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.

Coexistence barriers confine the poleward range of a globally distributed plant.

In the study of factors shaping species' poleward range boundaries, climatic constraints are often assigned greater importance than biotic interactions such as competition. However, theory suggests competition can truncate a species' fundamental niche in harsh environments. We test this by challenging a mechanistic niche model - containing explicit competition terms - to predict the poleward range boundaries of two globally distributed, ecologically similar aquatic plant species. Mechanistic competition models accurately predicted the northern range limits of our study species, outperforming competition-free mechanistic models and matching the predictive ability of statistical niche models fit to occurrence records. Using the framework of modern coexistence theory, we found that relative nonlinearity in competitors' responses to temperature fluctuations maintains their coexistence boundary, highlighting the importance of this fluctuation-dependent mechanism. Our results support a more nuanced, interactive role of climate and competition in determining range boundaries, and illustrate a practical, process-based approach to understanding the determinants of range limits.

Shifting limitation of primary production: experimental support for a new model in lake ecosystems.

The limits on primary production vary in complex ways across space and time. Strong tests of clear conceptual models have been instrumental in understanding these patterns in both terrestrial and aquatic ecosystems. Here we present the first experimental test of a new model describing how shifts from nutrient to light limitation control primary productivity in lake ecosystems as hydrological inputs of nutrients and organic matter vary. We found support for two key predictions of the model: that gross primary production (GPP) follows a hump-shaped relationship with increasing dissolved organic carbon (DOC) concentrations; and that the maximum GPP, and the critical DOC concentration at which the hump occurs, are determined by the stoichiometry and chromophoricity of the hydrological inputs. Our results advance fundamental understanding of the limits on aquatic primary production, and have important applications given ongoing anthropogenic alterations of the nutrient and organic matter inputs to surface waters.

Seasonal evaluation of biotic and abiotic factors suggests phosphorus retention in constructed floodplains in three agricultural streams.

Floodplain restoration constructed via the two-stage ditch in agricultural streams has the potential to enhance nutrient retention and prevent the eutrophication of downstream ecosystems. Identifying the role of biotic and abiotic factors influencing soluble reactive phosphorus (SRP) retention in floodplains is of interest given that changing redox conditions associated with floodplain inundation can result in a release of geochemically sorbed SRP to the water column. In three agricultural waterways (Indiana, USA), we conducted seasonal measurements of a suite of biogeochemical pools (total P, bioavailable P and Fe) and processes (SRP flux and microbial respiration) from multiple floodplain transects, along with their adjacent stream sediments, to determine the role of biotic and abiotic processes on floodplain SRP retention or release. Across floodplain soils, organic matter explained a significant amount of variation in soil respiration, and SRP flux from the water column to the floodplain soils was driven by the molar ratio of Fe: P, with values >6 indicating potential SRP sorption due to increased available sorption sites. We developed a mass balance model at a single site to relate seasonal floodplain processes with water column SRP export, above and below the study reach, using measurements in this study combined with data from the literature. Grab sample data suggest that the reach retained 26% of incoming SRP, which the mass balance model attributed to seasonal synergy between plant assimilation in spring and summer (removing P from floodplain soils) and abiotic P sorption during winter and spring inundation (adding SRP to the floodplain). Retention of SRP was higher in floodplain soils compared to stream sediments based on the modeled SRP budget. Thus, we suggest that these constructed floodplains will maximize SRP retention from the water column if they inundate regularly, have floodplain soils with Fe:P > 3-6, and that promote sustained plant life.

The Regenerating Adult Zebrafish Retina Recapitulates Developmental Fate Specification Programs.

Adult zebrafish possess the remarkable capacity to regenerate neurons. In the damaged zebrafish retina, Müller glia reprogram and divide to produce neuronal progenitor cells (NPCs) that proliferate and differentiate into both lost neuronal cell types and those unaffected by the damage stimulus, which suggests that developmental specification/differentiation programs might be recapitulated during regeneration. Quantitative real-time polymerase chain reaction revealed that developmental competence factors are expressed following photoreceptor damage induced by intense light or in a genetic rod photoreceptor cell ablation model. In both light- and N-Methyl-D-aspartic acid (NMDA)-damaged adult zebrafish retinas, NPCs, but not proliferating Müller glia, expressed fluorescent reporters controlled by promoters of ganglion (atoh7), amacrine (ptf1a), bipolar (vsx1), or red cone photoreceptor cell competence factors (thrb) in a temporal expression sequence. In both damage paradigms, atoh7:GFP was expressed first, followed by ptf1a:EGFP and lastly, vsx1:GFP, whereas thrb:Tomato was observed in NPCs at the same time as ptf1a:GFP following light damage but shifted alongside vsx1:GFP in the NMDA-damaged retina. Moreover, HuC/D, indicative of ganglion and amacrine cell differentiation, colocalized with atoh7:GFP prior to ptf1a:GFP expression in the ganglion cell layer, which was followed by Zpr-1 expression (red/green cone photoreceptors) in thrb:Tomato-positive cells in the outer nuclear layer in both damage paradigms, mimicking the developmental differentiation sequence. However, comparing NMDA- to light-damaged retinas, the fraction of PCNA-positive cells expressing atoh7:GFP increased, that of thrb:Tomato and vsx1:GFP decreased, and that of ptf1a:GFP remained similar. To summarize, developmental cell specification programs were recapitulated during retinal regeneration, which adapted to account for the cell type lost.

How sample heterogeneity can obscure the signal of microbial interactions.

Microbial community data are commonly subjected to computational tools such as correlation networks, null models, and dynamic models, with the goal of identifying the ecological processes structuring microbial communities. A major assumption of these methods is that the signs and magnitudes of species interactions and vital rates can be reliably parsed from observational data on species' (relative) abundances. However, we contend that this assumption is violated when sample units contain any underlying spatial structure. Here, we show how three phenomena-Simpson's paradox, context-dependence, and nonlinear averaging-can lead to erroneous conclusions about population parameters and species interactions when samples contain heterogeneous mixtures of populations or communities. At the root of this issue is the fundamental mismatch between the spatial scales of species interactions (micrometers) and those of typical microbial community samples (millimeters to centimetres). These issues can be overcome by measuring and accounting for spatial heterogeneity at very small scales, which will lead to more reliable inference of the ecological mechanisms structuring natural microbial communities.

Negative frequency-dependent growth underlies the stable coexistence of two cosmopolitan aquatic plants.

Identifying and quantifying the mechanisms influencing species coexistence remains a major challenge for the study of community ecology. These mechanisms, which stem from species' differential responses to competition and their environments, promote coexistence if they give each species a growth advantage when rare. Yet despite the widespread assumption that co-occurring species stably coexist, there have been few empirical demonstrations in support of this claim. Likewise, coexistence is often assumed to result from interspecific differences in life-history traits, but the relative contributions of these trait differences to coexistence are rarely quantified, particularly across environmental gradients. Using two widely co-occurring and ecologically similar species of freshwater duckweed plants (Spirodela polyrhiza and Lemna minor), we tested hypotheses that interspecific differences in facultative dormancy behaviors, thermal reaction norms, and density-dependent growth promote coexistence between these species, and that their relative influences on coexistence change as average temperatures and fluctuations around them vary. In competition experiments, we found strong evidence for negative frequency-dependent growth across a range of both static and fluctuating temperatures, suggesting a critical role of fluctuation-independent stabilization in coexistence. This negative frequency dependence could be explained by our observation that for both species, intraspecific competition was over 1.5 times stronger than interspecific competition, granting each species a low-density growth advantage. Using an empirically parameterized competition model, we found that while coexistence was facilitated by environmental fluctuations, fluctuation-independent stabilization via negative frequency dependence was crucial for coexistence. Conversely, the temporal storage effect, an important fluctuation-dependent mechanism, was relatively weak in comparison. Contrary to expectations, differences in the species' thermal reaction norms and dormancy behaviors did not significantly promote coexistence in fluctuating environments. Our results highlight how coexistence in two ubiquitous and ostensibly similar aquatic plants is not necessarily a product of their most obvious interspecific differences, and instead results from subtle niche differences causing negative frequency-dependent growth, which acts consistently on both species across environmental gradients.

Understanding how microbiomes influence the systems they inhabit.

Translating the ever-increasing wealth of information on microbiomes (environment, host or built environment) to advance our understanding of system-level processes is proving to be an exceptional research challenge. One reason for this challenge is that relationships between characteristics of microbiomes and the system-level processes that they influence are often evaluated in the absence of a robust conceptual framework and reported without elucidating the underlying causal mechanisms. The reliance on correlative approaches limits the potential to expand the inference of a single relationship to additional systems and advance the field. We propose that research focused on how microbiomes influence the systems they inhabit should work within a common framework and target known microbial processes that contribute to the system-level processes of interest. Here, we identify three distinct categories of microbiome characteristics (microbial processes, microbial community properties and microbial membership) and propose a framework to empirically link each of these categories to each other and the broader system-level processes that they affect. We posit that it is particularly important to distinguish microbial community properties that can be predicted using constituent taxa (community-aggregated traits) from those properties that cannot currently be predicted using constituent taxa (emergent properties). Existing methods in microbial ecology can be applied to more explicitly elucidate properties within each of these three categories of microbial characteristics and connect them with each other. We view this proposed framework, gleaned from a breadth of research on environmental microbiomes and ecosystem processes, as a promising pathway with the potential to advance discovery and understanding across a broad range of microbiome science.

Climate-mediated hybrid zone movement revealed with genomics, museum collection, and simulation modeling.

Climate-mediated changes in hybridization will dramatically alter the genetic diversity, adaptive capacity, and evolutionary trajectory of interbreeding species. Our ability to predict the consequences of such changes will be key to future conservation and management decisions. Here we tested through simulations how recent warming (over the course of a 32-y period) is affecting the geographic extent of a climate-mediated developmental threshold implicated in maintaining a butterfly hybrid zone (Papilio glaucus and Papilio canadensis; Lepidoptera: Papilionidae). These simulations predict a 68-km shift of this hybrid zone. To empirically test this prediction, we assessed genetic and phenotypic changes using contemporary and museum collections and document a 40-km northward shift of this hybrid zone. Interactions between the two species appear relatively unchanged during hybrid zone movement. We found no change in the frequency of hybridization, and regions of the genome that experience little to no introgression moved largely in concert with the shifting hybrid zone. Model predictions based on climate scenarios predict this hybrid zone will continue to move northward, but with substantial spatial heterogeneity in the velocity (55-144 km/1 °C), shape, and contiguity of movement. Our findings suggest that the presence of nonclimatic barriers (e.g., genetic incompatibilities) and/or nonlinear responses to climatic gradients may preserve species boundaries as the species shift. Further, we show that variation in the geography of hybrid zone movement could result in evolutionary responses that differ for geographically distinct populations spanning hybrid zones, and thus have implications for the conservation and management of genetic diversity.

Life history constraints explain negative relationship between fish productivity and dissolved organic carbon in lakes.

Resource availability constrains the life history strategies available to organisms and may thereby limit population growth rates and productivity. We used this conceptual framework to explore the mechanisms driving recently reported negative relationships between fish productivity and dissolved organic carbon (DOC) concentrations in lakes. We studied populations of bluegill (Lepomis macrochirus) in a set of lakes with DOC concentrations ranging from 3 to 24 mg/L; previous work has demonstrated that primary and secondary productivity of food webs is negatively related to DOC concentration across this gradient. For each population, we quantified individual growth rate, age at maturity, age-specific fecundity, maximum age, length-weight and length-egg size relationships, and other life history characteristics. We observed a strong negative relationship between maximum size and DOC concentration; for instance, fish reached masses of 150 to 260 g in low-DOC lakes but <120 g in high-DOC lakes. Relationships between fecundity and length, and between egg size and length, were constant across the DOC gradient. Because fish in high-DOC lakes reached smaller sizes but had similar fecundity and egg size at a given size, their total lifetime fecundity was as much as two orders of magnitude lower than fish in low-DOC lakes. High DOC concentrations appeared to constrain the range of bluegill life history strategies available; populations in high-DOC lakes always had low initial growth rates and high ages at maturity, whereas populations in low-DOC showed higher variability in these traits. This was also the case for the intrinsic rates of natural increase of these populations, which were always low at the high end of the DOC gradient. The potentially lower capacity for fish populations in high-DOC lakes to recover from exploitation has clear implications for the sustainable management of recreational fisheries in the face of considerable spatial heterogeneity and ongoing temporal change in lake DOC concentrations.

Terrestrial support of lake food webs: Synthesis reveals controls over cross-ecosystem resource use.

Widespread evidence that organic matter exported from terrestrial into aquatic ecosystems supports recipient food webs remains controversial. A pressing question is not only whether high terrestrial support is possible but also what the general conditions are under which it arises. We assemble the largest data set, to date, of the isotopic composition (δ2H, δ13C, and δ15N) of lake zooplankton and the resources at the base of their associated food webs. In total, our data set spans 559 observations across 147 lakes from the boreal to subtropics. By predicting terrestrial resource support from within-lake and catchment-level characteristics, we found that half of all consumer observations that is, the median were composed of at least 42% terrestrially derived material. In general, terrestrial support of zooplankton was greatest in lakes with large physical and hydrological connections to catchments that were rich in aboveground and belowground organic matter. However, some consumers responded less strongly to terrestrial resources where within-lake production was elevated. Our study shows that multiple mechanisms drive widespread cross-ecosystem support of aquatic consumers across Northern Hemisphere lakes and suggests that changes in terrestrial landscapes will influence ecosystem processes well beyond their boundaries.

Social-ecological outcomes in recreational fisheries: the interaction of lakeshore development and stocking.

Many ecosystems continue to experience rapid transformations due to processes like land use change and resource extraction. A systems approach to maintaining natural resources focuses on how interactions and feedbacks among components of complex social-ecological systems generate social and ecological outcomes. In recreational fisheries, residential shoreline development and fish stocking are two widespread human behaviors that influence fisheries, yet emergent social-ecological outcomes from these potentially interacting behaviors remain under explored. We applied a social-ecological systems framework using a simulation model and empirical data to determine whether lakeshore development is likely to promote stocking through its adverse effects on coarse woody habitat and thereby also on survival of juvenile and adult fish. We demonstrate that high lakeshore development is likely to generate dependency of the ecosystem on the social system, in the form of stocking. Further, lakeshore development can interact with social-ecological processes to create deficits for state-level governments, which threatens the ability to fund further ecosystem subsidies. Our results highlight the value of a social-ecological framework for maintaining ecosystem services like recreational fisheries.

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.

Experimental whole-lake increase of dissolved organic carbon concentration produces unexpected increase in crustacean zooplankton density.

The observed pattern of lake browning, or increased terrestrial dissolved organic carbon (DOC) concentration, across the northern hemisphere has amplified the importance of understanding how consumer productivity varies with DOC concentration. Results from comparative studies suggest these increased DOC concentrations may reduce crustacean zooplankton productivity due to reductions in resource quality and volume of suitable habitat. Although these spatial comparisons provide an expectation for the response of zooplankton productivity as DOC concentration increases, we still have an incomplete understanding of how zooplankton respond to temporal increases in DOC concentration within a single system. As such, we used a whole-lake manipulation, in which DOC concentration was increased from 8 to 11 mg L(-1) in one basin of a manipulated lake, to test the hypothesis that crustacean zooplankton production should subsequently decrease. In contrast to the spatially derived expectation of sharp DOC-mediated decline, we observed a small increase in zooplankton densities in response to our experimental increase in DOC concentration of the treatment basin. This was due to significant increases in gross primary production and resource quality (lower seston carbon-to-phosphorus ratio; C:P). These results demonstrate that temporal changes in lake characteristics due to increased DOC may impact zooplankton in ways that differ from those observed in spatial surveys. We also identified significant interannual variability across our study region, which highlights potential difficulty in detecting temporal responses of organism abundances to gradual environmental change (e.g., browning).

Molecular mechanisms of ionic liquid cytotoxicity probed by an integrated experimental and computational approach.

Ionic liquids (ILs) are salts that remain liquid down to low temperatures, and sometimes well below room temperature. ILs have been called "green solvents" because of their extraordinarily low vapor pressure and excellent solvation power, but ecotoxicology studies have shown that some ILs exhibit greater toxicity than traditional solvents. A fundamental understanding of the molecular mechanisms responsible for IL toxicity remains elusive. Here we show that one mode of IL toxicity on unicellular organisms is driven by swelling of the cell membrane. Cytotoxicity assays, confocal laser scanning microscopy, and molecular simulations reveal that IL cations nucleate morphological defects in the microbial cell membrane at concentrations near the half maximal effective concentration (EC50) of several microorganisms. Cytotoxicity increases with increasing alkyl chain length of the cation due to the ability of the longer alkyl chain to more easily embed in, and ultimately disrupt, the cell membrane.

Microbiomes in light of traits: A phylogenetic perspective.

A focus on the phenotypic characteristics of microorganisms-their traits-offers a path for interpreting the growing amount of microbiome data. We review key aspects of microbial traits, as well as approaches used to assay their phylogenetic distribution. Recent studies reveal that microbial traits are differentially conserved across the tree of life and appear to be conserved in a hierarchical fashion, possibly linked to their biochemical complexity. These results suggest a predictive framework whereby the genetic (or taxonomic) resolution of microbiome variation among samples provides information about the traits under selection. The organizational parallels seen among human and free-living microbiomes seem to support this idea. Developments in this framework may offer predictions not only for how microbial composition responds to changing environmental conditions, but also for how these changes may alter the health or functioning in human, engineered, and environmental systems.

Phytoplankton traits predict ecosystem function in a global set of lakes.

Predicting ecosystem function from environmental conditions is a central goal of ecosystem ecology. However, many traditional ecosystem models are tailored for specific regions or ecosystem types, requiring several regional models to predict the same function. Alternatively, trait-based approaches have been effectively used to predict community structure in both terrestrial and aquatic environments and ecosystem function in a limited number of terrestrial examples. Here, we test the efficacy of a trait-based model in predicting gross primary production (GPP) in lake ecosystems. We incorporated data from >1000 United States lakes along with laboratory-generated phytoplankton trait data to build a trait-based model of GPP and then validated the model with GPP observations from a separate set of globally distributed lakes. The trait-based model performed as well as or outperformed two ecosystem models both spatially and temporally, demonstrating the efficacy of trait-based models for predicting ecosystem function over a range of environmental conditions.

Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe.

Soil microorganisms are critical to ecosystem functioning and the maintenance of soil fertility. However, despite global increases in the inputs of nitrogen (N) and phosphorus (P) to ecosystems due to human activities, we lack a predictive understanding of how microbial communities respond to elevated nutrient inputs across environmental gradients. Here we used high-throughput sequencing of marker genes to elucidate the responses of soil fungal, archaeal, and bacterial communities using an N and P addition experiment replicated at 25 globally distributed grassland sites. We also sequenced metagenomes from a subset of the sites to determine how the functional attributes of bacterial communities change in response to elevated nutrients. Despite strong compositional differences across sites, microbial communities shifted in a consistent manner with N or P additions, and the magnitude of these shifts was related to the magnitude of plant community responses to nutrient inputs. Mycorrhizal fungi and methanogenic archaea decreased in relative abundance with nutrient additions, as did the relative abundances of oligotrophic bacterial taxa. The metagenomic data provided additional evidence for this shift in bacterial life history strategies because nutrient additions decreased the average genome sizes of the bacterial community members and elicited changes in the relative abundances of representative functional genes. Our results suggest that elevated N and P inputs lead to predictable shifts in the taxonomic and functional traits of soil microbial communities, including increases in the relative abundances of faster-growing, copiotrophic bacterial taxa, with these shifts likely to impact belowground ecosystems worldwide.

Ionic liquid biodegradability depends on specific wastewater microbial consortia.

Complete biodegradation of a newly-synthesized chemical in a wastewater treatment plant (WWTP) eliminates the potential for novel environmental pollutants. However, differences within- and between-WWTP microbial communities may alter expectations for biodegradation. WWTP communities can also serve as a source of unique consortia that, when enriched, can metabolize chemicals that tend to resist degradation, but are otherwise promising green alternatives. We tested the biodegradability of three ionic liquids (ILs): 1-octyl-3-methylpyridinium bromide (OMP), 1-butyl-3-methylpyridinium bromide (BMP) and 1-butyl-3-methylimidazolium chloride (BMIM). We performed tests using communities from two WWTPs at three time points. Site-specific and temporal variation both influenced community composition, which impacted the success of OMP biodegradability. Neither BMP nor BMIM degraded in any test, suggesting that these ILs are unlikely to be removed by traditional treatment. Following standard biodegradation assays, we enriched for three consortia that were capable of quickly degrading OMP, BMP and BMIM. Our results indicate WWTPs are not functionally redundant with regard to biodegradation of specific ionic liquids. However, consortia can be enriched to degrade chemicals that fail biodegradability assays. This information can be used to prepare pre-treatment procedures and prevent environmental release of novel pollutants.

Local-global overlap in diversity informs mechanisms of bacterial biogeography.

Spatial variation in environmental conditions and barriers to organism movement are thought to be important factors for generating endemic species, thus enhancing global diversity. Recent microbial ecology research suggested that the entire diversity of bacteria in the global oceans could be recovered at a single site, thus inferring a lack of bacterial endemism. We argue this is not the case in the global ocean, but might be in other bacterial ecosystems with higher dispersal rates and lower global diversity, like the human gut. We quantified the degree to which local and global bacterial diversity overlap in a diverse set of ecosystems. Upon comparison of observed local-global diversity overlap with predictions from a neutral biogeography model, human-associated microbiomes (gut, skin, mouth) behaved much closer to neutral expectations whereas soil, lake and marine communities deviated strongly from the neutral expectations. This is likely a result of differences in dispersal rate among 'patches', global diversity of these systems, and local densities of bacterial cells. It appears that overlap of local and global bacterial diversity is surprisingly large (but likely not one-hundred percent), and most importantly this overlap appears to be predictable based upon traditional biogeographic parameters like community size, global diversity, inter-patch environmental heterogeneity and patch connectivity.