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The rapid increase in microbial activity that occurs when a dry soil is rewetted has been well documented and is of great interest due to implications of changing precipitation patterns on soil C dynamics. Several studies have shown minor net changes in microbial population diversity or abundance following wet-up, but the gross population dynamics of bacteria and fungi resulting from soil wet-up are virtually unknown. Here we applied DNA stable isotope probing with H 2 18 O coupled with quantitative PCR to characterize new growth, survival, and mortality of bacteria and fungi following the rewetting of a seasonally dried California annual grassland soil. Microbial activity, as determined by CO 2 production, increased significantly within three hours of wet-up, yet new growth was not detected until after three hours, suggesting a pulse of nongrowth activity immediately following wet-up, likely due to osmo-regulation and resuscitation from dormancy in response to the rapid change in water potential. Total microbial abundance revealed little change throughout the seven-day post-wet incubation, but there was substantial turnover of both bacterial and fungal populations (49% and 52%, respectively). New growth was linear between 24 and 168 hours for both bacteria and fungi, with average growth rates of 2.3 × 10 8 bacterial 16S rRNA gene copies·[g dry mass] −1 ·h −1 and 4.3 × 10 7 fungal ITS copies·[g dry mass] −1 ·h −1 . While bacteria and fungi differed in their mortality and survival characteristics during the seven-day incubation, mortality that occurred within the first three hours was similar, with 25% and 27% of bacterial and fungal gene copies disappearing from the pre-wet community, respectively. The rapid disappearance of gene copies indicates that cell death, occurring either during the extreme dry down period (preceding five months) or during the rapid change in water potential due to wet-up, generates a significant pool of available C that likely contributes to the large pulse in CO 2 associated with wet-up. A dynamic assemblage of growing and dying organisms controlled the CO 2 pulse, but the balance between death and growth resulted in relatively stable total population abundances, even after a profound and sudden change in environment.

Nutrient amendment diminished bacterial functional diversity, consolidating carbon flow through fewer bacterial taxa. Here, we show strong differences in the bacterial taxa responsible for respiration from four ecosystems, indicating the potential for taxon-specific control over soil carbon cycling. Trends in functional diversity, defined as the richness of bacteria contributing to carbon flux and their equitability of carbon use, paralleled trends in taxonomic diversity although functional diversity was lower overall. Among genera common to all ecosystems, Bradyrhizobium , the Acidobacteria genus RB41 , and Streptomyces together composed 45–57% of carbon flow through bacterial productivity and respiration. Bacteria that utilized the most carbon amendment (glucose) were also those that utilized the most native soil carbon, suggesting that the behavior of key soil taxa may influence carbon balance. Mapping carbon flow through different microbial taxa as demonstrated here is crucial in developing taxon-sensitive soil carbon models that may reduce the uncertainty in climate change projections. The fate of soil carbon depends on microbial processes, but whether different microbial taxa have individualistic effects on carbon fluxes is unknown. Here the authors use 16 S amplicon sequencing and stable isotopes to show how taxonomic differences influence bacterial respiration and carbon cycling across four ecosystems.

Microorganisms perform most decomposition on Earth, mediating carbon (C) loss from ecosystems, and thereby influencing climate. Yet, how variation in the identity and composition of microbial communities influences ecosystem C balance is far from clear. Using quantitative stable isotope probing of DNA, we show how individual bacterial taxa influence soil C cycling following the addition of labile C (glucose). Specifically, we show that increased decomposition of soil C in response to added glucose (positive priming) occurs as a phylogenetically diverse group of taxa, accounting for a large proportion of the bacterial community, shift toward additional soil C use for growth. Our findings suggest that many microbial taxa exhibit C use plasticity, as most taxa altered their use of glucose and soil organic matter depending upon environmental conditions. In contrast, bacteria that exhibit other responses to glucose (reduced growth or reliance on glucose for additional growth) clustered strongly by phylogeny. These results suggest that positive priming is likely the prototypical response of bacteria to sustained labile C addition, consistent with the widespread occurrence of the positive priming effect in nature.

Microbial activity increases after rewetting dry soil, resulting in a pulse of carbon mineralization and nutrient availability. The biogeochemical responses to wet-up are reasonably well understood and known to be microbially mediated. Yet, the population level dynamics, and the resulting changes in microbial community patterns, are not well understood as ecological phenomena. Here, we used sequencing of 16S rRNA genes coupled with heavy water (H 2 18 O) DNA quantitative stable isotope probing to estimate population-specific rates of growth and mortality in response to a simulated wet-up event in a California annual grassland soil. Bacterial growth and mortality responded rapidly to wet-up, within 3 h, and continued throughout the 168 h incubation, with patterns of sequential growth observed at the phylum level. Of the 37 phyla detected in the prewet community, growth was found in 18 phyla while mortality was measured in 26 phyla. Rapid growth and mortality rates were measurable within 3 h of wet-up but had contrasting characteristics; growth at 3 h was dominated by select taxa within the Proteobacteria and Firmicutes, whereas mortality was taxonomically widespread. Furthermore, across the community, mortality exhibited density-independence, consistent with the indiscriminate shock resulting from dry-down and wet-up, whereas growth was density-dependent, consistent with control by competition or predation. Total aggregated growth across the community was highly correlated with total soil CO 2 production. Together, these results illustrate how previously “invisible” population responses can translate quantitatively to emergent observations of ecosystem-scale biogeochemistry.

Relationships between microbial genes and performance are often evaluated in the laboratory in pure cultures, with little validation in nature. Here, we show that genomic traits related to laboratory measurements of maximum growth potential failed to predict the growth rates of bacteria in unamended soil, but successfully predicted growth responses to resource pulses: growth increased with 16S rRNA gene copy number and declined with genome size after substrate addition to soils, responses that were repeated in four different ecosystems. Genome size best predicted growth rate in response to addition of glucose alone; adding ammonium with glucose weakened the relationship, and the relationship was absent in nutrient-replete pure cultures, consistent with the idea that reduced genome size is a mechanism of nutrient conservation. Our findings demonstrate that genomic traits of soil bacteria can map to their ecological performance in nature, but the mapping is poor under native soil conditions, where genomic traits related to stress tolerance may prove more predictive. These results remind that phenotype depends on environmental context, underscoring the importance of verifying proposed schemes of trait-based strategies through direct measurement of performance in nature, an important and currently missing foundation for translating microbial processes from genes to ecosystems.

Phylogeny is an ecologically meaningful way to classify plants and animals, as closely related taxa frequently have similar ecological characteristics, functional traits and effects on ecosystem processes. For bacteria, however, phylogeny has been argued to be an unreliable indicator of an organism’s ecology owing to evolutionary processes more common to microbes such as gene loss and lateral gene transfer, as well as convergent evolution. Here we use advanced stable isotope probing with 13 C and 18 O to show that evolutionary history has ecological significance for in situ bacterial activity. Phylogenetic organization in the activity of bacteria sets the stage for characterizing the functional attributes of bacterial taxonomic groups. Connecting identity with function in this way will allow scientists to begin building a mechanistic understanding of how bacterial community composition regulates critical ecosystem functions.

Understanding how population‐level dynamics contribute to ecosystem‐level processes is a primary focus of ecological research and has led to important breakthroughs in the ecology of macroscopic organisms. However, the inability to measure population‐specific rates, such as growth, for microbial taxa within natural assemblages has limited ecologists’ understanding of how microbial populations interact to regulate ecosystem processes. Here, we use isotope incorporation within DNA molecules to model taxon‐specific population growth in the presence of 18O‐labeled water. By applying this model to phylogenetic marker sequencing data collected from stable‐isotope probing studies, we estimate rates of growth, mortality, and turnover for individual microbial populations within soil assemblages. When summed across the entire bacterial community, our taxon‐specific estimates are within the range of other whole‐assemblage measurements of bacterial turnover. Because it can be applied to environmental samples, the approach we present is broadly applicable to measuring population growth, mortality, and associated biogeochemical process rates of microbial taxa for a wide range of ecosystems and can help reveal how individual microbial populations drive biogeochemical fluxes.

Organisms influence ecosystems, from element cycling to disturbance regimes, to trophic interactions and to energy partitioning. Microorganisms are part of this influence, and understanding their ecology in nature requires studying the traits of these organisms quantitatively in their natural habitats—a challenging task, but one which new approaches now make possible. Here, we show that growth rate and carbon assimilation rate of soil microorganisms are influenced more by evolutionary history than by climate, even across a broad climatic gradient spanning major temperate life zones, from mixed conifer forest to high-desert grassland. Most of the explained variation (~50% to ~90%) in growth rate and carbon assimilation rate was attributable to differences among taxonomic groups, indicating a strong influence of evolutionary history, and taxonomic groupings were more predictive for organisms responding to resource addition. With added carbon and nitrogen substrates, differences among taxonomic groups explained approximately eightfold more variance in growth rate than did differences in ecosystem type. Taxon-specific growth and carbon assimilation rates were highly intercorrelated across the four ecosystems, constrained by the taxonomic identity of the organisms, such that plasticity driven by environment was limited across ecosystems varying in temperature, precipitation and dominant vegetation. Taken together, our results suggest that, similar to multicellular life, the traits of prokaryotes in their natural habitats are constrained by evolutionary history to a greater degree than environmental variation. Using stable isotope probing to quantify growth and carbon assimilation rates of soil microbes along an elevation gradient, the authors show that these traits are more constrained by evolutionary history than environmental variation.

A large portion of activity in soil microbial communities occurs in short time frames in response to an increase in C availability, affecting the biogeochemical cycling of nitrogen. These changes are of particular importance as nitrogen represents both a limiting nutrient for terrestrial plants as well as a potential pollutant. Episodic inputs of labile carbon (C) to soil can rapidly stimulate nitrogen (N) immobilization by soil microorganisms. However, the transcriptional patterns that underlie this process remain unclear. In order to better understand the regulation of N cycling in soil microbial communities, we conducted a 48-h laboratory incubation with agricultural soil where we stimulated the uptake of inorganic N by amending the soil with glucose. We analyzed the metagenome and metatranscriptome of the microbial communities at four time points that corresponded with changes in N availability. The relative abundances of genes remained largely unchanged throughout the incubation. In contrast, glucose addition rapidly increased the transcription of genes encoding ammonium and nitrate transporters, enzymes responsible for N assimilation into biomass, and genes associated with the N regulatory network. This upregulation coincided with an increase in transcripts associated with glucose breakdown and oxoglutarate production, demonstrating a connection between C and N metabolism. When concentrations of ammonium were low, we observed a transient upregulation of genes associated with the nitrogen-fixing enzyme nitrogenase. Transcripts for nitrification and denitrification were downregulated throughout the incubation, suggesting that dissimilatory transformations of N may be suppressed in response to labile C inputs in these soils. These results demonstrate that soil microbial communities can respond rapidly to changes in C availability by drastically altering the transcription of N cycling genes. IMPORTANCE A large portion of activity in soil microbial communities occurs in short time frames in response to an increase in C availability, affecting the biogeochemical cycling of nitrogen. These changes are of particular importance as nitrogen represents both a limiting nutrient for terrestrial plants as well as a potential pollutant. However, we lack a full understanding of the short-term effects of labile carbon inputs on the metabolism of microbes living in soil. Here, we found that soil microbial communities responded to labile carbon addition by rapidly transcribing genes encoding proteins and enzymes responsible for inorganic nitrogen acquisition, including nitrogen fixation. This work demonstrates that soil microbial communities respond within hours to carbon inputs through altered gene expression. These insights are essential for an improved understanding of the microbial processes governing soil organic matter production, decomposition, and nutrient cycling in natural and agricultural ecosystems.