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Greenlon, A.

Publications and source records attributed to Greenlon, A..

8 recordsLinked to original sources

Drought reduces formation, but enhances persistence, of mineral-associated organic matter in a grassland soil

Drought effects are pervasive in many terrestrial ecosystems, yet little is known about the impact of drought on the transformation of plant C inputs to mineral-associated organic matter (MAOM) - the largest and slowest-cycling pool of organic carbon (C) on land. Using 13C-CO2 greenhouse labeling chambers, we tracked the formation of 13C-MAOM derived from Avena barbata living root inputs (13C-rhizodeposits) versus A. barbata decaying root inputs (13C-root detritus) under normal moisture and spring drought conditions in a semi-arid grassland soil, and then tested the durability of this 13C-MAOM in a subsequent persistence assay. Overall, drought reduced formation of MAOM - both per gram of soil and across the entire soil profile. Notably, drought conditions enhanced the persistence of MAOM derived from root detritus, though not of MAOM derived from rhizodeposition. Drought had the most pronounced effect on MAOM accrual from rhizodeposition late in plant development (week 12) whereas it had the most pronounced effect on MAOM accrual from root detritus early in root decomposition (week 4). These temporal responses were associated with distinct trajectories in microbial community-level growth rates, the average mass of OM compounds, and the number of unique metabolites within each habitat. Our results provide mechanistic evidence that drought reduces overall formation of MAOM but can enhance its persistence in a grassland soil.

ecology↗

Specialist Generalist Trade Offs in Microbial Growth Rates Across Soil Habitats

Microbial ecological strategies are shaped by a fundamental trade-off: is it better to specialize and thrive in a narrow niche or generalize and persist across diverse environments? In soils, this trade-off is particularly relevant in the rhizosphere and detritusphere, where microorganisms encounter distinct resource inputs from living and decaying roots. Using H {superscript 1} O quantitative stable isotope probing (qSIP), we measured in situ bacterial and fungal growth rates in the rhizosphere, the root detritusphere, and in the combined presence of rhizosphere + root detritus to test whether specialists--microbes growing in a single habitat--grow faster than generalists that persist across multiple environments. Specialists grew consistently faster than generalists, suggesting a trade-off between the breadth of environmental conditions a microorganism can tolerate and its ability to grow quickly in a specific habitat. This cost to broad niche adaptation was apparent for bacteria, but growth rates of fungal saprotrophs varied little between specialists and generalists, reflecting how fundamental differences in life-history strategies between bacteria and fungi can shape microbial responses to resource availability and habitat heterogeneity. Net relatedness and nearest taxon indices indicated total bacterial communities were phylogenetically clustered while specialist and generalist communities were phylogenetically random, suggesting that functional traits, not lineage, best predict ecological strategy. In annual grassland soils, fast-growing specialists may dominate ecosystem processes when resources abound, and slow-growing generalists may sustain element transformations when conditions shift; understanding this interplay is key to predicting soil-carbon trajectories.

microbiology↗

Divergent microbial traits influence the transformation of living versus dead root inputs to soil carbon

Soil microorganisms influence the global carbon cycle by transforming plant inputs into soil organic carbon (SOC), but the microbial traits that facilitate this process are unresolved. While current theory and biogeochemical models suggest microbial carbon-use efficiency and growth rate are positive predictors of SOC, recent observations demonstrate these relationships can be positive, negative, or neutral. To parse these contradictory effects, we used a 13C-labeling experiment to test whether different microbial traits influenced the transformation of plant C into SOC within the microbial habitats surrounding living root inputs (rhizosphere) versus decaying root litter (detritusphere), under both normal soil moisture and droughted conditions. In the rhizosphere, bacterial-dominated communities with fast growth, high carbon-use efficiency, and high production of extracellular polymeric substances formed microbial-derived SOC under normal moisture conditions. However, in the detritusphere - and the rhizosphere under drought - more fungal-dominated communities with slower growth but higher exoenzyme activity formed plant-derived SOC. These findings emphasize that microbial traits linked with SOC accrual are not universal, but contingent on how microorganisms allocate carbon under different resource conditions and environmental stressors.

ecology↗

Functional succession of actively growing soil microorganisms during rewetting is shaped by precipitation history

Rewetting of seasonally dry soils induces a burst of microbial activity and carbon mineralization that changes nutrient availability and leads to succession. Yet the microbial functions that underpin this succession are not well described. Further, its unclear how previous precipitation frames microbial capacities after rewetting and how long these effects persist. We used isotopically-labeled water to rewet seasonally dry annual grassland soil that experienced either mean annual or reduced precipitation during the previous two years, and sampled at five subsequent time points. We used quantitative stable isotope probing (qSIP)-informed genome- resolved metagenomics to identify growing microorganisms, predict their capabilities, and analyze how these traits differed over time and between precipitation treatments. Organisms that grew after wetup were more abundant than non-growing organisms prior to the wet-up, suggesting that traits that initiate succession are pre-defined at the end of the prior plant growing season or via survival over the summer. Fast-growing organisms had fewer carbohydrate active enzyme (CAZy) genes per genome than slower-growing organisms, suggesting that although fast-growers were capable of degrading complex C, they may not specialize in this process. Differential abundance of CAZy genes in growing organisms throughout the succession implies that substrate availability varied with time. In contrast, the abundance of peptidases in growing organisms differed between precipitation treatments, but not over time following wet-up. Before wet-up, the soil organisms gene inventories were different between the two precipitation treatments. Surprisingly, this legacy effect waned after just one week. Thus, pre-wetup differences in microbial functional capacity converged shortly after rewetting.

microbiology↗

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 likely dependent on current and prior soil moisture levels. Here, we developed and applied a genome-resolved metagenomic implementation of quantitative stable isotope probing (qSIP) to an H218O labeling experiment to determine which microbial community members, and with what capacities, are growing under in situ conditions. 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 an active subset of soil community members and identify the ecophysiological traits that characterize them. Higher year-round precipitation levels correlated with higher activity and growth rates of flagellar motile microorganisms. In addition to bacteria that were heavily isotopically labeled, 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 capabilities to decompose the diverse complex carbohydrates common in soil necromass 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.

microbiology↗

Active communities and growth of soil microorganisms are framed by mean annual precipitation in three California annual grasslands

Earth system models project altered precipitation regimes across much of the globe; in California, the winter wet season is predicted to extend into spring, and the summer dry period to lengthen. How these precipitation trends will affect microbial traits and soil carbon (C) cycling is a key knowledge gap. Specifically, we do not have a mechanistic understanding of the linkages between soil moisture legacy effects, microbial population dynamics and soil C persistence. Using quantitative stable isotope probing (qSIP), we compared total and growing soil microbial communities across three California annual grasslands that span a rainfall gradient yet developed on similar parent material. We also assessed multiple edaphic variables, including the radiocarbon (14C) age of soil C, and found soil C turnover time increased with annual precipitation, but that soil microbes respired recently-fixed C regardless of site rainfall history. Samples were assayed in the wet season, when we expected environmental conditions would be most similar across sites. We hypothesized that growing communities would be more compositionally similar across the gradient than the total background microbiome. We also predicted that the long-term legacy effect of soil water limitation would be reflected in a lower community growth capacity at the driest site. We found that the proportion of the total community that was detected as growing was 28%, 48% and 58% at the wet, intermediate and dry sites, respectively. The composition of growing communities strongly resembled that of total communities, and growing communities were no more similar across the gradient than total communities, indicating a strong effect of climate of the structure of growing microbial communities. Members of three phyla, Acidobacteria, Actinobacteria, and Proteobacteria, were responsible for [~]79% of the cumulative 18O assimilation and 80% of all taxa that we defined as growers. Bacterial growth rates were low at the driest site relative to the intermediate and wettest sites. Reduced growth at the driest site was observed across major phyla, including the Actinobacteria, Acidobacteria, Bacteroidetes, Gemmatimonadetes and Proteobacteria. Microbial communities at the driest site displayed phylogenetic clustering, suggesting that climate history impacts microbial growth through environmental filtering for slow growing taxa. Taxonomic identity was a strong predictor of growth, such that the growth rates of a taxon at one site predicted its growth rates at the others. This cross-site coherence in growth is likely a consequence of genetically determined physiological traits, and is consistent with the idea that evolutionary history influences growth rate.

ecology↗

The Functional Significance of Bacterial Predators

Predation structures food webs, influences energy flow, and alters rates and pathways of nutrient cycling through ecosystems, effects that are well documented for macroscopic predators. In the microbial world, predatory bacteria are common, yet little is known about their rates of growth and roles in energy flows through microbial food webs, in part because these are difficult to quantify. Here, we show that growth and carbon uptake were higher in predatory bacteria compared to non-predatory bacteria, a finding across 15 sites, synthesizing 82 experiments and over 100,000 taxon-specific measurements of element flow into newly synthesized bacterial DNA. Obligate predatory bacteria grew 36% faster and assimilated carbon at rates 211% higher than non-predatory bacteria. These differences were less pronounced for facultative predators (6% higher growth rates, 17% higher carbon assimilation rates), though high growth and carbon assimilation rates were observed for some facultative predators, such as members of the genera Lysobacter and Cytophaga, both capable of gliding motility and wolfpack hunting behavior. Added carbon substrates disproportionately stimulated growth of obligate predators, with responses 63% higher than non-predators for the Bdellovibrionales and 81% higher for the Vampirovibrionales, whereas responses of facultative predators to substrate addition were no different from non-predators. This finding supports ecological theory that higher productivity increases predator control of lower trophic levels. These findings also indicate that the functional significance of bacterial predators increases with energy flow, and that predatory bacteria influence element flow through microbial food webs.

ecology↗

Measurement error and resolution in quantitative stable isotope probing: implications for experimental design

Quantitative stable isotope probing (qSIP) estimates the degree of incorporation of an isotope tracer into nucleic acids of metabolically active organisms and can be applied to microorganisms growing in complex communities, such as the microbiomes of soil or water. As such, qSIP has the potential to link microbial biodiversity and biogeochemistry. As with any technique involving quantitative estimation, qSIP involves measurement error; a more complete understanding of error, precision and statistical power will aid in the design of qSIP experiments and interpretation of qSIP data. We used several existing qSIP datasets of microbial communities found in soil and water to evaluate how variance in the estimate of isotope incorporation depends on organism abundance and on the resolution of the density fractionation scheme. We also assessed statistical power for replicated qSIP studies, and sensitivity and specificity for unreplicated designs. We found that variance declines as taxon abundance increases. Increasing the number of density fractions reduces variance, although the benefit of added fractions declines as the number of fractions increases. Specifically, nine fractions appear to be a reasonable tradeoff between cost and precision for most qSIP applications. Increasing replication improves power and reduces the minimum detectable threshold for inferring isotope uptake to 5 atom%. Finally, we provide evidence for the importance of internal standards to calibrate the %GC to mean weighted density regression per sample. These results should benefit those designing future SIP experiments, and provide a reference for metagenomic SIP applications where financial and computational limitations constrain experimental scope. ImportanceOne of the biggest challenges in microbial ecology is correlating the identity of microorganisms with the roles they fulfill in natural environmental systems. Studies of microbes in pure culture reveal much about genomic content and potential functions, but may not reflect an organisms activity within its natural community. Culture-independent studies supply a community-wide view of composition and function in the context of community interactions, but fail to link the two. Quantitative stable isotope probing (qSIP) is a method that can link the identity and function of specific microbes within a naturally occurring community. Here we explore how the resolution of density-gradient fractionation affects the error and precision of qSIP results, how they may be improved via additional replication, and cost-benefit balanced scenarios for SIP experimental design.

microbiology↗