Unearthing the Soil Microbiome, Climate Change, Carbon Storage Nexus

May 13, 2021

Soil is one of the most diverse microbial ecosystems in the world, replete with not just bacteria, but fungi, archaea, viruses and protists. These microbial communities are critical to plant health and their resistance to stressors, such as drought, heavy metal pollution and even parasitism. Soils—and their microbes—provide humans with up to 98.8% of the food we eat. However, the Food and Agriculture Organization (FAO) predicts that due to human activity and climate change, soil erosion could result in between 20-80% losses in agricultural yields, depending on the soil. Moreover, new topsoil (the uppermost organic-rich layer of soil, usually the top 5-10 inches) is generated at a sluggish rate of only 0.25-1.5mm per year. As such, soil is also one of Earth's precious non-renewable resources, and its microbial communities sustain that.

The soil and its microbiome are notoriously difficult to generalize because they are so dependent on biotic and abiotic factors, like moisture, pH, type of vegetation in the area, soil structure and aeration and competition or cooperation with other nearby microbes. Soil health therefore can vary by ecosystem and its local flora and fauna. However, the real business of soils generally occurs in the top layers where organic matter and mineral content are concentrated, and thus life is most amenable to plant roots and microorganisms. Dead vegetation, such as discarded leaves, feeds a carpet of organic decay that replenishes this layer and provides fuel and carbon for the ecosystem below. Good structure in these soil layers allows porous ‘micropockets' to form for water, oxygen and nutrients, making it easier for roots and microbes to weave through.

The Root Microbiome (The ‘Rhizobiome')

The largest and most ancient living thing known to man is, incidentally, a single fungus of the honey mushroom family that threads underneath the earthy humus of the mystical Blue Mountains in the Pacific Northwest. Estimated to be between 2,400-8,650 years old, Armillaria ostoyae spreads across more than 2,300 acres of land in what some would call a savory array. Its impressive breadth is a result of seemingly endless networks of hyphae, or microscopic branching filaments, that wend through the rich forest soil.

Although A. ostoyae parasitizes conifer trees (an unfortunate hustle), its way of life doesn't represent soil fungi overall. In fact, an astonishing 80-90% of land plants benefit from symbiosis with fungi, not to mention abundant partnerships with other kingdoms of microbes. Much of this mutualistic exchange is mediated through the plants' roots and the ecological zone surrounding them, dubbed the ‘rhizosphere.'

Plants themselves play no small role in shaping the soil microbiome, as they actively help shape the community structure by luring their most-wanted players. When plants photosynthesize sugars in their leaves, they share some of these sugars—up to 20% of their photosynthesis products—with the below-deck crew via their roots, in what are called ‘exudates' (i.e., secreted by the plant). As plants die off and contribute to leaf litter and organic matter in the topsoil, their unique characteristics also help shape the community of microbes and other creatures that break them down.

Fungal hyphae (small white strands) surround a root tip.
Fungal hyphae (small white strands) surround a root tip.
Source: Wellcome Collection

Early in a plant's life cycle, it exudes higher levels of sugar in an effort to recruit cooperative microbes. In response, bacteria and fungi that are able to detect these exudates travel in the direction of the roots and establish microscopic niches on, around, in between and, in some cases, inside of the roots. In exchange for sugars from the plant, microbes provide the plant with nutrients, water, protection from parasitic organisms and protection from drought. Some mycorrhizal fungi—'myco,' the Latin word for fungus and 'rhiza,' the Greek word for root—can even create a direct connection to the plant roots to facilitate ready nutrient sharing. The spindly fungal hyphae are only 4-6 ųm in diameter (~20x narrower than a human hair), and are able to network into numerous microscopic pockets of nutrients and water in the soil. This network of hyphae helps them scout water that they can then share with the plant and bacterial populations.

Symbiosis between a plant and its root microbiome.
The root microbiome inhabits a narrow zone around plant roots. Fungi and bacteria consume plant exudates, and in exchange they provide plants with nutrients and metabolites essential for growth and health.
Source: Montgomery and Biklé/The Hidden Half of Nature, 2016.

Some plants are said to have a stronger "rhizosphere effect," which is to say that they appear to more selectively recruit the microbes they desire to their root system, whereas others don't seem to recruit as vigorously. They do this by virtue of nuances in their root exudates that even differ by plant developmental stage and location on the root itself. The "rhizobiome," as the root microbiome has been called, moves in tandem with the exudates, differing by very miniscule changes in geography, including factors such as radial distance extending outward from the root or location on the root itself, in addition to other abiotic factors like soil moisture, soil structure and temperature. For these reasons, the rhizobiome can be quite difficult to study.

It's not just the plant that microbes communicate with, but each other. Interkingdom interactions between different members of the rhizobiome are thought to be key in how the whole system functions. For example, fungal mycelia (i.e., the entire network of its hyphae) not only deliver water to isolated bacteria, but promote horizontal gene transfer between bacteria, serve as tiny bacterial highways and attenuate dangerous dips in soil pH. Protists and nematodes feed on certain populations of bacteria and thus help shape the overall community by predation. Viruses can aid in the transfer of genes between microbial groups, such as antimicrobial resistance genes. On a macroscopic level, nematodes and arthropods that burrow through the soil help create needed structure for water, fungal hyphae and plant roots to intertwine.

Climate Change and Soil Carbon Fixation

In addition to being host to an incredibly important symbiotic exchange between plants and their microbes, soil is also a silo for the majority of carbon found in terrestrial ecosystems (nearly 80%). About half of this terra-carbon is tucked away in the perpetually frozen soils of the arctic, which are heating up at nearly twice the rate as other global regions in response to climate change. The soil microbiome and that community's interaction with plants are a central component of the carbon storage process, and unique ecosystems accomplish this in specific ways. For the arctic, higher temperatures mean more metabolically active microbes, which decompose organic material and release the large reservoir of carbon from ancient deceased plants and animals into the atmosphere. Forests and grasslands together cover approximately 56% of the earth's land area and account for large swaths of carbon soil fixation as well, with grasslands alone making up about 20% of the Earth's soil carbon store.

Climate models have come to differing conclusions about how a warming future could impact soil sequestration or release of carbon, and it likely differs both by regional factors and temporal ones. Some models suggest that higher atmospheric carbon could lead to an initial burst in plant growth and carbon sequestration, but a long-term depletion of soil microbe diversity and activity, and thus a decline in plant viability and release of carbon back into the atmosphere. However, these models have an intensely intricate number of variables to account for, with little ability to generalize globally.

There are some trends that may indicate how microbes will respond to ongoing climate change. A greater diversity of plants in a region corresponds to more active soil microbes and greater carbon storage; however climate change is slowly diminishing the diversity of many plant ecosystems. Carbon is also more readily stored in soils with sufficient moisture, or else by microbes that can withstand drought stress. However, climate change is ushering forth widespread desertification and expansion of arid lands, suggesting that fewer soils will be available for adequate carbon fixation unless we can develop and support microbial solutions.

According to field studies, elevated carbon in the atmosphere is able to measurably shift the soil community structure of multiple microbial kingdoms, including fungi, archaea and bacteria. Functional studies indicate in these populations that genes involved in different aspects of microbial nitrogen cycling were enriched in surviving communities, which could imply that rhizobiome shifts favor those microbes that can keep up with emerging metabolic demands. Atmospheric warming, independent of atmospheric carbon, has a documented effect on the metabolic activity and stress biomarkers of the microbial community as well. In general, fungi are less heat-resistant than bacteria, and warming can increase the bacteria:fungal ratio. Recall that fungi are important shuttles of nutrients and water due to their narrow branching mycelia, thus their loss can have detrimental impacts on other interkingdom communities and on the plants they partner with.

Although models differ, some climate change predictions for the soil microbiome include an initial increase in plant growth, followed by a depletion of microbial and plant diversity and enhanced relea
Although models differ, some climate change predictions for the soil microbiome include an initial increase in plant growth, followed by a depletion of microbial and plant diversity and enhanced release of carbon dioxide into the atmosphere.
Source: annualreviews.org.

Climate change is also affiliated with more unpredictable and extreme weather events, such as drought, flooding and irregular seasons. These fluctuations in soil moisture, a drying and re-wetting cycle, can have deleterious effects on its microbiome and carbon sequestration. Studies indicate that while soil communities can demonstrate resilience to an initial dry/wetting cycle, repeated insults weaken the community over time. On the brighter side, bacterial communities on roots can help plants to be more drought-resilient, and are currently an intervention under investigation.

Climate-Friendly Soil Interventions

Some work has been done investigating the use of microbial interventions to regenerate soil or provide enhanced resilience to plants. Making use of the natural ability of some microbes to sequester carbon, much research is underway to investigate ways to enlist their help in balancing the carbon ledger. Strategies abound, from using autotrophic organisms like algae to transform carbon into lipids, to manipulating adenosine triphosphate (ATP) to improve carbon sequestration efficiency, to adjusting various metabolic pathways in bacteria, to direct gene editing of photosynthetic bacteria.

Other approaches have focused on the relationship between plants and their rhizobiome, working to increase plant resilience through microbial supplementation. When applied to soil, for instance, some fungi can help plants enhance their drought resistance, which is important in a time of increasing aridification. Bacterial treatments were also able to increase plant tolerance to heat stress by reducing reactive oxygen species, boost plant immunity and also assist with drought stress. Seed coating is an effective delivery method for many beneficial microbes and has been shown to boost plant health.

Microbes have also been investigated for bioremediation efforts, such as the conversion of environmental pollutants, like heavy metals, into stable and less harmful forms. This enhances the safety of agricultural production and helps restore polluted agricultural land.

As creative and emergent as these solutions are, the problem of fossil fuels still accounts for the lion's share of greenhouse gas emissions. Soils, their plants and their microbiomes—the foundation of food production—will continue to suffer from elevated temperatures and atmospheric carbon until these factors can be brought under control.

How can microbial culture collections be used to infer ecological and evolutionary responses to warming soil temperature? Find out in this episode of "Meet the Microbiologist" featuring Dr. Mallory Choudoir.

Author: Christy Clutter, Ph.D.

Christy Clutter, Ph.D.
Christy Clutter, Ph.D., is a scientist, microbiome aficionado and writer whose research work focused on gut immunity and the microbiota, along with public health disparities in nutrition.