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Mini Review

Soil Formation: A Microbial Housing Process. A Mini Review

Zhen Bai

Chinese Academy Of Sciences (CAS) Key Laboratory Of Forest Ecology And Management, Institute Of Applied Ecology, CAS, Shenyang 110016, China


Recieved on: 2024-12-11, Accepted on: 2024-12-26, Published on: 2024-12-31

Abstract

Soil plays a crucial role in global carbon cycling and climate change mitigation, with its function largely dependent upon organo-mineral associations formed through microbial processes. Microbial communities are key drivers of soil genesis, as they facilitate decomposition processes that incorporate nutrients into stable soil aggregates. This article first reviews evidence supporting the idea that soil formation can be viewed as a housing process in which microbial communities act as architects, creating structural elements that fortify soil architecture and enhance their own habitats. It then delves into the mechanisms and driving forces behind soil-microbe interactions and highlights promising strategies for enhancing organic matter accrual in soil. Lastly, it explores the potential of harnessing microbial dynamics to boost carbon sequestration into soil particles, thereby promoting the restoration of degraded lands and fostering more resilient and sustainable terrestrial ecosystems.

Keywords

Microbial housing; Organo-mineral association; Soil formation; Soil organic matter; Carbon sequestration; Soil restoration; Sustainable land management

Introduction

Soil is a dynamic, three-dimensional matrix primarily composed of mineral particles and organic components. The mineral fraction forms the foundational structure, consisting of clay (< 2 μm), silt (2-63 μm), and sand (63-2000 μm). These particles aggregate into structures of varying sizes, including silt-sized aggregates (< 50 μm), microaggregates (50-250 μm), and macroaggregates (250 μm). The organic constituents exhibit binding functions and include metal oxides (Al, Fe), simple compounds (carbonates), macromolecules (proteins, lipids), and residues (humus, char) [1]. Terrestrial organic carbon (OC) majorly stores in mineral-associated organic matter (MAOM, 840-1540 Pg C), particulate organic matter (POM, 715-1395 Pg C), and plant biomass (400-600 Pg C). MAOM-C globally accounts for 34-51% of total terrestrial OC and is most concentrated in forest and grassland than other ecosystems (e.g., shrublands) [2]. POM is commonly derived from partially degraded plant residues, whereas MAOM is always binding to minerals and occluded in microaggregates (< 50 μm). Usually, POM is regarded as a direct precursor of MAOM [3].

High soil quality is characterized by abundant organic matter, optimal microbial activity, large populations of earthworms, stable aggregate pore structure, low bulk density, easy penetrability, and thick topsoil [4]. Soil erosion, a significant threat to soil quality, has been widely studied using the radionuclide 137Cs (T1/2 = 30.17 years). A prior study used 137Cs analysis to investigate 12 black soil profiles and to estimate soil erosion rates in Northeast China. Using the mean erosion rate (2.22 mm/year) as a reference, the black soil will be completely eroded in ~113 years [5]. This highlights the urgent need to understand the processes of soil formation and nutrient retention, which are crucial for effective land management and maximizing the C sequestration potential of terrestrial ecosystems. The soil formation is determined by both plant and microbial biomass and their activities, which influence the input of organic material ("feedstock traits") and the proportion that is incorporated into MAOM ("MAOM formation traits"). This process plays a crucial role in soil C cycling and overall soil health [2].

Soil serves as a habitat for a diverse range of microbes, which are physically separated by aggregate barriers and rarely contact one another directly. Soil structure and microbiome interact with each other, influencing soil fertility [1]. Understanding the interactions between soil structure and microbial communities over millennia raises an important question: does soil structure drive the microbiome, or is it the microbiome that shapes soil structure? Our work on microbial necromass (e.g., amino sugars) formation kinetics has revealed intriguing dynamics in microbial-meditated organic matter formation (Figure 1) [6]. For example, the input of residues from different plant parts (grain, leaf, and root) results in a similar pattern of microbial-derived amino sugar formation. Regardless of the substrate quality or microbial community distinction, amino sugar formation plateaus within 5–10 days and does not continue to increase over a period of 21 days.

 

 Figure 1: Modeled and measured residue-derived amino sugar concentration (ASR) in function of time. GlcNR, GalNR and MurNR stand for residue derived glucosamine, galactosamine and muramic acid, respectively. Modelled values are calculated using ASR = ASR,Max(1?e-kt) where ASR,Max and k are derived by non-linear regression analysis. Data points are averages of three replicates and error bars represent standard errors. NT = no-till (filled symbols) and CT = conventional till (empty symbols). / = grain, q/s = leaf, ¢/£ = root incubated soil. This figure is cited from reference [6].

This plateau effect has sparked the curiosity: why does microbial necromass accumulate rapidly to a certain level, yet fail to increase further over time? Similar patterns have been observed in other studies, suggesting that there may be inherent mechanisms in microbial communities and/or their relationships with soil organic matter (SOM) that restrict further accumulation. The questions arise: are microbes consciously involved in SOM formation, or is it simply an incidental outcome of their activities? What are the mechanisms that drive this process and lead to its eventual plateau? This review provides insights into soil formation process in which microbes often produce organic matter as a by-product of their metabolism and contribute to SOM build-up and stability.

Evidence For Microbial Housing

It is very interesting that microbes can serve as architects in next-generation sustainable architectures for human society [7]. Intriguingly, Venkatesh et al. demonstrated that phylogenetically and ecologically diverse free-living bacteria can colonize fungal chlamydospores stimulated by bacterial lipopeptides (Figure 2a) [8]. This colonization offers bacteria survival benefits under abiotic stress conditions. Albeit SOM is mainly derived from plants and microbes, recent studies propose that microbes dominate in building micro-scale habitats in soil, too [9].

 

 

Figure 2: Evidence for microbial housing process (elements in this figure adapted from related references). a) Free-living bacteria colonize fungal chlamydospores [8], b) Fungi play a vital role in constructing microhabitats, facilitating water movement, and distributing nutrients [10], c) Microbes generate dark grainy residue [11], d) Phenolic compounds are most important in building up SOM [12], and e) Calcium enhances the persistence of SOM by altering microbial transformations of plant litter [13].

For instance, microorganisms, particularly fungi, play a vital role in constructing microhabitats that facilitate water movement and nutrient distribution. Fungal hyphae—referred to as fungal highways—can create networks that support long-range dispersal of water-dwelling organisms (bacteria and protists) and reshape the pore architecture within the soil, developing stream channels among mineral particles along with water mass flow. Fungi can construct hyphae to occupy and obstruct the access to their colonized space, restricting dispersal of large predators such as nematodes. Usually, water and nutrient status constrain water-dwelling bacteria and protists; the shape of microstructures/pore space geometrical characteristics influences fungal dispersal (Figure 2b) [10]. Notably, bacterial necromass, rather than fungal, shows a strong association with soil minerals, thereby influencing the formation of mineral-associated organic C (MAOC) [14]. Furthermore, during anaerobic oxidation of methane, microbes generate black C (both amorphous and crystalline forms) (Figure 2c). Amorphous C is produced from dissolved inorganic C while methane serves as energy source. Amorphous C is highly inert and serves as a scaffold for microbial attachment, providing a protective barrier against environmental stress (toxic compounds). And biogenic amorphous C can also be used to donate, transfer and/or accept electron. Amorphous C accounts for up to 3.2% of the dry weight of cells in microbial cultures and 70% of dark grainy residue [11].

Rapid microbial degradation can lead to a reduction in SOM and high microbial growth efficiency and turnover rates may diminish MAOC, suggesting that microbial products are not the sole driver of soil formation and stability [14]. Phenolic compounds are believed to be most important building blocks in soil, as the application of p-hydroxybenzoic acid (pHB) stimulated soil habiting pHB degraders (e.g., Paraburkholderia and Caballeronia), and the pHB reduction caused greater losses of SOC (positive priming) compared to glucose addition. Further, six Burkholderiaceae phylotypes dominated in situ pHB degradation. These pHB degraders consist majorly of fast-growing bacteria characterized by less C use efficiency (greater C loss, but less incorporation into biomass). Notably, the positive priming effect driven by pHB is distinct from that caused by glucose: pHB decomposition is primarily facilitated by specialized bacteria, while glucose-induced priming involves a broader range of microbial activities. The observed positive priming effect is attributed to a stoichiometric imbalance, where increased C catabolism occurs alongside reduced C anabolism. This results in a predominance of fast-growing bacteria that exhibit lower C use efficiency, leading to greater C loss rather than incorporation into biomass (Figure 2d) [12]. Furthermore, Calcium (Ca) has been shown to enhance the persistence of SOM by altering microbial transformations of plant litter. The application of Ca promotes the growth of surface-colonizing bacteria and increases the conversion of litter-derived C into microbial biomass, leading to reduced CO2 emissions by 4% and improved C use efficiency by 45%. Additionally, Ca aids in retaining nitrogen (N) from litter in MAOM by enhancing associations between mineral and N-rich organic compounds. Moreover, Ca drives the formation of organo-mineral associations via microbially-transformed products, probably resulting from increases in soluble aromatic and carboxylic functional groups (but not aliphatic-C) (Figure 2e) [13]. Moreover, it is reported that permafrost C storage is majorly constrained by organo-mineral protection (SOC-Ca bridges, organically complexed Fe/Al oxides) and microbial diversity (the average of the standardized bacterial and fungal diversity indexes) [15].

Mechanisms and Driving Forces behind Microbial Architects

It is an interesting question: how can SOM accumulate despite microbial decomposition? The interplay between microbial communities and their environment, along with nutrient cycling and organo-mineral associations, significantly influences SOM accumulation. Several key principles govern the microbial housing process. First, the microbial architectures are formed by a porous and internally structured medium composed of weathered rocks and organic debris, providing the physical structure essential for microbial habitation. Second, the particle size distribution of the dominant mineral phase plays a crucial role in shaping pore system and determining how microbes inhabit and interact within these spaces. Third, the presence of a water phase and available substrates is vital as they facilitate biochemical processes necessary for microbial activity and nutrient cycling. Finally, microorganisms themselves modify the pore shapes and biochemical activities, creating dynamic and sustainable architectures that support diverse life styles [16].

Social interactions within microbial communities at the micro-scale can regulate organic matter turnover at larger spatial scales [17]. For instance, the presence of "cheaters"—organisms that exploit resources without contributing to the community—can negatively impact the production of decomposers and extracellular enzymes. This, in turn, slows down the decomposition process and enhances the retention of N-rich microbial necromass, leading to increased organic matter accumulation. The balance between cheaters and decomposers is essential. When N is abundant (e.g., low C/N ratio), fast-growing cheaters can dominate, reducing decay rates. Conversely, in N-poor conditions (e.g., high C/N ratios), cheaters become less competitive, allowing slow-growing decomposers to thrive. This enhances extracellular enzyme production and accelerates the decay rates of recalcitrant substrates. At the micro-scale habitats, the "flash mob" effect of cheaters at the edges of decomposer patches leads to spatial distributions of microbial products, constraining the expansion of microbial-produced patches and resulting in high heterogeneity of decaying residues, great retention of microbially-mediated products, and thus promoting SOM formation and stabilization. All these suggest social dynamics in complex microbial communities are pivotal driving forces in soil formation and stability [17].

Furthermore, nutrient feedback mechanisms, particularly responding to N and phosphorus (P) addition, can alter microbial processes and SOM dynamics. N addition, for example, suppresses lignin-modifying enzymes, resulting in a 22.7% increase in soil recalcitrant C pool and a 9.2% increase in the proportion of recalcitrant C to total soil C storage [18]. On the other hand, increased P levels can reduce the diversity of enzymes involved in C and N cycling. Interestingly, while the addition of P may suppress certain N-acquisition enzymes, it can also enhance the preservation of microbial necromass, indirectly increasing its contribution to SOM. The addition of P indirectly lowered the contribution of lignin phenols to SOC primarily by decreasing fine root biomass (standardized total effect = 0.66), with a decline in microbial decomposition of lignin phenols owing to reduced phenol oxidase activity (standardized total effect = 0.59). These findings suggest that decreased plant lignin content in SOC in response to the addition of P is largely attributed to a greater drop in root C input than drop in C output. Moreover, the addition of P suppresses N-acquisition enzyme (such as leucine aminopeptidase) activity in decomposing microbial necromass, particularly amino sugars. This suppression facilitates the preservation of N-rich microbial necomass in soil, while living microbial biomass (indicated by phospholipid fatty acids), remains unchanged. As a result, microbial necromass contributes more to SOC indirectly [19].

Overall, the interactions between microbes and SOM reflect a complex and unified system. Microbes communicate with each other through signalling substances, fostering beneficial relationships that enhance soil quality. Healthy soils rich in organic matter enable microbes to grow more easily and efficiently, reducing the energy expended on nutrient acquisition and promoting overall ecosystem productivity. In summary, the intricate social dynamics within microbial communities and their responses to nutrient status are pivotal in driving soil formation and stability, highlighting the importance of maintaining healthy ecosystems for sustainable development.

Potential of Microbial Architects in Soil Forming

Global C stock amounts to 899 Pg C at a depth of 1 m in non-permafrost mineral soils. Notably, while these stocks represent 66% and 70% of soil C in surface and deeper layers, respectively, they only account for 42% and 21% of the mineralogical capacity. In particular, regions under agricultural management and deeper soil layers show even larger undersaturation of MAOC. Research shows that soils that are further from their mineralogical capacity are more effective at accumulating C, with sequestration rates averaging three times higher in soils at one tenth of their capacity compared to those at half capacity. This indicates that regions under agricultural management and deeper soil layers have substantial room for improvement in MAOC storage. Over half of SOC is physic-chemically associated with soil MAOC, which is not accessible to microbial decomposition, allowing MAOC to persist 1000-time longer (100-10000 years) than particulate C. MAOC formation occurs through various mechanisms, including ligand exchange, hydrophobic interactions, and cation bridging [20].

Different soil minerals exhibit varying reactivities, with a ranking of kaolinite < montmorillonite < goethite. Though kaolinite and montmorillonite similarly impact MAOC formation, they have distinct cation exchange capacities and surface areas, which should not profoundly influence organic matter and minerals. Soil mineralogy traits govern C stability and loss: phyllosilicate minerals such as kaolinite and montmorillonite (1:1 and 2:1, respectively) are normally negatively charged; in contrast, goethite consists of variably charged metal oxides and hydroxyl groups, which can form the most durable bonds via ligand exchange with microbial-derived hydroxyl/carboxyl-rich compounds (e.g., oxalic acid, glutamate). As mineral reactivity increased, root-exudate primed C accumulation (C pools) increased but CO2 flux decreased [21]. Therefore, SOM can be improved by POM- and MAOM-targeted managements. POM–centric strategy, i.e., input of highly structured and recalcitrant plant residues, should be applied in soils, where reactive surface areas of minerals have reached their theoretical C-saturation limit (e.g., forests, croplands). The POM management (leaves and branches) applied to soils with C-saturated minerals may promote persistence of macro aggregates and SOM stability. MAOM-strategy should be used for soils far from C-saturation. Aerobic grassland soils, for example, have great potential C accrual in association with minerals which are C deficit and contain high proportion of reactive surfaces [3].

Microbial processes play an essential role in soil C dynamics, particularly in the formation and stabilization of MAOC. By leveraging microbial "architects" to enhance soil structure and mineral-organic matter interactions, we can improve C sequestration, boost soil fertility, and restore degraded ecosystems. For instance, the restoration of degraded lands can be achieved through particular soil-microbe interactions. Techniques such as applying algae to improve water retention, using fungal hyphae to increase soil porosity, and employing microbes that produce either hydrophilic or hydrophic substances to modify soil surface microtopography are beneficial [22]. Furthermore, arbuscular mycorrhizal fungi (AMF) form symbiotic relationships with plant roots, extending hyphal networks into the soil and enabling plants to access otherwise inaccessible nutrients like P and N in exchange for C compounds. This nutrient exchange enhances plant growth and increases organic matter input to the soil, promoting SOM formation. Nitrification inhibitors—e.g., dicyandiamide—can largely offset AMF-mediated OC decomposition, which suggests that high demand for soil NH4+ is the driving force in enhancing AMF-mediated decomposition [23]. These insights highlight the importance of understanding microbial roles in soil health, with significant implications for sustainable land management practices and C storage strategies.

Conclusion And Perspective

The formation and persistence of soil are essential for maintaining soil C stocks and supporting terrestrial ecosystem services. Microbial communities play a pivotal role in shaping soil structure and C sequestration potential. By inoculating soils with specialized microbial groups that are adapted to various environmental stressors—such as drought, excessive moisture, cold, and heat—we can enhance its C sequestration capacity and improve soil quality (Figure 3).

 

 Figure 3: Diagram of managing microbial housing process to increase SOM and create self-sustaining ecosystems. Note: H = human beings’ management; M = microbial communities; P = soil particles; D = plant residue decomposition and root exudations.

Microbial dynamics, particularly the associations between cheaters and decomposers, are central to the cycling and retention of nutrients. The "flash mob" effect of cheaters at the edges of decaying organic matter constrains spatial expansion of microbially-transformed products, resulting in high heterogeneity of decaying residues and living microbiota, slowing down nutrient turnover, and favoring long-term nutrient storage in soil. In addition to these natural microbial processes, external interventions such as the use of nitrification inhibitors—e.g., dicyandiamide—can significantly reduce organic matter decomposition by slowing microbial activity, which in turn increases the residence time of SOC.

As we look to the future, the principles of soil biology may not only be critical for sustaining terrestrial ecosystems but could also have applications in extraterrestrial habitats. The potential to create self-sustaining ecosystems on distant planets, such as the Moon or Mars, could rely on understanding and harnessing microbial communities for soil health and nutrient cycling. In such environments, we could imagine ecosystems with free living forests, grasses and even clear lakes, reminiscent of those we are striving to understand and protect on Earth. The lessons learned from soil biology today may one day contribute to sustaining life beyond our planet.

Funding

This research is funded by the National Natural Science Foundation of China (32371732 and 42230515), and Hunan Natural Science Foundation - Departmental Joint Fund (2024JJ8297).

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