Summary
It is increasingly acknowledged that plant–soil feedbacks may play an important role in driving the composition of plant communities and functioning of terrestrial ecosystems. However, the mechanistic understanding of plant–soil feedbacks, as well as their roles in natural ecosystems in proportion to other possible drivers, is still in its infancy. Such knowledge will enhance our capacity to determine the contribution of plant–soil feedback to community and ecosystem responses under global environmental change.
Here, we review how plant–soil feedbacks may develop under extreme drought and precipitation events, CO2 and nitrogen enrichment, temperature increase, land use change and plant species loss vs. gain. We present a framework for opening the ‘black box of soil’ considering the responses of the various biotic components (enemies, symbionts and decomposers) of plant–soil feedback to the global environmental changes, and we discuss how to integrate these components to understand and predict the net effects of plant–soil feedbacks under the various scenarios of change.
To gain an understanding of how plant–soil feedback plays out in realistic settings, we also use the framework to discuss its interaction with other drivers of plant community composition, including competition, facilitation, herbivory, and soil physical and chemical properties.
We conclude that understanding the role that plant–soil feedback plays in shaping the responses of plant community composition and ecosystem processes to global environmental changes requires unravelling the individual contributions of enemies, symbionts and decomposers. These biotic factors may show different response rates and strengths, thereby resulting in different net magnitudes and directions of plant–soil feedbacks under various scenarios of global change. We also need tests of plant–soil feedback under more realistic conditions to determine its contribution to changes in patterns and processes in the field, both at ecologically and evolutionary relevant time-scales.

https://besjournals.onlinelibrary.wiley.com/doi/pdf/10.1111/1365-2435.12657

Where, when and how plant-soil feedback matters in a changing world

Environmental stress is increasing worldwide, yet we lack a clear picture of how stress disrupts the stability of microbial communities and the ecosystem services they provide. Here, we present the first evidence that naturally-occurring microbiomes display network properties characteristic of unstable communities when under persistent stress. By assessing changes in diversity and structure of soil microbiomes along 40 replicate stress gradients (elevation/water availability gradients) in the Florida scrub ecosystem, we show that: (1) prokaryotic and fungal diversity decline in high stress, and (2) two network properties of stable microbial communities-modularity and negative:positive cohesion-have a clear negative relationship with environmental stress, explaining 51-78% of their variation. Interestingly, pathogenic taxa/functional guilds decreased in relative abundance along the stress gradient, while oligotrophs and mutualists increased, suggesting that the shift in negative:positive cohesion could result from decreasing negative:positive biotic interactions consistent with the predictions of the Stress Gradient Hypothesis. Given the crucial role microbiomes play in ecosystem functions, our results suggest that, by limiting the compartmentalization of microbial associations and creating communities dominated by positive associations, increasing stress in the Anthropocene could destabilize microbiomes and undermine their ecosystem services.

Environmental stress destabilizes microbial networks.

Soil organic matter (SOM) represents a major reservoir of stored carbon (C). However, uncertainties regarding the composition and origin of stabilized SOM hinder the implementation of sustainable management strategies. Here, we synthesize data on the contribution of plant- and microbial-derived compounds to stabilized SOM, i.e., aggregates and mineral-associated organic matter (MAOM), and review the role of environmental factors influencing this contribution. Extrapolating amino sugar concentrations in soil based on molecular stoichiometry, we find that microbial necromass accounts for ~50% (agroecosystems) or less (forest ecosystems) of the C stabilized within aggregates and MAOM across studies. This implies that plant biomolecules, including lipids, lignin, and sugars, might account for a substantial portion (≥50%) of the organic matter protected by minerals and aggregates. Indeed, plant-specific sugars and lipids can each account for as much as 10% of organic C within mineral soil fractions, and most reported quantities of plant-specific lipids and lignin in mineral soil fractions are likely underestimates due to irreversible sorption to minerals. A relatively balanced contribution of plant and microbial biomolecules to stabilized SOM in aggregates and MAOM is inconsistent with recent suggestions that stable SOM is comprised mostly of microbial compounds. Land use and soil type appear to profoundly affect the contribution of plant and microbial compounds to stabilized SOM. Consistent with studies of bulk soils, favorable conditions for microbial proliferation in grasslands or fertile Chernozems or Luvisols appear to increase the contribution of microbial compounds, while less favorable conditions for microbial proliferation in forest soils or Podzols/Alisols appear to favor the abundance of plant compounds in stabilized SOM. Combined with a tight link between substrate quality and the abundance of microbial compounds in stabilized SOM, and a potentially inverse relationship between substrate quality and the abundance of plant compounds, these results provide evidence that plant biomolecules might be preferentially stabilized by organo-mineral interactions in some ecosystems. Various areas warrant further research. For example, difficulties in distinguishing direct and indirect effects of temperature and precipitation on the composition of stabilized SOM may be overcome by long-term observational studies that include climate manipulations. Knowledge gaps in the contribution of plant and microbial compounds to stabilized SOM in soil layers below 30 cm depth may simply be closed by extending the sampling depth. Moreover, a refined focus on soil fauna, with potentially strong effects on microbial and plant compounds in stabilized SOM, will provide new insights into SOM dynamics. Future studies should quantify both microbial and plant biomolecules in mineral soil fractions to allow direct comparisons and overcome limitations in existing data. For example, because biomarker-based estimates of microbial-derived C can only indirectly estimate the maximum amount of plant-derived C, exhaustive studies of plant biomarker concentrations could be conducted, including estimates of plant-specific lipids, sugars, and lignin (and biomarkers released following mineral dissolution). Generally, more integrative studies, e.g., combining molecular and isotopic tracers of organic matter inputs with targeted sampling of mineral fractions, are required to improve knowledge of the formation and persistence of stabilized SOM.

Plant- or microbial-derived? A review on the molecular composition of stabilized soil organic matter

In the Paris Agreement on Climate Change, the United Nations is pursuing efforts to limit global warming to 1.5°C, whereas earlier aspirations focused on a 2°C limit. With current pledges, corresponding to ~3.2°C warming, climatically determined geographic range losses of >50% are projected in ~49% of insects, 44% of plants, and 26% of vertebrates. At 2°C, this falls to 18% of insects, 16% of plants, and 8% of vertebrates and at 1.5°C, to 6% of insects, 8% of plants, and 4% of vertebrates. When warming is limited to 1.5°C as compared with 2°C, numbers of species projected to lose >50% of their range are reduced by ~66% in insects and by ~50% in plants and vertebrates.

/pdf/the-projected-effect-on-insects-vertebrates-and-plants-of-1wmz7ptsrv.pdf

The projected effect on insects, vertebrates, and plants of limiting global warming to 1.5°C rather than 2°C.

Trophic regulations of the soil microbiome

Global change is altering species distributions and thus interactions among organisms. Organisms live in concert with thousands of other species, some beneficial, some pathogenic, some which have little to no effect in complex communities. Since natural communities are composed of organisms with very different life history traits and dispersal ability it is unlikely they will all respond to climatic change in a similar way. Disjuncts in plant-pollinator and plant-herbivore interactions under global change have been relatively well described, but plant-soil microorganism and soil microbe-microbe relationships have received less attention. Since soil microorganisms regulate nutrient transformations, provide plants with nutrients, allow co-existence among neighbors, and control plant populations, changes in soil microorganism-plant interactions could have significant ramifications for plant community composition and ecosystem function. In this paper we explore how climatic change affects soil microbes and soil microbe-plant interactions directly and indirectly, discuss what we see as emerging and exciting questions and areas for future research, and discuss what ramifications changes in these interactions may have on the composition and function of ecosystems.

/pdf/direct-and-indirect-effects-of-climate-change-on-soil-pil6iee174.pdf

Direct and indirect effects of climate change on soil microbial and soil microbial‐plant interactions: What lies ahead?

Summary
Plant roots, their associated microbial community and free-living soil microbes interact to regulate the movement of carbon from the soil to the atmosphere, one of the most important and least understood fluxes of terrestrial carbon. Our inadequate understanding of how plant–microbial interactions alter soil carbon decomposition may lead to poor model predictions of terrestrial carbon feedbacks to the atmosphere.
Roots, mycorrhizal fungi and free-living soil microbes can alter soil carbon decomposition through exudation of carbon into soil. Exudates of simple carbon compounds can increase microbial activity because microbes are typically carbon limited. When both roots and mycorrhizal fungi are present in the soil, they may additively increase carbon decomposition. However, when mycorrhizas are isolated from roots, they may limit soil carbon decomposition by competing with free-living decomposers for resources.
We manipulated the access of roots and mycorrhizal fungi to soil in situ in a temperate mixed deciduous forest. We added 13C-labelled substrate to trace metabolized carbon in respiration and measured carbon-degrading microbial extracellular enzyme activity and soil carbon pools. We used our data in a mechanistic soil carbon decomposition model to simulate and compare the effects of root and mycorrhizal fungal presence on soil carbon dynamics over longer time periods.
Contrary to what we predicted, root and mycorrhizal biomass did not interact to additively increase microbial activity and soil carbon degradation. The metabolism of 13C-labelled starch was highest when root biomass was high and mycorrhizal biomass was low. These results suggest that mycorrhizas may negatively interact with the free-living microbial community to influence soil carbon dynamics, a hypothesis supported by our enzyme results. Our steady-state model simulations suggested that root presence increased mineral-associated and particulate organic carbon pools, while mycorrhizal fungal presence had a greater influence on particulate than mineral-associated organic carbon pools.
Synthesis. Our results suggest that the activity of enzymes involved in organic matter decomposition was contingent upon root–mycorrhizal–microbial interactions. Using our experimental data in a decomposition simulation model, we show that root–mycorrhizal–microbial interactions may have longer-term legacy effects on soil carbon sequestration. Overall, our study suggests that roots stimulate microbial activity in the short term, but contribute to soil carbon storage over longer periods of time.

https://besjournals.onlinelibrary.wiley.com/doi/epdf/10.1111/1365-2745.12484

Interactions among roots, mycorrhizas and free-living microbial communities differentially impact soil carbon processes.

Climate change affects communities both directly and indirectly via changes in interspecific interactions. One such interaction that may be altered under climate change is the ant-plant seed dispersal mutualism common in deciduous forests of eastern North America. As climatic warming alters the abundance and activity levels of ants, the potential exists for shifts in rates of ant-mediated seed dispersal. We used an experimental temperature manipulation at two sites in the eastern US (Harvard Forest in Massachusetts and Duke Forest in North Carolina) to examine the potential impacts of climatic warming on overall rates of seed dispersal (using Asarum canadense seeds) as well as species-specific rates of seed dispersal at the Duke Forest site. We also examined the relationship between ant critical thermal maxima (CTmax) and the mean seed removal temperature for each ant species. We found that seed removal rates did not change as a result of experimental warming at either study site, nor were there any changes in species-specific rates of seed dispersal. There was, however, a positive relationship between CTmax and mean seed removal temperature, whereby species with higher CTmax removed more seeds at hotter temperatures. The temperature at which seeds were removed was influenced by experimental warming as well as diurnal and day-to-day fluctuations in temperature. Taken together, our results suggest that while temperature may play a role in regulating seed removal by ants, ant plant seed-dispersal mutualisms may be more robust to climate change than currently assumed.

Ant-mediated seed dispersal in a warmed world.

Plant roots stimulate the decomposition of complex, but not simple, soil carbon

To maximize limited conservation funds and prioritize management projects that are likely to succeed, accurate assessment of invasive nonnative species impacts is essential. A common challenge to prioritization is a limited knowledge of the difference between the impacts of a single nonnative species compared to the impacts of nonnative species when they co-occur, and in particular predicting when impacts of co-occurring nonnative species will be non-additive. Understanding non-additivity is important for management decisions because the management of only one co-occurring invader will not necessarily lead to a predictable reduction in the impact or growth of the other nonnative plant. Nonnative plants are frequently associated with changes in soil biotic and abiotic characteristics, which lead to plant-soil interactions that influence the performance of other species grown in those soils. Whether co-occurring nonnative plants alter soil properties additively or non-additively relative to their effects on soils when they grow in monoculture is rarely addressed. We use a greenhouse plant-soil feedback experiment to test for non-additive soil impacts of two common invasive nonnative woody shrubs, Lonicera maackii and Ligustrum sinense, in deciduous forests of the southeastern United States. We measured the performance of each nonnative shrub, a native herbaceous community, and a nonnative woody vine in soils conditioned by each shrub singly or together in polyculture. Soils conditioned by both nonnative shrubs had non-additive impacts on native and nonnative performance. Root mass of the native herbaceous community was 1.5 times lower and the root mass of the nonnative L. sinense was 1.8 times higher in soils conditioned by both L. maackii and L. sinense than expected based upon growth in soils conditioned by either shrub singly. This result indicates that when these two nonnative shrubs co-occur, their influence on soils disproportionally favors persistence of the nonnative L. sinense relative to this native herbaceous community, and could provide an explanation of why native species abundance is frequently depressed in these communities. Additionally, the difference between native and nonnative performance demonstrates that invasive impact studies focusing on the impact only of single species can be insufficient for determining the impact of co-occurring invasive plant species.

Courtney M. Patterson

Papers

Direct and indirect effects of climate change on soil microbial and soil microbial‐plant interactions: What lies ahead?

Interactions among roots, mycorrhizas and free-living microbial communities differentially impact soil carbon processes.

Ant-mediated seed dispersal in a warmed world.

Plant roots stimulate the decomposition of complex, but not simple, soil carbon

Co‐occurring nonnative woody shrubs have additive and non‐additive soil legacies