CORBIS, MICHAEL POLE
Human beings have inexorably altered the world’s ecosystems. We’ve plowed and seeded more than 40 percent of the Earth’s land surfaces, introduced alien species into new territories, poured carbon dioxide into the atmosphere, disrupted natural climate cycles, and polluted aquatic ecosystems with excessive nitrogen and other contaminants.
These far-reaching changes have spurred scores of researchers to examine the impacts of human activities on biodiversity and ecosystem functioning, and to devise management strategies that might lessen the damage. Scientists have scoured ecosystems from the ocean’s depths to the highest mountain peaks searching for signals of global change. But only recently has this attention extended under the Earth’s surface to the soil, and the linkages between plants and belowground microbial and animal communities. This realm of research is of paramount importance because the impact of human-induced disturbances on the functioning of terrestrial ecosystems is often indirect: they tend to operate via changes aboveground that cascade belowground to the hugely complex and diverse, soil-bound biological community, driving biogeochemical processes and feeding back to the whole Earth-system.
And these studies may be overturning a commonly held view of how plants help mitigate the impacts of global warming. Indeed, it is widely thought that vegetation, especially trees, will respond to increasing atmospheric CO2 concentrations by growing more vigorously, and thus help to moderate climate change by locking up more carbon in their leaves, branches, and trunks. But research into the intricate dynamics occurring just below the soil surface, where carbon, nitrogen, and other elements flow through plant roots into the soil and react with the microbial and animal communities living there—including bacteria, fungi and a host of fauna—is complicating this simplistic view. In fact, some work suggests that as plant growth increases because of elevated CO2, more carbon not only flows into the plants themselves, but also exits their roots to impact the growth and activity of soil microbes. This causes a net increase in CO2 and other greenhouse gases escaping from the soil and entering the atmosphere, thus adding to anthropogenic levels.
These insights indicate that a combined plant-microbial-soil approach can lead to a more holistic understanding of the consequences of global change—including climate change—for the health and functioning of both terrestrial ecosystems and the whole Earth-system. Most importantly, the role that plant-microbial-soil interactions, and specifically carbon transfer from roots to soil, play in governing climate change and its impact on ecosystem carbon cycling is coming to light.
Getting Down and Dirty
Soils are the Earth’s third largest carbon storage depot after oceans and fossil fuels and together with vegetation contain about 2.7 times more carbon than the atmosphere. As a result, there is much concern that climate change will enhance the decomposition of this soil-bound carbon, potentially shifting soils from being sinks to sources of atmospheric CO2, thereby accelerating climate change: the so called carbon-cycle feedback. There is also a vigorous debate about the feasibility of slowing climate change by increasing the capacity of soils to sequester carbon from the atmosphere. Recent research is revealing that both the loss and gain of carbon in soil depend heavily on the pattern of interaction between plants, microbes, and the soil itself.
Climate change impacts soil carbon in a variety of ways, both direct and indirect.[1. R.D. Bardgett et al., “Microbial contributions to climate change through carbon-cycle feedbacks,” ISME J, 2:805-14, 2008.] Even a subtle uptick in global air temperatures (of approximately 1°C) can directly stimulate microbial activity, causing an increase in ecosystem respiration rates in the subarctic peatlands which cover vast tracts of northern hemisphere and harbor a large portion of the organic carbon found in the world’s soil.[2. E. Dorrepaal et al., “Carbon respiration from subsurface peat accelerated by climate warming in the subarctic,” Nature, 460:616-19, 2009.] Researchers monitoring an Alaskan tundra landscape also showed that permafrost thaw occurring over a span of decades has led to significant losses of soil carbon through soil respiration, despite increased plant growth and consequent ecosystem carbon input to soil, in the form of leaf litter and other plant sources.[3. E.A.G. Schuur et al., “The effect of permafrost thaw on old carbon release and net carbon exchange from tundra,” Nature, 459:556-59, 2009.] Given that tundra soils are among the world’s largest carbon stores, these studies indicate a potentially large and long-lasting positive feedback of carbon to the global climate system.
There remains much uncertainty, however, about how soil organisms directly respond to warming. For instance, it is unclear whether short-term increases in microbial activity and carbon cycling in response to warming will be sustained when fast-cycling soil carbon pools, such as carbohydrates and amino acids, become depleted and soil communities become acclimated to living in a warmer world.[4. M.A. Bradford et al., “Thermal adaptation of soil microbial respiration to elevated temperature,” Ecol Lett, 11:1316-27, 2008.]
While more work remains to be done to fully elucidate the direct effects of climate change on soil microbes and carbon cycling, understanding strong indirect effects—for example, responses mediated via plants—is perhaps even more important. Two types of mechanisms drive these processes: first, rising atmospheric CO2 indirectly impacts soil microbes by way of increased plant photosynthesis and transfer of photosynthetic carbon to soil as root exudates; and, second, long-term, climate change-induced alterations in the composition and diversity of vegetation alter the amount and quality of organic matter entering soil, affecting the activity and structure of belowground communities.
It is becoming clear that both of these indirect mechanisms—short-term, individual plant-level and long-term, community-level inputs—have significant consequences for the carbon budget of terrestrial ecosystems under conditions of climate change. With regard to short-term effects, University of Illinois graduate student John Drake and colleagues constructed a belowground carbon budget based on 12 years of measurements from the Duke Forest free-air CO2 enrichment (FACE) experiment in North Carolina, and showed that elevated CO2 concentrations caused a carbon cascade through the root-microbial-soil system in a low-fertility pine forest, altering the carbon budget of this ecosystem. Specifically, the researchers found that elevated atmospheric CO2 increased the flux of carbon to roots, which in turn stimulated microbial activity and the breakdown of organic matter in the soil. Because this process also stimulated the release and turnover of nitrogen and its uptake by the trees, it set in motion a positive feedback loop that sustained enhanced rates of tree growth, which locked up even more carbon in tree biomass, but not in soil.[5. J. E. Drake et al., “Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2,” Ecol Lett, 14: 349-57, 2011.]
In a related study at Duke Forest, Indiana University’s Richard Phillips and collaborators, investigated the mechanisms behind this carbon cascade: over a period of 3 years, elevated CO2 concentrations in the air increased the rate at which tree roots exuded carbon by 55 percent, leading to a 50 percent annual increase in soluble organic inputs to soil.[6. R.P. Philips et al., “Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation,” Ecol Lett, 14:187-94, 2011.] Upping the amount of carbon oozing from plant roots drove belowground microbes to release more extracellular enzymes involved in breakdown of organic nitrogen and accelerated the turnover rate of organic nitrogen in the soil. In sum, these findings point to the importance of such indirect, plant-driven mechanisms for understanding how climate change impacts the functioning of terrestrial ecosystems.
Scientists have scoured ecosystems from the ocean’s depths to the highest mountain peaks searching for signals of global change. But only recently has this attention extended under the Earth’s surface to the soil.
Despite these reports, there is still uncertainly about how soil microbes respond to more carbon being pumped into soil in a high CO2 world. For example, while the above studies show that upping the amount of carbon entering the soil stimulated soil microbes and nitrogen cycling, other studies show a different pattern. That is, enhanced root exudation under elevated CO2 can stimulate the locking up of nitrogen by microbes—termed nitrogen immobilization—which in turn limits nitrogen availability to plants, plant growth, and, ultimately, carbon transfer to soil. The reason for this discrepancy is unclear, but it is most likely due to the quality of the exudates and of other plant-derived organic matter, such as plant litter, entering soil. When the material is rich in nitrogen and hence has a low carbon-to-nitrogen ratio, microbes will use the carbon for growth and liberate the excess nitrogen that they don’t need into the soil, thereby increasing nitrogen availability to plants. Conversely, when those substrates are low in nitrogen and have a high carbon-to-nitrogen ratio, the microbes become nitrogen starved and soak up any nitrogen that is available, therefore reducing its availability to plants. This often occurs because elevated CO2 reduces the nitrogen concentrations in plant tissues, unless there is a continuing supply of nitrogen to the plants, for example through fertilizers.
More carbon coming from roots can also result in the mineralization of both recent and old soil organic carbon, making it metabolically available and leading to net carbon loss from soil through respiration.[7. J. Heath et al., “Rising atmospheric CO2 reduces soil carbon sequestration of root-derived soil carbon,” Science, 309:1711-13, 2005.] This mineralization can also increase the growth of mycorrhizal fungi, which can alter the release of carbon to the soil microbial community and enhance the stabilization of organic carbon by causing soil particles to aggregate.[8. G.W.T Wilson et al., “Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments,” Ecol Lett, 12:452-61, 2009.] These studies show that forests respond to elevated CO2 in complex ways that tightly link plant-microbial-soil feedbacks fueled by inputs of root-derived carbon to soil. Moreover, they bolster the growing view that the transfer of recently fixed carbon from roots to the belowground subsystem serves as a major driver of soil food webs, and this has significant consequences for the functioning of terrestrial ecosystems adapting to climate change.
Evidence is also emerging that climate change can cause both local and regional shifts in the composition of vegetation by altering precipitation patterns and temperature regimes and by further elevating atmospheric CO2 concentrations. It’s becoming clear that such long-term shifts in composition of the plant community can affect the transfer of recent photosynthetic carbon belowground and thus affect ecosystem carbon dynamics. For example, Sue Ward and colleagues at the Lancaster Environment Centre, UK, used in situ stable carbon-isotope labeling approaches to show that removing key plant species from a dwarf-shrub heath community strongly affected belowground transfer and metabolism of recently added photosynthetic carbon.[9. S.E. Ward et al., “Plant functional group identity influences short-term peatland ecosystem carbon flux: evidence from a plant removal experiment,” Funct Ecol, 23:454-62, 2009.] In particular, the removal of dwarf shrubs greatly increased community-level photosynthesis rates, the transfer of this recently assimilated carbon to soil, and its use by soil microbes, thereby speeding up rates of carbon cycling. There is growing evidence from a variety of ecosystems that plant species and functional groups—different species, such as legumes, grasses, and herbs, with similar physiological characteristics—differentially influence the uptake and transfer of carbon to soil via their exudates, suggesting that global warming-induced changes in plant community structure have the potential to alter patterns of carbon exchange. In general, however, much remains unknown about how changing the composition of plant communities can affect carbon cycling, and an important challenge will be to better understand the role of plant-soil feedbacks in modifying ecosystem carbon dynamics, especially given the extent to which climate-mediated changes in vegetation are already occurring worldwide.
In all the work being done to illuminate and quantify the importance of belowground dynamics in driving the carbon cycle, the central message is similar: to better understand ecosystem functioning and its response to global change, we must consider feedbacks among plants, microbes, and soil processes. It’s clear that root carbon transfer and resulting carbon cascades through the plant-microbial-soil system play a primary role in driving carbon-cycle feedbacks and in regulating ecosystem responses to climate change.
Recent studies highlight the potential application of such understanding to land management challenges, such as enhancing soil carbon sequestration in grassland and degraded soils, which also hold potential benefits for food production and biodiversity conservation. Further study is also required to realize the potential for targeted crop-improvement strategies based on root traits that favor carbon sequestration in soil while also efficiently producing food. A new age of research and funding is needed to meet these scientific challenges and to integrate such understanding into future land-management and climate change mitigation strategies.
Richard D. Bardgett is a Professor of Ecology at Lancaster University’s Lancaster Environment Centre, in the UK. His research is focused on understanding the role that linkages between plant and soil communities play in the delivery of ecosystem services, especially sequestration in soils and nutrient cycling.
This article is adapted from a review in F1000 Biology Reports, DOI: 10.3410/B3-16 (open access at http://f1000.com/reports/b/3/16/). For citation purposes, please refer to that version.