Regenerating Soil Microbiome: Balancing Microbial CO₂ Sequestration and Emission

Abstract

Soil microbiome plays a significant role in soil’s ecosystem for soils to be physically and biologically healthy. Soil health is fundamental for plant growth and crops productivity. In the introduction part, the roles and dynamics of the microbial community in soils, primarily in the cycle of soil organic carbon and CO2 release and absorption, are deliberated. Next, the impact of crop management practices and climate change on the soil carbon balance are described, as well as other issues related to soil degradation, such as unbalanced nutrient recycling and mineral weathering. In response to these issues, various approaches to soil regeneration have been developed in order to foster an efficient and active soil microbiome, thereby balancing the CO2 cycle and carbon sequestration in the soil ecosystem.

1. Introduction

Microbes are the most diverse organisms on the planet, both in terms of species and in terms of driving vital Earth system operations like the carbon cycle. The majority of this microbial biodiversity is found in soils [1]. According to Lederberg and McCray [2], the term microbiome refers to “the biological community of commensal, symbiotic, and pathogenic microbes that share human body space.” This term grew in popularity as its definition evolved from organisms as taxonomic units (i.e., microbiota) to a collective genetic material throughout the years. However, as the term’s popularity grew, there are various definitions of the term microbiome in the scientific literature.

Nowadays, most “microbiome” research focuses solely on bacteria, and the term “microbiome” is used interchangeably with “bacteria.” As a result, new words for various microbial groupings have emerged, such as mycobiome, which refers to fungi, virome for the viruses, and eukaryome for the microbial eukaryotes [3]. Furthermore, the composition of microbiomes is known to change across time and space, making it difficult to find consistent and dependable sources of specific microbiomes [4]. The microbiome of the Earth accounts for almost half of all biomass on the globe [1]. Recent advances in DNA sequencing techniques have expanded our understanding of microbial biogeography, particularly among bacteria and fungi [5, 6]. Currently, the diverse composition of soil microbial community is widely known worldwide. The soil microbiome governs the biogeochemical cycling of macronutrients, micronutrients, and other elements that are vital for plants growth and animal life.

Microbiomes play an important role in a variety of biogeochemical processes, including the carbon and nitrogen cycles, which are necessary for ecosystems to function properly and sustainably. What functions do bacteria play in nutrient cycling and carbon sequestration to support the forests? It is critical to investigate the dynamics of microbial communities in order to comprehend their vital function in such a unique ecosystem. Acknowledging microbial ecology will aid in their management practices and protection, allowing peat accretion to continue and their carbon sequestration capacity to be protected [7].

The significance of soil microbiome activity in the soil ecosystem dynamics demands special consideration, as it promotes soil health and plant productivity [8]. Soil microbial activity is a possible indicator of soil quality as it responds quickly to changes in soil management and the environment. The carbon in crop residues moves via soil microbial biomass at least once, where it is moved from one C pool to another and eventually lost as carbon dioxide (CO₂) [9]. It is critical to understand the factors that determine the richness of soil bacterial communities, as well as the organization of these communities, in order to forecast the responses of an ecosystem toward a specific environment. Changes in microbial populations or activity can occur prior to visible changes in soil physical and chemical properties, acting as an early indicator of soil improvement or degradation [10].

Soil characteristics such as pH, carbon, and nitrogen have been shown to influence soil microbial diversity and biogeography [11]. As a result, changes in the structure and behavior of soil microbial communities are more likely to be caused by differences in soil characteristics. Aside from that, soil organic matter (SOM) is critical to the function and quality of the soil. The high amount of SOM could increase nutrient availability while also improving the physical and biological features of the soil [12]. The level of soil organic carbon (SOC) is used to quantify the amount of SOM, and changes in SOC have an impact on the carbon (C) and nitrogen (N) cycles in terrestrial ecosystems [13]. The combined effects of chemical and biological features of the soil will affect the organic C and N fractions in organic compounds. As a result, understanding the processes that determine soil fertility, which is critical in farmland production systems, requires knowledge of soil microbial community dynamics and the factors that influence those dynamics in croplands.

2. CO₂ balance in soils

The technique of increasing soil carbon storage by reducing net CO₂ emissions in agricultural soils is known as carbon sequestration. Soil carbon sequestration (SCS) is the process of absorbing C-containing compounds from the atmosphere and storing them in soil C pools. Variations in the ability to store carbon in soils have been linked to the activity of the soil microbial community (SMC). The turnover and supply of nutrients, as well as the rate of decomposition of SOM, are all influenced by the structure and activity of the SMC, which is crucial for the maintenance of soil ecosystem services. As a result, the influence of farming activities on SMC and SCS should be quantified as part of any soil management practice’s sustainability evaluation.

Because a big fraction of the biomass is produced in agricultural systems cycles via the soil decomposer community, the quantity of gross CO₂ fluxes between agricultural soils and the atmosphere is significant. The difference between photosynthetically fixed CO₂ entering the soil as plant wastes and CO₂ exhaled during decomposition, on the other hand, is far smaller. This distinction determines whether the ecosystem is a CO2 source or sink in terms of its net carbon balance.

Raising the C content of agricultural soils is a well-known technique. The equilibrium between C inputs from plant residues and C losses, primarily through decomposition, determines the soil C levels. The increasing residue inputs and/or delaying breakdown rates (i.e., heterotrophic soil respiration) also govern the C level in soils. The relationship between C inputs and SOC levels could be straightforward; in which many agricultural soils’ steady-state C contents have been shown to be linearly related to C input levels, that is compatible with the current SOM dynamics theory [14]. This may not be the case in soils with exceptionally high quantities of carbon, which may exhibit “saturation” behavior.

The following factors must be considered when developing soil carbon sequestration management practices and policies: Soils have a finite capacity to store carbon, gains in soil carbon can be reversed if proper management is not maintained, and fossil fuel inputs for various management practices must be factored into the total agricultural CO₂ balance [15].

The interaction of numerous ecosystem activities, the most important of which are photosynthesis, respiration, and decomposition, results in the SOC level. Photosynthesis is the process of converting atmospheric CO₂ into plant biomass. The root biomass of a plant determines the majority of SOC ingestion rates, however, litter deposited by plant shoots also plays a role. The growth and death of plant roots, as well as the transfer of carbon-rich molecules from roots to soil microbes, produce carbon in the soil both directly and indirectly.

Decomposition of biomass by soil microbes leads to carbon loss as CO₂ as a result of microbial respiration. Through the formation of humus, a material that gives carbon-rich soils their unique black hue, a small fraction of the original carbon is kept in the soil (Figure 1). These various forms of SOC differ in their recalcitrance, or resistance to decomposition. Humus is a recalcitrant plant that takes a long time to degrade, resulting in a long period of time spent in the soil. Plant waste is less abrasive; therefore, it stays in the soil for a shorter period of time. When carbon imports and outputs are in equilibrium, there is no net change in SOC levels. When carbon inputs from photosynthesis exceed carbon losses, SOC levels rise over time.

Figure 1.

Carbon inputs from photosynthesis and carbon losses from respiration govern the carbon balance within the soil. Humus, long-lived storage of SOC, is formed through the decomposition of roots and root products by soil bacteria. Created with BioRender.com.

2.1 Impact of climate change on soils carbon

The effects of climate change on soil functions, including soil carbon, is a complex subject since numerous direct and indirect factors are involved. For instance, the atmospheric temperature may affect the rate of SOM decomposition, a process that could release greenhouse gases that contribute to climate change [16]. The effects of moisture and temperature due to climate change will be highlighted as key parameters since soil humidity and temperature are among the most important variables in determining microbial activity and therefore SOC [17].

One of the most critical effects of climate change on soil is the alteration of rainfall patterns, resulting in intense rain and drought. These phenomena may be beneficial or detrimental according to the agricultural activities and climatic requirements, but they present economic challenges nonetheless [18]. The selective migration of soil particles, where fine particles and micro-aggregates are transported via erosion while macroaggregates are left in situ resulted in different carbon mineralization patterns. These lateral redistributions of sediments create (i) eroded environments dominated by large particles exhibiting increased porosity and permeability but decreased water-holding capacity, and (ii) deposited environments where enrichment of fine particles enhances the water holding capacity [17]. Similar to water erosion induced by water runoff, wind erosion induced by drought also redistributes a large amount of SOC as well as soil inorganic carbon (SIC). In addition to soil particles, the net effects of these soil C redistribution on the soil as a C source or sink also depend on site-specific topography (such as slope gradient and location), distribution distance, and duration [19]. Some of these interacting factors are outlined in Figure 2.

Figure 2.

Interaction of diverse factors affecting soil as C source or sink.

Among the most consistent narrative of climate change is climate warming as a result of rising temperature [20]. Climate warming has been associated mainly with SOC decomposition due to the effects of temperature on soil microbial community and their enzymatic and metabolic activities. Unlike the effects of moisture, however, the dynamic relationship between temperature and soil C is less certain and more constrained. In general, elevated atmospheric temperature could also elevate soil temperature, which would subsequently elevate microbial processes and SOC decomposition rate [21]. This is not always the case due to the difference in temperature sensitivity of soil biota, especially the microbial community, where the higher-temperature sensitivity such as in colder regions exhibited more enhanced soil respiration, potentially resulting in a net efflux of C toward increased atmospheric CO₂ in comparison with those inhabiting soils in hotter regions [22]. In contrast, a higher rate of microbial OM decomposition was reported in hotter regions, suggesting other environmental factors that may affect the SOC, including topography, soil texture, and pH. Ultimately, climate warming leads to decreased SOC input and increased SOC output [23].

2.2 Effect of agronomic management on soils microbiome and CO₂ balance in soils

Agronomic management involves a combination of soil and crop management practices that when appropriately applied will improve soil performance and nutrient availability, and contribute to better growth and higher crop yield [24]. These management practices can be further categorized into an untargeted approach based on common agricultural practices, or targeted approaches based on specific interactions between soil and plant. Targeted approaches often involve biotechnological applications such as biofertilizers and biostimulants. Regardless of the type of approach, the soil microbiome will be affected either directly or indirectly. Considering that the soil microbiome is regarded as the primary organism that may influence the overall plant health due to its close interaction with plant roots, applying the right management practice is crucial toward achieving the goal of food security for the growing global population [25]. Therefore, soil microbiome must not be overlooked in agronomic management practice especially when SOM is concerned due to its major role in soil C pool. For instance, additional OM applications may result in increased decomposition and reduced C storage due to reduced microbial C use efficiency, positive priming effect from enhanced mineralization of SOM, as well as increased C skimming due to accumulation of microbial products and residues, or necromass over time [26].

SOC is known to be directly influenced by the stabilization and decomposition of SOM. Therefore, agronomic management that boosts SOM such as fertilization, conservation tillage, cover cropping, and crop rotation will also affect SOC [27]. More importantly, soil biotic and abiotic factors such as texture, moisture, C/N ratio, SOC content, pH, climate, vegetation, and land use also affect the persistence of SOM, and ultimately the C pools [28]. It is due to the complex interactions of these various factors that it is uncommon for an ecosystem to change from a net C source to a C sink in a relatively short time [29]. Thus, agronomic management practice must take into account the most appropriate way to minimize its impact on climate change [27].

Crop management refers to a collection of agricultural activities aimed at enhancing crop growth, development, and production. It starts with seedbed preparation, seed sowing, and crop maintenance and concludes with crop harvest, storage, and commercialization. Although fertilization not only improves soil fertility and quality but also crop production, it causes soil pollution, soil hardness, organic matter mineralization, increased nitrous oxide emissions, and nitrate leaching into groundwater and surface waters [30]. Fertilizer application considerably affected the soil C/N ratio. When Liu et al. [30] analyzed chemical and organic fertilizers, they discovered that chemical fertilizer (NPK) treatment lowers soil pH, and when combined with organic fertilizer, it lowers the soil pH even more. Furthermore, the relative populations of microbiome components varied after organic waste (straw) treatment due to changes in ammonium nitrogen (NH₄⁺-N) and nitrate nitrogen (NO₃⁺-N).

Bhattacharyya et al. [26] reported that the influence of organic matter accessibility on the significance of SMC to soil C control can be explained in numerous ways:

1. Increased organic matter inputs may hasten decomposition and decrease C storage by reducing microbial C usage efficiency.

2. Greater organic matter additions, labile carbon inputs, or nutrient inputs result in increased SOM mineralization in soil, which is referred to as a positive priming effect.

3. Increased organic matter additions can boost C skimming by increasing the formation of microbial necromass over time.

The interrelationship between nutrients, roots, water, and SOM is another component that influences SOM to build up in more complex cropping systems. In the surface soil layer, available nutrients are dynamic; they may be reduced by net microbial immobilization during heavy litter intake times and abundant during times of net mineralization. Microorganisms regulate root proliferation through their effects on nutrient availability and water, while roots influence microbial activity through their effects on nutrient availability. Increased litter inputs encourage competition for nutrients between microorganisms. When litter and organic matter pool sizes increase over longer periods, mechanisms favoring C sequestration are reinforced such as improved plant water availability, stronger nutrient recycling capacity, and reduction of nutrient leakage. Since microbial and plant respiratory processes are dominated by nutrient availability, cover crops that increase CO₂ and N₂O fluxes would have a good impact on soil respiration.

The pH of the soil influences microbial activity. As a result, soil management activities such as liming have an impact on soil emissions as additional carbonate can be emitted as CO₂. Soil emissions are reduced when the soil is acidic. The ideal pH for methanogenesis (CH₄ generation) is found between pH 4 and 7. CO2 emissions are at their highest when the pH levels are neutral. Under acidic soil conditions, N2O emissions are reduced. Because the balance between NH3 and NO3 flips to ammonia at higher pH values, nitrification rises. However, there was no evidence of a link between NO and N2O emissions and pH. Denitrification produces NO emissions under acidic soil conditions, whereas nitrification produces NO emissions under alkaline soil conditions.

Crop rotation (CR) changes soil microbial profiles toward microorganisms with C-sequestering characteristics. According to Venter et al. [31], microbial diversity and richness can be increased by 15 and 3.4%, respectively, using CR. Different crop rotation practices may cause variations in soil C storage and SMC use. After a long-term CR practice involving legumes, SOC stock, MBC, and soil enzymatic activity (acid/alkaline phosphatase, beta-glucosidase, and arylsulfatase) may rise. The presence of legumes in CR may help to protect the SMC in general.

3. Balancing soil CO₂: a race against time

If left undisturbed, soil carbon may remain sequestered for thousands of years [32]. Disturbed soils, which are primarily due to intensive cultivation, have decreased the soil’s ability to maintain and store carbon, amplifying the impacts of climate change and the accompanying costs to mitigate them [33]. While soil ability as a carbon sequester varies with location, climate, and soil type, one common cause of carbon loss, the majority of which is emitted as carbon dioxide is due to unsustainable management practices at the macroscopical level. Further approaches to sustainable management practices should consider and employ our current knowledge at the microscopical or cellular level. Acknowledgment and immediate actions from all relevant stakeholders must be engaged in the race against time to mitigate the climate change while ensuring the benefits for the environment, community, and economy.

3.1 Macroscopical level: sustainable soil management

Among the easiest options to avoid or reduce soil carbon loss are sustainable soil management practices at the ground level where the results of carbon sequestration can be detected within several years of implementation [34]. Enhanced food security and nutrition as well as improved ecosystem services are some of the possible benefits to be gained over the short to medium term (Figure 3).

Figure 3.

Benefits of sustainable soil management practices.

Sustainable soil management practices involve the increase of SOM to offset the effects of land conversion, tillage disturbance, soil erosion, and leaching from human activities [35]. The conundrum in sustainable soil management practices is that determining the best practices does not only depend on the dynamic properties of the soil, but also relies on various environmental conditions and social and economic factors. Nevertheless, several studies agreed that sustainable soil management practices should include the following:

1. Adoption of no-till or conservation tillage to preserve soil structure [36];

2. Use of cover crops to increase SOM, water holding capacity, and protection from wind and water erosion [37];

3. Organic soil amendment from plant residues, compost, and biochars to lower C:N ratio [38]; and

4. Better irrigation to manage soil salinity [39].

Following these strategies, the measurement of soil CO₂ flux can be used to determine whether the ecosystem is functioning as a net carbon sink [40]. This is important since there are reports that the application of organic manures and residues could increase CO₂ emission, which negates the goals of mitigating climate change [41]. Verifying the most appropriate sustainable soil management practices is deemed of the utmost importance to ensure successful soil-specific microbial carbon sequestration.

3.2 Microscopical level: engineered microorganisms

Modern climate change mitigation techniques have included the use of biotechnology and engineering technologies at the cellular level in recent years. Microorganisms, both autotrophic and heterotrophic, can be genetically modified to boost their CO2 sequestration ability, notably by increasing microbial CO2 fixing and decreasing CO2 release. Due to the presence of a complete CO2-fixing pathway and the ability to transfer energy from sunlight and inorganic compounds into cellular metabolites, autotrophic bacteria have evolved to subsist only on CO2. Heterotrophic microbes, on the other hand, rely on organic substances to thrive [42]. Therefore, the autotrophs could be engineered to improve the efficiency of their CO₂-fixing pathway, energy-harvesting systems and to regulate their cell resources, whereas the heterotrophs could be engineered to improve their carboxylation reactions in the metabolic pathways, to establish non-native CO₂-fixing bypass and ultimately to engineer them into autotrophs (Table 1).

Microorganisms	Targets	Strategies	References
Autotrophs	Improve the efficiency of the CO2-fixing pathway	(1) Regulate the expression of CO2-fixing pathway enzymes; (2) Improve the catalytic properties of; carboxylases; (3) Create synthetic CO2-fixing pathways.	[43, 44]
	Developing and optimizing energy harvesting systems	(1) Optimize natural photosystems; (2) Create artificial photosystems; (3) Develop electricity utilizing systems.	[45, 46]
	Regulating cell resources	(1) Enhance the product synthesis pathway; (2) Engineer transcription; factors; (3) Provide organic carbon resources.	[47, 48]
Heterotrophs	Improve carboxylation reactions in metabolic pathways	(1) Augment the activity of carboxylases; (2) Increase intracellular CO2 availability.	[49, 50]
	Establish non-native CO2-fixing bypass	(1) Establish autotrophs transferred non-native CO2-fixing bypass; (2) Create artificial pathways.	[44, 51]
	Engineer heterotrophs into autotrophs	(1) Install complete CO2-fixing pathways; (2) Equip energy harvesting systems.	[46, 52]

Table 1.

Selected strategies to improve microbial CO₂ sequestration.

Modifications of both autotrophic and heterotrophic microorganisms to increase their efficiency in CO₂ sequestration via genetic engineering approaches are highly promising strategies for mitigating climate change. Lower costs of production and the naturally rapid growth rate of soil microorganisms should accelerate its adoption as a reliable CO₂ sequestration strategy. Furthermore, microbial CO₂ sequestration can be applied directly to complement agricultural activities on the same land compared with conventional CO₂ sequestration technologies that require purpose-built infrastructures that compete for land resources [53].

4. Conclusion

Soil microbiome activity has a huge implication on soil ecosystem dynamics, generally by promoting soil fertility and plant productivity. Soil is also a storage for carbon bulk either as SOM or SOC in terrestrial ecosystems. Carbon storage is the result of symbiotic interactions between plants and microbes in soils, through dynamic ecological processes of photosynthesis, decomposition, and soil respiration. The interaction and carbon sequestration are complicated to be measured precisely. Nonetheless, various research in recent years has clarified that human activities and climate change have had a significant impact on the soil’s ecosystem, thus necessitating effective carbon balancing measures. As the shift toward sustainable agriculture is strengthening, the carbon footprint is one point of interest to benchmark the level of sustainability in agriculture activities. Moving forward, many techniques for carbon balancing and mitigation in soils and plant dynamic systems can be used, both at the macroscopical and microscopical levels of soil management.