Zachary T. Aanderud

Mapping the niche space of soil microorganisms using taxonomy and traits

The biodiversity of microbial communities has important implications for the stability and functioning of ecosystem processes. Yet, very little is known about the environmental factors that define the microbial niche and how this influences the composition and activity of microbial communities. In this study, we derived niche parameters from physiological response curves that quantified microbial respiration for a diverse collection of soil bacteria and fungi along a soil moisture gradient. On average, soil microorganisms had relatively dry optima (0.3 MPa) and were capable of respiring under low water potentials (-2.0 MPa). Within their limits of activity, microorganisms exhibited a wide range of responses, suggesting that some taxa may be able to coexist by partitioning the moisture niche axis. For example, we identified dry-adapted generalists that tolerated a broad range of water potentials, along with wet-adapted specialists with metabolism restricted to less-negative water potentials. These contrasting ecological strategies had a phylogenetic signal at a coarse taxonomic level (phylum), suggesting that the moisture niche of soil microorganisms is highly conserved. In addition, variation in microbial responses along the moisture gradient was linked to the distribution of several functional traits. In particular, strains that were capable of producing biofilms had drier moisture optima and wider niche breadths. However, biofilm production appeared to come at a cost that was reflected in a prolonged lag time prior to exponential growth, suggesting that there is a trade-off associated with traits that allow microorganisms to contend with moisture stress. Together, we have identified functional groups of microorganisms that will help predict the structure and functioning of microbial communities under contrasting soil moisture regimes.

Linking nitrogen partitioning and species abundance to invasion resistance in the Great Basin

Resource partitioning has been suggested as an important mechanism of invasion resistance. The relative importance of resource partitioning for invasion resistance, however, may depend on how species abundance is distributed in the plant community. This study had two objectives. First, we quantified the degree to which one resource, nitrogen (N), is partitioned by time, depth and chemical form among coexisting species from different functional groups by injecting 15N into soils around the study species three times during the growing season, at two soil depths and as two chemical forms. A watering treatment also was applied to evaluate the impact of soil water content on N partitioning. Second, we examined the degree to which native functional groups contributed to invasion resistance by seeding a non-native annual grass into plots where bunchgrasses, perennial forbs or annual forbs had been removed. Bunchgrasses and forbs differed in timing, depth and chemical form of N capture, and these patterns of N partitioning were not affected by soil water content. However, when we incorporated abundance (biomass) with these relative measures of N capture to determine N sequestration by the community there was no evidence suggesting that functional groups partitioned different soil N pools. Instead, dominant bunchgrasses acquired the most N from all soil N pools. Consistent with these findings we also found that bunchgrasses were the only functional group that inhibited annual grass establishment. At natural levels of species abundance, N partitioning may facilitate coexistence but may not necessarily contribute to N sequestration and invasion resistance by the plant community. This suggests that a general mechanism of invasion resistance may not be expected across systems. Instead, the key mechanism of invasion resistance within a system may depend on trait variation among coexisting species and on how species abundance is distributed in the system.

Resuscitation of the rare biosphere contributes to pulses of ecosystem activity

Dormancy is a life history trait that may have important implications for linking microbial communities to the functioning of natural and managed ecosystems. Rapid changes in environmental cues may resuscitate dormant bacteria and create pulses of ecosystem activity. In this study, we used heavy-water (H182O) stable isotope probing (SIP) to identify fast-growing bacteria that were associated with pulses of trace gasses (CO2, CH4, and N2O) from different ecosystems [agricultural site, grassland, deciduous forest, and coniferous forest (CF)] following a soil-rewetting event. Irrespective of ecosystem type, a large fraction (69–74%) of the bacteria that responded to rewetting were below detection limits in the dry soils. Based on the recovery of sequences, in just a few days, hundreds of rare taxa increased in abundance and in some cases became dominant members of the rewetted communities, especially bacteria belonging to the Sphingomonadaceae, Comamonadaceae, and Oxalobacteraceae. Resuscitation led to dynamic shifts in the rank abundance of taxa that caused previously rare bacteria to comprise nearly 60% of the sequences that were recovered in rewetted communities. This rapid turnover of the bacterial community corresponded with a 5–20-fold increase in the net production of CO2 and up to a 150% reduction in the net production of CH4 from rewetted soils. Results from our study demonstrate that the rare biosphere may account for a large and dynamic fraction of a community that is important for the maintenance of bacterial biodiversity. Moreover, our findings suggest that the resuscitation of rare taxa from seed banks contribute to ecosystem functioning.

Validation of heavy-water stable isotope probing for the characterization of rapidly responding soil bacteria.

ABSTRACT Rapid responses of bacteria to sudden changes in their environment can have important implications for the structure and function of microbial communities. In this study, we used heavy-water stable isotope probing (H2 18O-SIP) to identify bacteria that respond to soil rewetting. First, we conducted experiments to address uncertainties regarding the H2 18O-SIP method. Using liquid chromatography-mass spectroscopy (LC-MS), we determined that oxygen from H2 18O was incorporated into all structural components of DNA. Although this incorporation was uneven, we could effectively separate 18O-labeled and unlabeled DNAs derived from laboratory cultures and environmental samples that were incubated with H2 18O. We found no evidence for ex vivo exchange of oxygen atoms between DNA and extracellular H2O, suggesting that 18O incorporation into DNA is relatively stable. Furthermore, the rate of 18O incorporation into bacterial DNA was high (within 48 to 72 h), coinciding with pulses of CO2 generated from soil rewetting. Second, we examined shifts in the bacterial composition of grassland soils following rewetting, using H2 18O-SIP and bar-coded pyrosequencing of 16S rRNA genes. For some groups of soil bacteria, we observed coherent responses at a relatively course taxonomic resolution. Following rewetting, the relative recovery of Alphaproteobacteria, Betaproteobacteria, and Gammaproteobacteria increased, while the relative recovery of Chloroflexi and Deltaproteobacteria decreased. Together, our results suggest that H2 18O-SIP is effective at identifying metabolically active bacteria that influence soil carbon dynamics. Our results contribute to the ecological classification of soil bacteria while providing insight into some of the functional traits that influence the structure and function of microbial communities under dynamic soil moisture regimes.

Plants Mediate the Sensitivity of Soil Respiration to Rainfall Variability

Soil respiration from grasslands plays a critical role in determining carbon dioxide (CO2) feedbacks between soils and the atmosphere. In these often mesic systems, soil moisture and temperature tend to co-regulate soil respiration. Increasing variance of rainfall patterns may alter aboveground–belowground interactions and have important implications for the sensitivity of soil respiration to fluctuations in moisture and temperature. We conducted a set of field experiments to evaluate the independent and interactive effects of rainfall variability and plant–soil processes on respiration dynamics. Plant removal had strong effects on grassland soils, which included altered CO2 flux owing to absence of root respiration; increased soil moisture and temperature; and reduced availability of dissolved organic carbon (DOC) for heterotrophic respiration by microorganisms. These plant-mediated effects interacted with our rainfall variability treatments to determine the sensitivity of soil respiration to both moisture and temperature. Using time-series multiple regression, we found that plants dampened the sensitivity of respiration to moisture under high variability rainfall treatments, which may reflect the relative stability of root contributions to total soil respiration. In contrast, plants increased the sensitivity of respiration to temperature under low variability rainfall treatment suggesting that the environmental controls on soil CO2 dynamics in mesic habitats may be context dependent. Our results provide insight into the aboveground–belowground mechanisms controlling respiration in grasslands under variable rainfall regimes, which may be important for predicting CO2 dynamics under current and future climate scenarios.

Vegetation Response to Piñon and Juniper Tree Shredding

ABSTRACT Piñon (Pinus spp.) and juniper (Juniperus spp.) expansion and infilling in sagebrush (Artemisia L.) steppe communities can lead to high-severity fire and annual weed dominance. To determine vegetation response to fuel reduction by tree mastication (shredding) or seeding and then shredding, we measured cover for shrub and herbaceous functional groups on shredded and adjacent untreated areas on 44 sites in Utah. We used mixed model analysis of covariance to determine significant differences among ecological site type (expansion and tree climax) and treatments across a range of pretreatment tree cover as the covariate. Although expansion and tree climax sites differed in cover values for some functional groups, decreasing understory cover with increasing tree cover and increased understory cover with tree reduction was similar for both ecological site types. Shrub cover decreased by 50% when tree cover exceeded 20%. Shredding trees at ≤ 20% cover maintained a mixed shrub (18.6% cover)—perennial herbaceous (17.6% cover) community. Perennial herbaceous cover decreased by 50% when tree cover exceeded 40% but exceeded untreated cover by 11% (20.1% cover) when trees were shredded at 15–90% tree cover. Cheatgrass (Bromus tectorum L.) cover also increased after tree shredding or seeding and then shredding but was much less dominant (< 10% cover) where perennial herbaceous cover exceeded 42%. Sites with high cheatgrass cover on untreated plots had high cheatgrass cover on shredded and seeded-shredded plots. Seeding and then shredding decreased cheatgrass cover compared with shredding alone when implemented at tree cover ≥ 50%. Vegetation responses to shredding on expansion sites were generally similar to those for tree cutting treatments in the SageSTEP study. Shredding or seeding and then shredding should facilitate wildfire suppression, increase resistance to weed dominance, and lead toward greater resilience to disturbance by increasing perennial herbaceous cover.

Bacterial Dormancy Is More Prevalent in Freshwater than Hypersaline Lakes

Bacteria employ a diverse array of strategies to survive under extreme environmental conditions but maintaining these adaptations comes at an energetic cost. If energy reserves drop too low, extremophiles may enter a dormant state to persist. We estimated bacterial dormancy and identified the environmental variables influencing our activity proxy in 10 hypersaline and freshwater lakes across the Western United States. Using ribosomal RNA:DNA ratios as an indicator for bacterial activity, we found that the proportion of the community exhibiting dormancy was 16% lower in hypersaline than freshwater lakes. Based on our indicator variable multiple regression results, saltier conditions in both freshwater and hypersaline lakes increased activity, suggesting that salinity was a robust environmental filter structuring bacterial activity in lake ecosystems. To a lesser degree, higher total phosphorus concentrations reduced dormancy in all lakes. Thus, even under extreme conditions, the competition for resources exerted pressure on activity. Within the compositionally distinct and less diverse hypersaline communities, abundant taxa were disproportionately active and localized in families Microbacteriaceae (Actinobacteria), Nitriliruptoraceae (Actinobacteria), and Rhodobacteraceae (Alphaproteobacteria). Our results are consistent with the view that hypersaline communities are able to capitalize on a seemingly more extreme, yet highly selective, set of conditions and finds that extremophiles may need dormancy less often to thrive and survive.

Rapid adjustment of leaf angle explains how the desert moss, Syntrichia caninervis, copes with multiple resource limitations during rehydration

Although the desert moss Syntrichia caninervis Mitt. is extremely desiccation tolerant, it still requires water and photosynthates for growth. The ecological significance of the leaf angle in maintaining a balance between water and light availability is critical to its survival. Active leaf repositioning balances water and light availability following rehydration. S. caninervis can adjust leaf angles from a steep (84-69°) to a stable level at 30° within 7s after rehydration, obtaining maximum net photosynthetic gain at a shoot relative water content of ~60%. Leaf morphological characters, (leaf hair points, surface papillae and costal anatomy) and ultrastructural changes (chloroplast reordering and loss of lipid reserves as shown by changes in osmiophilic globules) were linked to rapid leaf spreading, water gain and sunlight reflectivity of leaves during rehydration. The high 377.20±91.69 (cm2g-1) surface area to mass ratio was a major factor in facilitating the rapid response to rewetting. Hyaline cells of the leaf base absorbed water, swelled and forced the leaf away from the stem as soon as rehydration commenced. Loss of leaf hair points retards leaf angle adjustment during rehydration.

Exploitation of nutrient-rich soil patches by invasive annual and native perennial grasses.

Abstract Invasion of nutrient-poor habitats might be related to the ability of a species to exploit nutrient-rich microsites. Recent research suggests fast-growing species might have a greater ability to allocate root biomass to nutrient-rich microsites (root foraging precision) than slow-growing species. We examined if differences in relative growth rate (RGR) between invasive and native species were related to differences in foraging precision. We hypothesized that invasive species would: (1) have greater foraging precision than native species but (2) greater foraging precision would come at a cost in terms of root nutrient uptake rate. Foraging precision was evaluated on plants growing in soils with uniform or patchy nutrient distribution. Plants were harvested at a common time and a common developmental stage to separate indirect effects of RGR on foraging. Nutrient uptake rate was examined by exposing plants to a low or high nitrogen pulse. Invasives foraged more precisely than natives but had lower nitrogen uptake rate. Although these results support the idea of a positive relationship between RGR and foraging precision, biomass production in heterogeneous soils showed no relationship to foraging precision. Instead, species with greater RGR produced more biomass and root length across all treatments, allowing greater nutrient capture in heterogeneous soils. Although these results do not exclude a role for proliferation in influencing invasion of nutrient-poor systems or the potential for heterogeneity to influence population processes, these results suggest other traits may have an overriding importance in determining invader success in these systems.

Thermal groundwater contributions of arsenic and other trace elements to the middle Provo River, Utah, USA

Groundwater inputs can impact river water quality but are difficult to disentangle from agricultural, urban, and storm runoff. To better understand the multiple processes affecting water quality, we used major solute and trace element concentrations with continuous measurements of flow rates and specific conductance to track temporal and spatial changes in surface water and groundwater solute inputs into the middle Provo River, located in northern Utah, USA. Thermal groundwater was the most important source of major solutes and trace elements to the middle Provo River, with concentrations of As, B, Cs, Li, Sr, and Rb increasing dramatically (twofold to tenfold) downstream of thermal water inputs in the Snake Creek tributary. Snake Creek accounted for only 20% of the flow to the Provo River but increased the As concentrations ~four-fold. Diffuse groundwater inputs, including thermal water, along the Provo River also contributed a measureable increase in solute concentrations. Mixing calculations indicate that groundwater contributed up to 10% of the total streamflow to the middle Provo River, causing an increase in thermal groundwater-derived trace element concentrations. In addition to natural groundwater inputs, water quality was impacted by anthropogenic trace and major element inputs from surface water tributaries. Nitrate, Ba, and V concentrations increased substantially downstream of agricultural/urban inputs. Specific conductance data showed that tributaries added solutes to the Provo River during runoff events, likely from the washoff of road salts. With evidence of both natural and anthropogenic inputs of trace and major elements to the middle Provo River, our study has implications for understanding water quality in complex coupled human–natural systems and demonstrates the influence of thermal groundwater inputs on water quality where such systems discharge.