Priorities, opportunities, and challenges for integrating microorganisms into Earth system models for climate change prediction.

Climate change jeopardizes human health, global biodiversity, and sustainability of the biosphere. To make reliable predictions about climate change, scientists use Earth system models (ESMs) that integrate physical, chemical, and biological processes occurring on land, the oceans, and the atmosphere. Although critical for catalyzing coupled biogeochemical processes, microorganisms have traditionally been left out of ESMs. Here, we generate a "top 10" list of priorities, opportunities, and challenges for the explicit integration of microorganisms into ESMs. We discuss the need for coarse-graining microbial information into functionally relevant categories, as well as the capacity for microorganisms to rapidly evolve in response to climate-change drivers. Microbiologists are uniquely positioned to collect novel and valuable information necessary for next-generation ESMs, but this requires data harmonization and transdisciplinary collaboration to effectively guide adaptation strategies and mitigation policy.

A trade-off between plant and soil carbon storage under elevated CO2.

Terrestrial ecosystems remove about 30 per cent of the carbon dioxide (CO2) emitted by human activities each year1, yet the persistence of this carbon sink depends partly on how plant biomass and soil organic carbon (SOC) stocks respond to future increases in atmospheric CO2 (refs. 2,3). Although plant biomass often increases in elevated CO2 (eCO2) experiments4-6, SOC has been observed to increase, remain unchanged or even decline7. The mechanisms that drive this variation across experiments remain poorly understood, creating uncertainty in climate projections8,9. Here we synthesized data from 108 eCO2 experiments and found that the effect of eCO2 on SOC stocks is best explained by a negative relationship with plant biomass: when plant biomass is strongly stimulated by eCO2, SOC storage declines; conversely, when biomass is weakly stimulated, SOC storage increases. This trade-off appears to be related to plant nutrient acquisition, in which plants increase their biomass by mining the soil for nutrients, which decreases SOC storage. We found that, overall, SOC stocks increase with eCO2 in grasslands (8 ± 2 per cent) but not in forests (0 ± 2 per cent), even though plant biomass in grasslands increase less (9 ± 3 per cent) than in forests (23 ± 2 per cent). Ecosystem models do not reproduce this trade-off, which implies that projections of SOC may need to be revised.

Sinks for nitrogen inputs in terrestrial ecosystems: a meta-analysis of 15N tracer field studies.

Effects of anthropogenic nitrogen (N) deposition and the ability of terrestrial ecosystems to store carbon (C) depend in part on the amount of N retained in the system and its partitioning among plant and soil pools. We conducted a meta-analysis of studies at 48 sites across four continents that used enriched 15N isotope tracers in order to synthesize information about total ecosystem N retention (i.e., total ecosystem 15N recovery in plant and soil pools) across natural systems and N partitioning among ecosystem pools. The greatest recoveries of ecosystem 15N tracer occurred in shrublands (mean, 89.5%) and wetlands (84.8%) followed by forests (74.9%) and grasslands (51.8%). In the short term (< 1 week after 15N tracer application), total ecosystem 15N recovery was negatively correlated with fine-root and soil 15N natural abundance, and organic soil C and N concentration but was positively correlated with mean annual temperature and mineral soil C:N. In the longer term (3-18 months after 15N tracer application), total ecosystem 15N retention was negatively correlated with foliar natural-abundance 15N but was positively correlated with mineral soil C and N concentration and C:N, showing that plant and soil natural-abundance 15N and soil C:N are good indicators of total ecosystem N retention. Foliar N concentration was not significantly related to ecosystem 15N tracer recovery, suggesting that plant N status is not a good predictor of total ecosystem N retention. Because the largest ecosystem sinks for 15N tracer were below ground in forests, shrublands, and grasslands, we conclude that growth enhancement and potential for increased C storage in aboveground biomass from atmospheric N deposition is likely to be modest in these ecosystems. Total ecosystem 15N recovery decreased with N fertilization, with an apparent threshold fertilization rate of 46 kg N x ha(-1) x yr(-1) above which most ecosystems showed net losses of applied 15N tracer in response to N fertilizer addition.

Potential role of Thermus thermophilus and T. oshimai in high rates of nitrous oxide (N2O) production in ∼80 °C hot springs in the US Great Basin.

Ambient nitrous oxide (N(2)O) emissions from Great Boiling Spring (GBS) in the US Great Basin depended on temperature, with the highest flux, 67.8 ± 2.6 µmol N(2)O-N m(-2) day(-1) , occurring in the large source pool at 82 °C. This rate of N(2)O production contrasted with negligible production from nearby soils and was similar to rates from soils and sediments impacted with agricultural fertilizers. To investigate the source of N(2)O, a variety of approaches were used to enrich and isolate heterotrophic micro-organisms, and isolates were screened for nitrate reduction ability. Nitrate-respiring isolates were identified by 16S rRNA gene sequencing as Thermus thermophilus (31 isolates) and T. oshimai (three isolates). All isolates reduced nitrate to N(2)O but not to dinitrogen and were unable to grow with N(2)O as a terminal electron acceptor. Representative T. thermophilus and T. oshimai strains contained genes with 96-98% and 93% DNA identity, respectively, to the nitrate reductase catalytic subunit gene (narG) of T. thermophilus HB8. These data implicate T. thermophilus and T. oshimai in high flux of N(2)O in GBS and raise questions about the genetic basis of the incomplete denitrification pathway in these organisms and on the fate of biogenic N(2)O in geothermal environments.

Carbon and water fluxes from ponderosa pine forests disturbed by wildfire and thinning.

Disturbances alter ecosystem carbon dynamics, often by reducing carbon uptake and stocks. We compared the impact of two types of disturbances that represent the most likely future conditions of currently dense ponderosa pine forests of the southwestern United States: (1) high-intensity fire and (2) thinning, designed to reduce fire intensity. High-severity fire had a larger impact on ecosystem carbon uptake and storage than thinning. Total ecosystem carbon was 42% lower at the intensely burned site, 10 years after burning, than at the undisturbed site. Eddy covariance measurements over two years showed that the burned site was a net annual source of carbon to the atmosphere whereas the undisturbed site was a sink. Net primary production (NPP), evapotranspiration (ET), and water use efficiency were lower at the burned site than at the undisturbed site. In contrast, thinning decreased total ecosystem carbon by 18%, and changed the site from a carbon sink to a source in the first posttreatment year. Thinning also decreased ET, reduced the limitation of drought on carbon uptake during summer, and did not change water use efficiency. Both disturbances reduced ecosystem carbon uptake by decreasing gross primary production (55% by burning, 30% by thinning) more than total ecosystem respiration (TER; 33-47% by burning, 18% by thinning), and increased the contribution of soil carbon dioxide efflux to TER. The relationship between TER and temperature was not affected by either disturbance. Efforts to accurately estimate regional carbon budgets should consider impacts on carbon dynamics of both large disturbances, such as high-intensity fire, and the partial disturbance of thinning that is often used to prevent intense burning. Our results show that thinned forests of ponderosa pine in the southwestern United States are a desirable alternative to intensively burned forests to maintain carbon stocks and primary production.

Nitrogen stable isotope composition of leaves and roots of plants growing in a forest and a meadow.

In controlled N-nutrition experiments, differences in delta15N composition of leaves and roots are regularly found. In this paper we report results from a survey of nitrogen stable isotope signatures of leaves and roots of 16 plant species growing under natural conditions in a meadow and a forest understorey, which differed in nitrate and ammonium availability. Significant differences between leaf and root were observed. The range of delta15N [leaf-root] values was -0.97 to +0.86 per thousand, small compared to published values from controlled N-nutrition experiment, but almost as large as the range of leaf delta15N values (-1.04 to +1.08 per thousand). Forbs showed the largest differences between leaves and roots and showed a significant difference with respect to habitat. Grasses and legumes did not show significant differences in delta15N [leaf-root] between the two habitats. Care must be taken when using leaf delta15N values as representative for whole-plant 15N composition in these two habitats.

Tree species of the Central Amazon and soil moisture alter stable isotope composition of nitrogen and oxygen in nitrous oxide evolved from soil.

The use of stable isotopes of N and O in N2O has been proposed as a way to better constrain the global budget of atmospheric N2O and to better understand the relative contributions of the main microbial processes (nitrification and denitrification) responsible for N2O formation in soil. This study compared the isotopic composition of N2O emitted from soils under different tree species in the Brazilian Amazon. We also compared the effect of tree species with that of soil moisture, as we expected the latter to be the main factor regulating the proportion of nitrifier- and denitrifier-derived N2O and, consequently, isotopic signatures of N2O. Tree species significantly affected delta15N in nitrous oxide. However, there was no evidence that the observed variation in delta15N in N2O was determined by varying proportions of nitrifier- vs. denitrifier-derived N2O. We submit that the large variation in delta15N-N2O is the result of competition between denitrifying and immobilizing microorganisms for NO3(-). In addition to altering delta15N-N2O, tree species affected net rates of N2O emission from soil in laboratory incubations. These results suggest that tree species contribute to the large isotopic variation in N2O observed in a range tropical forest soils. We found that soil water affects both 15N and 18O in N2O, with wetter soils leading to more depleted N2O in both 15N and 18O. This is likely caused by a shift in biological processes for 15N and possible direct exchange of 18O between H2O and N2O.

Extensive belowground carbon storage supports roots and mycorrhizae in regenerating scrub oaks.

Portions of a regenerating scrub oak ecosystem were enclosed in open-top chambers and exposed to elevated CO2. The distinct 13C signal of the supplemental CO2 was used to trace the rate of C integration into various ecosystem components. Oak foliage, stems, roots and ectomycorrhizae were sampled over 3 years and were analyzed for 13C composition. The aboveground tissue 13C equilibrated to the novel 13C signal in the first season, while the belowground components displayed extremely slow integration of the new C. Roots taken from ingrowth cores showed that 33% of the C in newly formed roots originated from a source other than recent photosynthesis inside the chamber. In this highly fire-prone system, the oaks re-establish primarily by resprouting from large rhizomes. Remobilization from belowground C stores may support fine roots and mycorrhizae for several years into stand re-establishment and, therefore, may explain why belowground tissues contain less of the new photosynthate than expected. Though it has been shown that long-term cycles of C storage are theoretically advantageous for plants in systems with frequent and severe disturbances, such patterns have not been previously examined in wild systems.

Effects of elevated carbon dioxide on soils in a Florida scrub oak ecosystem.

The results of a 3-yr study on the effects of elevated CO2 on soil N and P, soil pCO2, and calculated CO2 efflux in a fire-regenerated Florida scrub oak ecosystem are summarized. We hypothesized that elevated CO2 would cause (i) increases in soil pCO2 and soil respiration and (ii) reduced levels of soil-available N and P. The effects of elevated CO2 on soil N availability differed according to the method used. Results of resin lysimeter collections and anion exchange membrane tests in the field showed reduced NO3- in soils in Years 1 and 3. On the other hand, re-analysis of homogenized, buried soil bags after 1 yr suggested a relative increase in N availability (lower C to N ratio) under elevated CO2. In the case of P, the buried bags and membranes suggested a negative effect of CO2 on P during the first year; this faded over time, however, as P availability declined overall, probably in response to P uptake. Elevated CO2 had no effect on soil pCO2 or calculated soil respiration at any time, further suggesting that plant rather than microbial uptake was the primary factor responsible for the observed changes in N and P availability with elevated CO2.

Soil microbiota in two annual grasslands: responses to elevated atmospheric CO2.

We measured soil bacteria, fungi, protozoa, nematodes, and biological activity in serpentine and sandstone annual grasslands after 4 years of exposure to elevated atmospheric CO2. Measurements were made during the early part of the season, when plants were in vegetative growth, and later in the season, when plants were approaching their maximum biomass. In general, under ambient CO2, bacterial biomass, total protozoan numbers, and numbers of bactivorous nematodes were similar in the two grasslands. Active and total fungal biomasses were higher on the more productive sandstone grassland compared to the serpentine. However, serpentine soils contained nearly twice the number of fungivorous nematodes compared to the sandstone, perhaps explaining the lower standing crop of fungal biomass in the serpentine and suggesting higher rates of energy flow through the fungal-based soil food web. Furthermore, root biomass in the surface soils of these grasslands is comparable, but the serpentine contains 6 times more phytophagous nematodes compared to the sandstone, indicating greater below-ground grazing pressure on plants in stressful serpentine soils. Elevated CO2 increased the biomass of active fungi and the numbers of flagellates in both grasslands during the early part of the season and increased the number of phytophagous nematodes in the serpentine. Elevated CO2 had no effect on the total numbers of bactivorous or fungivorous nematodes, but decreased the diversity of the nematode assemblage in the serpentine at both sampling dates. Excepting this reduction in nematode diversity, the effects of elevated CO2 disappeared later in the season as plants approached their maximum biomass. Elevated CO2 had no effect on total and active bacterial biomass, total fungal biomass, or the total numbers of amoebae and ciliates in either grassland during either sampling period. However, soil metabolic activity was higher in the sandstone grassland in the early season under elevated CO2, and elevated CO2 altered the patterns of use of individual carbon substrates in both grasslands at this time. Rates of substrate use were also significantly higher in the sandstone, indicating increased bacterial metabolic activity. These changes in soil microbiota are likely due to an increase in the flux of carbon from roots to soil in elevated CO2, as has been previously reported for these grasslands. Results presented here suggest that some of the carbon distributed below ground in response to elevated CO2 affects the soil microbial food web, but that these effects may be more pronounced during the early part of the growing season.

Decreased leaf-miner abundance in elevated CO2: reduced leaf quality and increased parasitoid attack.

Most studies on the effects of elevated CO2 have focused on the effects on plant growth and ecosystem processes. Fewer studies have examined the effects of elevated CO2 on herbivory, and of these, most have examined feeding rates in laboratory conditions. Our study takes advantage of an open-top CO2 fertilization study in a Florida scrub-oak community to examine the effects of elevated CO2 on herbivore densities, herbivore feeding rates, and levels of attack of herbivores by natural enemies. Higher atmospheric CO2 concentration reduced plant foliar nitrogen concentrations, decreased abundance of leaf-mining insect herbivores, increased per capita leaf consumption by leafminers, and increased leafminer mortality. As suggested by other authors, reduced foliar quality contributed to the increase in herbivore mortality, but only partly. The major factor increasing mortality was higher attack rate by parasitoids. Thus increasing CO2 concentrations may reduce the survivorship of insect herbivores directly, by reducing plant quality, but also indirectly, by changing herbivore feeding and eliciting greater top-down pressure from natural enemies.

Stimulation of grassland nitrogen cycling under carbon dioxide enrichment.

Nitrogen (N) limits plant growth in many terrestrial ecosystems, potentially constraining terrestrial ecosystem response to elevated CO2. In this study, elevated CO2 stimulated gross N mineralization and plant N uptake in two annual grasslands. In contrast to other studies that have invoked increased C input to soil as the mechanism altering soil N cycling in response to elevated CO2, increased soil moisture, due to decreased plant transpiration in elevated CO2, best explains the changes we observed. This study suggests that atmospheric CO2 concentration may influence ecosystem biogeochemistry through plant control of soil moisture.