structural changes. Together, these results show that altered aquatic terrestrial linkages can have profound effects on the activity and stability of the base of the food web and thus can alter ecosystem functioning.

Rapid responses of soil microorganisms improve plant fitness in novel environments.

Global change is challenging plant and animal populations with novel environmental conditions, including increased atmospheric CO(2) concentrations, warmer temperatures, and altered precipitation regimes. In some cases, contemporary or "rapid" evolution can ameliorate the effects of global change. However, the direction and magnitude of evolutionary responses may be contingent upon interactions with other community members that also are experiencing novel environmental conditions. Here, we examine plant adaptation to drought stress in a multigeneration experiment that manipulated aboveground-belowground feedbacks between plants and soil microbial communities. Although drought stress reduced plant growth and accelerated plant phenologies, surprisingly, plant evolutionary responses to drought were relatively weak. In contrast, plant fitness in both drought and nondrought environments was linked strongly to the rapid responses of soil microbial community structure to moisture manipulations. Specifically, plants were most fit when their contemporary environmental conditions (wet vs. dry soil) matched the historical environmental conditions (wet vs. dry soil) of their associated microbial community. Together, our findings suggest that, when faced with environmental change, plants may not be limited to "adapt or migrate" strategies; instead, they also may benefit from association with interacting species, especially diverse soil microbial communities, that respond rapidly to environmental change.

The relative importance of rapid evolution for plant-microbe interactions depends on ecological context.

Evolution can occur on ecological time-scales, affecting community and ecosystem processes. However, the importance of evolutionary change relative to ecological processes remains largely unknown. Here, we analyse data from a long-term experiment in which we allowed plant populations to evolve for three generations in dry or wet soils and used a reciprocal transplant to compare the ecological effect of drought and the effect of plant evolutionary responses to drought on soil microbial communities and nutrient availability. Plants that evolved under drought tended to support higher bacterial and fungal richness, and increased fungal : bacterial ratios in the soil. Overall, the magnitudes of ecological and evolutionary effects on microbial communities were similar; however, the strength and direction of these effects depended on the context in which they were measured. For example, plants that evolved in dry environments increased bacterial abundance in dry contemporary environments, but decreased bacterial abundance in wet contemporary environments. Our results suggest that interactions between recent evolutionary history and ecological context affect both the direction and magnitude of plant effects on soil microbes. Consequently, an eco-evolutionary perspective is required to fully understand plant-microbe interactions.