Shifts in soil ammonia-oxidizing community maintain the nitrogen stimulation of nitrification across climatic conditions.

Anthropogenic nitrogen (N) loading alters soil ammonia-oxidizing archaea (AOA) and bacteria (AOB) abundances, likely leading to substantial changes in soil nitrification. However, the factors and mechanisms determining the responses of soil AOA:AOB and nitrification to N loading are still unclear, making it difficult to predict future changes in soil nitrification. Herein, we synthesize 68 field studies around the world to evaluate the impacts of N loading on soil ammonia oxidizers and nitrification. Across a wide range of biotic and abiotic factors, climate is the most important driver of the responses of AOA:AOB to N loading. Climate does not directly affect the N-stimulation of nitrification, but does so via climate-related shifts in AOA:AOB. Specifically, climate modulates the responses of AOA:AOB to N loading by affecting soil pH, N-availability and moisture. AOB play a dominant role in affecting nitrification in dry climates, while the impacts from AOA can exceed AOB in humid climates. Together, these results suggest that climate-related shifts in soil ammonia-oxidizing community maintain the N-stimulation of nitrification, highlighting the importance of microbial community composition in mediating the responses of the soil N cycle to N loading.

Rapid growth rate responses of terrestrial bacteria to field warming on the Antarctic Peninsula.

Ice-free terrestrial environments of the western Antarctic Peninsula are expanding and subject to colonization by new microorganisms and plants, which control biogeochemical cycling. Measuring growth rates of microbial populations and ecosystem carbon flux is critical for understanding how terrestrial ecosystems in Antarctica will respond to future warming. We implemented a field warming experiment in early (bare soil; +2 °C) and late (peat moss-dominated; +1.2 °C) successional glacier forefield sites on the western Antarctica Peninsula. We used quantitative stable isotope probing with H218O using intact cores in situ to determine growth rate responses of bacterial taxa to short-term (1 month) warming. Warming increased the growth rates of bacterial communities at both sites, even doubling the number of taxa exhibiting significant growth at the early site. Growth responses varied among taxa. Despite that warming induced a similar response for bacterial relative growth rates overall, the warming effect on ecosystem carbon fluxes was stronger at the early successional site-likely driven by increased activity of autotrophs which switched the ecosystem from a carbon source to a carbon sink. At the late-successional site, warming caused a significant increase in growth rate of many Alphaproteobacteria, but a weaker and opposite gross ecosystem productivity response that decreased the carbon sink-indicating that the carbon flux rates were driven more strongly by the plant communities. Such changes to bacterial growth and ecosystem carbon cycling suggest that the terrestrial Antarctic Peninsula can respond fast to increases in temperature, which can have repercussions for long-term elemental cycling and carbon storage.

A meta-evaluation of the quality of reporting and execution in ecological meta-analyses.

Quantitatively summarizing results from a collection of primary studies with meta-analysis can help answer ecological questions and identify knowledge gaps. The accuracy of the answers depends on the quality of the meta-analysis. We reviewed the literature assessing the quality of ecological meta-analyses to evaluate current practices and highlight areas that need improvement. From each of the 18 review papers that evaluated the quality of meta-analyses, we calculated the percentage of meta-analyses that met criteria related to specific steps taken in the meta-analysis process (i.e., execution) and the clarity with which those steps were articulated (i.e., reporting). We also re-evaluated all the meta-analyses available from Pappalardo et al. [1] to extract new information on ten additional criteria and to assess how the meta-analyses recognized and addressed non-independence. In general, we observed better performance for criteria related to reporting than for criteria related to execution; however, there was a wide variation among criteria and meta-analyses. Meta-analyses had low compliance with regard to correcting for phylogenetic non-independence, exploring temporal trends in effect sizes, and conducting a multifactorial analysis of moderators (i.e., explanatory variables). In addition, although most meta-analyses included multiple effect sizes per study, only 66% acknowledged some type of non-independence. The types of non-independence reported were most often related to the design of the original experiment (e.g., the use of a shared control) than to other sources (e.g., phylogeny). We suggest that providing specific training and encouraging authors to follow the PRISMA EcoEvo checklist recently developed by O'Dea et al. [2] can improve the quality of ecological meta-analyses.

Microbial growth under drought is confined to distinct taxa and modified by potential future climate conditions.

Climate change increases the frequency and intensity of drought events, affecting soil functions including carbon sequestration and nutrient cycling, which are driven by growing microorganisms. Yet we know little about microbial responses to drought due to methodological limitations. Here, we estimate microbial growth rates in montane grassland soils exposed to ambient conditions, drought, and potential future climate conditions (i.e., soils exposed to 6 years of elevated temperatures and elevated CO2 levels). For this purpose, we combined 18O-water vapor equilibration with quantitative stable isotope probing (termed 'vapor-qSIP') to measure taxon-specific microbial growth in dry soils. In our experiments, drought caused >90% of bacterial and archaeal taxa to stop dividing and reduced the growth rates of persisting ones. Under drought, growing taxa accounted for only 4% of the total community as compared to 35% in the controls. Drought-tolerant communities were dominated by specialized members of the Actinobacteriota, particularly the genus Streptomyces. Six years of pre-exposure to future climate conditions (3 °C warming and + 300 ppm atmospheric CO2) alleviated drought effects on microbial growth, through more drought-tolerant taxa across major phyla, accounting for 9% of the total community. Our results provide insights into the response of active microbes to drought today and in a future climate, and highlight the importance of studying drought in combination with future climate conditions to capture interactive effects and improve predictions of future soil-climate feedbacks.

Resource partitioning and amino acid assimilation in a terrestrial geothermal spring.

High-temperature geothermal springs host simplified microbial communities; however, the activities of individual microorganisms and their roles in the carbon cycle in nature are not well understood. Here, quantitative stable isotope probing (qSIP) was used to track the assimilation of 13C-acetate and 13C-aspartate into DNA in 74 °C sediments in Gongxiaoshe Hot Spring, Tengchong, China. This revealed a community-wide preference for aspartate and a tight coupling between aspartate incorporation into DNA and the proliferation of aspartate utilizers during labeling. Both 13C incorporation into DNA and changes in the abundance of taxa during incubations indicated strong resource partitioning and a significant phylogenetic signal for aspartate incorporation. Of the active amplicon sequence variants (ASVs) identified by qSIP, most could be matched with genomes from Gongxiaoshe Hot Spring or nearby springs with an average nucleotide similarity of 99.4%. Genomes corresponding to aspartate primary utilizers were smaller, near-universally encoded polar amino acid ABC transporters, and had codon preferences indicative of faster growth rates. The most active ASVs assimilating both substrates were not abundant, suggesting an important role for the rare biosphere in the community response to organic carbon addition. The broad incorporation of aspartate into DNA over acetate by the hot spring community may reflect dynamic cycling of cell lysis products in situ or substrates delivered during monsoon rains and may reflect N limitation.

The predictive power of phylogeny on growth rates in soil bacterial communities.

Predicting ecosystem function is critical to assess and mitigate the impacts of climate change. Quantitative predictions of microbially mediated ecosystem processes are typically uninformed by microbial biodiversity. Yet new tools allow the measurement of taxon-specific traits within natural microbial communities. There is mounting evidence of a phylogenetic signal in these traits, which may support prediction and microbiome management frameworks. We investigated phylogeny-based trait prediction using bacterial growth rates from soil communities in Arctic, boreal, temperate, and tropical ecosystems. Here we show that phylogeny predicts growth rates of soil bacteria, explaining an average of 31%, and up to 58%, of the variation within ecosystems. Despite limited overlap in community composition across these ecosystems, shared nodes in the phylogeny enabled ancestral trait reconstruction and cross-ecosystem predictions. Phylogenetic relationships could explain up to 38% (averaging 14%) of the variation in growth rates across the highly disparate ecosystems studied. Our results suggest that shared evolutionary history contributes to similarity in the relative growth rates of related bacteria in the wild, allowing phylogeny-based predictions to explain a substantial amount of the variation in taxon-specific functional traits, within and across ecosystems.

Long-term elevated precipitation induces grassland soil carbon loss via microbe-plant-soil interplay.

Global climate models predict that the frequency and intensity of precipitation events will increase in many regions across the world. However, the biosphere-climate feedback to elevated precipitation (eP) remains elusive. Here, we report a study on one of the longest field experiments assessing the effects of eP, alone or in combination with other climate change drivers such as elevated CO2 (eCO2 ), warming and nitrogen deposition. Soil total carbon (C) decreased after a decade of eP treatment, while plant root production decreased after 2 years. To explain this asynchrony, we found that the relative abundances of fungal genes associated with chitin and protein degradation increased and were positively correlated with bacteriophage genes, suggesting a potential viral shunt in C degradation. In addition, eP increased the relative abundances of microbial stress tolerance genes, which are essential for coping with environmental stressors. Microbial responses to eP were phylogenetically conserved. The effects of eP on soil total C, root production, and microbes were interactively affected by eCO2 . Collectively, we demonstrate that long-term eP induces soil C loss, owing to changes in microbial community composition, functional traits, root production, and soil moisture. Our study unveils an important, previously unknown biosphere-climate feedback in Mediterranean-type water-limited ecosystems, namely how eP induces soil C loss via microbe-plant-soil interplay.

Using source-associated mobile genetic elements to identify zoonotic extraintestinal E. coli infections.

A one-health perspective may provide new and actionable information about Escherichia coli transmission. E. coli colonizes a broad range of vertebrates, including humans and food-production animals, and is a leading cause of bladder, kidney, and bloodstream infections in humans. Substantial evidence supports foodborne transmission of pathogenic E. coli strains from food animals to humans. However, the relative contribution of foodborne zoonotic E. coli (FZEC) to the human extraintestinal disease burden and the distinguishing characteristics of such strains remain undefined. Using a comparative genomic analysis of a large collection of contemporaneous, geographically-matched clinical and meat-source E. coli isolates (n = 3111), we identified 17 source-associated mobile genetic elements - predominantly plasmids and bacteriophages - and integrated them into a novel Bayesian latent class model to predict the origins of clinical E. coli isolates. We estimated that approximately 8 % of human extraintestinal E. coli infections (mostly urinary tract infections) in our study population were caused by FZEC. FZEC strains were equally likely to cause symptomatic disease as non-FZEC strains. Two FZEC lineages, ST131-H22 and ST58, appeared to have particularly high virulence potential. Our findings imply that FZEC strains collectively cause more urinary tract infections than does any single non-E. coli uropathogenic species (e.g., Klebsiella pneumoniae). Our novel approach can be applied in other settings to identify the highest-risk FZEC strains, determine their sources, and inform new one-health strategies to decrease the heavy public health burden imposed by extraintestinal E. coli infections.

Microbial carbon use efficiency promotes global soil carbon storage.

Soils store more carbon than other terrestrial ecosystems1,2. How soil organic carbon (SOC) forms and persists remains uncertain1,3, which makes it challenging to understand how it will respond to climatic change3,4. It has been suggested that soil microorganisms play an important role in SOC formation, preservation and loss5-7. Although microorganisms affect the accumulation and loss of soil organic matter through many pathways4,6,8-11, microbial carbon use efficiency (CUE) is an integrative metric that can capture the balance of these processes12,13. Although CUE has the potential to act as a predictor of variation in SOC storage, the role of CUE in SOC persistence remains unresolved7,14,15. Here we examine the relationship between CUE and the preservation of SOC, and interactions with climate, vegetation and edaphic properties, using a combination of global-scale datasets, a microbial-process explicit model, data assimilation, deep learning and meta-analysis. We find that CUE is at least four times as important as other evaluated factors, such as carbon input, decomposition or vertical transport, in determining SOC storage and its spatial variation across the globe. In addition, CUE shows a positive correlation with SOC content. Our findings point to microbial CUE as a major determinant of global SOC storage. Understanding the microbial processes underlying CUE and their environmental dependence may help the prediction of SOC feedback to a changing climate.

Hyperactive nanobacteria with host-dependent traits pervade Omnitrophota.

Candidate bacterial phylum Omnitrophota has not been isolated and is poorly understood. We analysed 72 newly sequenced and 349 existing Omnitrophota genomes representing 6 classes and 276 species, along with Earth Microbiome Project data to evaluate habitat, metabolic traits and lifestyles. We applied fluorescence-activated cell sorting and differential size filtration, and showed that most Omnitrophota are ultra-small (~0.2 µm) cells that are found in water, sediments and soils. Omnitrophota genomes in 6 classes are reduced, but maintain major biosynthetic and energy conservation pathways, including acetogenesis (with or without the Wood-Ljungdahl pathway) and diverse respirations. At least 64% of Omnitrophota genomes encode gene clusters typical of bacterial symbionts, suggesting host-associated lifestyles. We repurposed quantitative stable-isotope probing data from soils dominated by andesite, basalt or granite weathering and identified 3 families with high isotope uptake consistent with obligate bacterial predators. We propose that most Omnitrophota inhabit various ecosystems as predators or parasites.

Life history strategies among soil bacteria-dichotomy for few, continuum for many.

Study of life history strategies may help predict the performance of microorganisms in nature by organizing the complexity of microbial communities into groups of organisms with similar strategies. Here, we tested the extent that one common application of life history theory, the copiotroph-oligotroph framework, could predict the relative population growth rate of bacterial taxa in soils from four different ecosystems. We measured the change of in situ relative growth rate to added glucose and ammonium using both 18O-H2O and 13C quantitative stable isotope probing to test whether bacterial taxa sorted into copiotrophic and oligotrophic groups. We saw considerable overlap in nutrient responses across most bacteria regardless of phyla, with many taxa growing slowly and few taxa that grew quickly. To define plausible life history boundaries based on in situ relative growth rates, we applied Gaussian mixture models to organisms' joint 18O-13C signatures and found that across experimental replicates, few taxa could consistently be assigned as copiotrophs, despite their potential for fast growth. When life history classifications were assigned based on average relative growth rate at varying taxonomic levels, finer resolutions (e.g., genus level) were significantly more effective in capturing changes in nutrient response than broad taxonomic resolution (e.g., phylum level). Our results demonstrate the difficulty in generalizing bacterial life history strategies to broad lineages, and even to single organisms across a range of soils and experimental conditions. We conclude that there is a continued need for the direct measurement of microbial communities in soil to advance ecologically realistic frameworks.

Distinct Growth Responses of Tundra Soil Bacteria to Short-Term and Long-Term Warming.

Increases in Arctic temperatures have thawed permafrost and accelerated tundra soil microbial activity, releasing greenhouse gases that amplify climate warming. Warming over time has also accelerated shrub encroachment in the tundra, altering plant input abundance and quality, and causing further changes to soil microbial processes. To better understand the effects of increased temperature and the accumulated effects of climate change on soil bacterial activity, we quantified the growth responses of individual bacterial taxa to short-term warming (3 months) and long-term warming (29 years) in moist acidic tussock tundra. Intact soil was assayed in the field for 30 days using 18O-labeled water, from which taxon-specific rates of 18O incorporation into DNA were estimated as a proxy for growth. Experimental treatments warmed the soil by approximately 1.5°C. Short-term warming increased average relative growth rates across the assemblage by 36%, and this increase was attributable to emergent growing taxa not detected in other treatments that doubled the diversity of growing bacteria. However, long-term warming increased average relative growth rates by 151%, and this was largely attributable to taxa that co-occurred in the ambient temperature controls. There was also coherence in relative growth rates within broad taxonomic levels with orders tending to have similar growth rates in all treatments. Growth responses tended to be neutral in short-term warming and positive in long-term warming for most taxa and phylogenetic groups co-occurring across treatments regardless of phylogeny. Taken together, growing bacteria responded distinctly to short-term and long-term warming, and taxa growing in each treatment exhibited deep phylogenetic organization. IMPORTANCE Soil carbon stocks in the tundra and underlying permafrost have become increasingly vulnerable to microbial decomposition due to climate change. The microbial responses to Arctic warming must be understood in order to predict the effects of future microbial activity on carbon balance in a warming Arctic. In response to our warming treatments, tundra soil bacteria grew faster, consistent with increased rates of decomposition and carbon flux to the atmosphere. Our findings suggest that bacterial growth rates may continue to increase in the coming decades as faster growth is driven by the accumulated effects of long-term warming. Observed phylogenetic organization of bacterial growth rates may also permit taxonomy-based predictions of bacterial responses to climate change and inclusion into ecosystem models.

Nutrients strengthen density dependence of per-capita growth and mortality rates in the soil bacterial community.

Density dependence in an ecological community has been observed in many macro-organismal ecosystems and is hypothesized to maintain biodiversity but is poorly understood in microbial ecosystems. Here, we analyze data from an experiment using quantitative stable isotope probing (qSIP) to estimate per-capita growth and mortality rates of bacterial populations in soils from several ecosystems along an elevation gradient which were subject to nutrient addition of either carbon alone (glucose; C) or carbon with nitrogen (glucose + ammonium-sulfate; C + N). Across all ecosystems, we found that higher population densities, quantified by the abundance of genomes per gram of soil, had lower per-capita growth rates in C + N-amended soils. Similarly, bacterial mortality rates in C + N-amended soils increased at a significantly higher rate with increasing population size than mortality rates in control and C-amended soils. In contrast to the hypothesis that density dependence would promote or maintain diversity, we observed significantly lower bacterial diversity in soils with stronger negative density-dependent growth. Here, density dependence was significantly but weakly responsive to nutrients and was not associated with higher bacterial diversity.

Plugging the leaks: antibiotic resistance at human-animal interfaces in low-resource settings.

Antibiotic resistance is one of the greatest public health challenges of our time. International efforts to curb resistance have largely focused on drug development and limiting unnecessary antibiotic use. However, in areas where water, sanitation, and hygiene infrastructure is lacking, we propose that bacterial flow between humans and animals can exacerbate the emergence and spread of resistant pathogens. Here, we describe the consequences of poor environmental controls by comparing mobile resistance elements among Escherichia coli recovered from humans and meat in Cambodia, a middle-income country with substantial human-animal connectivity and unregulated antibiotic use. We identified identical mobile resistance elements and a conserved transposon region that were widely dispersed in both humans and animals, a phenomenon rarely observed in high-income settings. Our findings indicate that plugging leaks at human-animal interfaces should be a critical part of addressing antibiotic resistance in low- and especially middle-income countries.

In situ diversity of metabolism and carbon use efficiency among soil bacteria.

The central carbon (C) metabolic network harvests energy to power the cell and feed biosynthesis for growth. In pure cultures, bacteria use some but not all of the network's major pathways, such as glycolysis and pentose phosphate and Entner-Doudoroff pathways. However, how these pathways are used in microorganisms in intact soil communities is unknown. Here, we analyzed the incorporation of 13C from glucose isotopomers into phospholipid fatty acids. We showed that groups of Gram-positive and Gram-negative bacteria in an intact agricultural soil used different pathways to metabolize glucose. They also differed in C use efficiency (CUE), the efficiency with which a substrate is used for biosynthesis. Our results provide experimental evidence for diversity among microbes in the organization of their central carbon metabolic network and CUE under in situ conditions. These results have important implications for our understanding of how community composition affects soil C cycling and organic matter formation.

Quantitative Stable-Isotope Probing (qSIP) with Metagenomics Links Microbial Physiology and Activity to Soil Moisture in Mediterranean-Climate Grassland Ecosystems.

The growth and physiology of soil microorganisms, which play vital roles in biogeochemical cycling, are shaped by both current and historical soil environmental conditions. Here, we developed and applied a genome-resolved metagenomic implementation of quantitative stable isotope probing (qSIP) with an H218O labeling experiment to identify actively growing soil microorganisms and their genomic capacities. qSIP enabled measurement of taxon-specific growth because isotopic incorporation into microbial DNA requires production of new genome copies. We studied three Mediterranean grassland soils across a rainfall gradient to evaluate the hypothesis that historic precipitation levels are an important factor controlling trait selection. We used qSIP-informed genome-resolved metagenomics to resolve the active subset of soil community members and identify their characteristic ecophysiological traits. Higher year-round precipitation levels correlated with higher activity and growth rates of flagellar motile microorganisms. In addition to heavily isotopically labeled bacteria, we identified abundant isotope-labeled phages, suggesting phage-induced cell lysis likely contributed to necromass production at all three sites. Further, there was a positive correlation between phage activity and the activity of putative phage hosts. Contrary to our expectations, the capacity to decompose the diverse complex carbohydrates common in soil organic matter or oxidize methanol and carbon monoxide were broadly distributed across active and inactive bacteria in all three soils, implying that these traits are not highly selected for by historical precipitation. IMPORTANCE Soil moisture is a critical factor that strongly shapes the lifestyle of soil organisms by changing access to nutrients, controlling oxygen diffusion, and regulating the potential for mobility. We identified active microorganisms in three grassland soils with similar mineral contexts, yet different historic rainfall inputs, by adding water labeled with a stable isotope and tracking that isotope in DNA of growing microbes. By examining the genomes of active and inactive microorganisms, we identified functions that are enriched in growing organisms, and showed that different functions were selected for in different soils. Wetter soil had higher activity of motile organisms, but activity of pathways for degradation of soil organic carbon compounds, including simple carbon substrates, were comparable for all three soils. We identified many labeled, and thus active bacteriophages (viruses that infect bacteria), implying that the cells they killed contributed to soil organic matter. The activity of these bacteriophages was significantly correlated with activity of their hosts.

Nitrogen and water availability control plant carbon storage with warming.

Plants may slow global warming through enhanced growth, because increased levels of photosynthesis stimulate the land carbon (C) sink. However, how climate warming affects plant C storage globally and key drivers determining the response of plant C storage to climate warming remains unclear, causing uncertainty in climate projections. We performed a comprehensive meta-analysis, compiling 393 observations from 99 warming studies to examine the global patterns of plant C storage responses to climate warming and explore the key drivers. Warming significantly increased total biomass (+8.4 %), aboveground biomass (+12.6 %) and belowground biomass (+10.1 %). The effect of experimental warming on plant biomass was best explained by the availability of soil nitrogen (N) and water. Across the entire dataset, warming-induced changes in total, aboveground and belowground biomass all positively correlated with soil C:N ratio, an indicator of soil N availability. In addition, warming stimulated plant biomass more strongly in humid than in dry ecosystems, and warming tended to decrease root:shoot ratios at high soil C:N ratios. Together, these results suggest dual controls of warming effects on plant C storage; warming increases plant growth in ecosystems where N is limiting plant growth, but it reduces plant growth where water availability is limiting plant growth.

Long-term nitrogen deposition enhances microbial capacities in soil carbon stabilization but reduces network complexity.

BACKGROUND: Anthropogenic activities have increased the inputs of atmospheric reactive nitrogen (N) into terrestrial ecosystems, affecting soil carbon stability and microbial communities. Previous studies have primarily examined the effects of nitrogen deposition on microbial taxonomy, enzymatic activities, and functional processes. Here, we examined various functional traits of soil microbial communities and how these traits are interrelated in a Mediterranean-type grassland administrated with 14 years of 7 g m-2 year-1 of N amendment, based on estimated atmospheric N deposition in areas within California, USA, by the end of the twenty-first century. RESULTS: Soil microbial communities were significantly altered by N deposition. Consistent with higher aboveground plant biomass and litter, fast-growing bacteria, assessed by abundance-weighted average rRNA operon copy number, were favored in N deposited soils. The relative abundances of genes associated with labile carbon (C) degradation (e.g., amyA and cda) were also increased. In contrast, the relative abundances of functional genes associated with the degradation of more recalcitrant C (e.g., mannanase and chitinase) were either unchanged or decreased. Compared with the ambient control, N deposition significantly reduced network complexity, such as average degree and connectedness. The network for N deposited samples contained only genes associated with C degradation, suggesting that C degradation genes became more intensely connected under N deposition. CONCLUSIONS: We propose a conceptual model to summarize the mechanisms of how changes in above- and belowground ecosystems by long-term N deposition collectively lead to more soil C accumulation. Video Abstract.