Sustainable agriculture is a cornerstone strategy for balancing global food security with environmental stewardship amidst escalating climate challenges and anthropogenic pressures [1]. Central to this paradigm is the rhizosphere microbiome—a dynamic consortium of bacteria, fungi, and archaea that colonizes the soil–plant interface. These microorganisms orchestrate essential agroecological processes through symbiotic relationships with plant roots [2], directly influencing nutrient acquisition, stress resilience [3], and overall soil ecosystem function [4].

The root-associated microbiota is typically dominated by Proteobacteria (~50%), Actinobacteria (~10%), Firmicutes (~10%), and Bacteroidetes (~10%), and exhibits notable host-specific structuring. In contrast, the broader rhizosphere maintains greater phylogenetic diversity, supporting a wide range of ecological roles [5]. By decomposing organic matter and solubilizing mineral nutrients, rhizosphere microbes enhance phosphorus availability by 20–30% and improve nitrogen-use efficiency through symbiotic fixation pathways [6]. They also activate systemic resistance against pathogens via phytohormone modulation (e.g., jasmonic acid and ethylene signaling) and antibiotic production, reducing disease incidence by 40–70% [7]. Furthermore, microbial synthesis of osmoprotectants and modulation of root architecture improve crop tolerance to drought and salinity [8]. Through biofilm formation and polysaccharide secretion, these organisms enhance soil aggregate stability by 15–25% in loam soils, as evidenced by meta-analyses of plant growth promoting rhizobacteria (PGPR) inoculations [9]. Additionally, they contribute to the degradation of agricultural pollutants, including a 60–90% reduction in pesticide residues via enzymatic detoxification [10].

Recent advances in molecular tools have revolutionized our ability to harness these microbial communities. High-throughput sequencing and metagenomics now allow precise mapping of microbial consortium dynamics across diverse soil types and management regimes [11]. Meanwhile, CRISPR-based engineering of nitrogen-fixing bacteria has increased symbiotic efficiency by 1.5-fold in non-leguminous crops [12]. Field trials demonstrate that tailored microbial inoculants can raise crop yields by 12–40% while reducing synthetic fertilizer inputs by 30–50%, resulting in carbon footprints 2.3 times lower than conventional practices [13].

Despite these advances, translational challenges remain. Heterogeneous field conditions often reduce inoculant efficacy, with survival rates falling below 20% in arid or acidic soils [14]. Regulatory frameworks also lag behind technological innovation; only about 15% of characterized PGPR strains have been commercialized worldwide [15,16].

Previous reviews have laid important foundations for understanding rhizosphere microbiomes. Early work focused on specific microbial groups such as nitrogen-fixing rhizobia [17] and phosphate-solubilizing bacteria [18], clarifying their roles in nutrient cycling. The advent of molecular tools prompted a paradigm shift, with meta-analyses revealing microbial community responses to climate stressors [19] and agronomic practices [20]. More recent reviews have highlighted the co-evolution of plants and root-associated microbes [21,22] and the agronomic potential of PGPR [23]. However, many of these studies compartmentalize microbial functions (e.g., treating biological nitrogen fixation separately from disease suppression) or emphasize theoretical frameworks over practical application.

In contrast, this review connects discrete microbial traits—such as siderophore production or 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase activity—to field-scale outcomes, including yield increases of 12–40% under microbial inoculation [24] and reductions in synthetic fertilizer dependence by 30–50% [25]. Unlike reviews focused solely on yield optimization, we emphasize triple-win solutions: enhancing food security [26], mitigating climate change [27], and restoring soil health—exemplified by a 15–25% improvement in aggregate stability through biofilm formation [28].

Acknowledging the persistent gap between laboratory discoveries and field implementation, we propose actionable strategies such as nano-encapsulation to improve microbial survival [29], CRISPR-engineered inoculants [12], and policy frameworks to promote biofertilizer adoption in developing regions.

This review integrates three decades of research to present a coherent roadmap for rhizosphere engineering in sustainable agriculture. We highlight: (1) Synergistic combinations of nitrogen fixers (e.g., Azospirillum), phosphate solubilizers (e.g., Pseudomonas), and biocontrol agents (e.g., Trichoderma) that improve field adaptability. (2) Nano-encapsulation techniques that increase microbial survival from 14% to 68% under drought stress [30]. (3) pathways to align microbial biotechnology with the United Nations Sustainable Development Goals (SDGs), particularly Zero Hunger and Climate Action. By clarifying the mechanisms and scalable applications of rhizosphere engineering, this work provides a practical guide for translating laboratory breakthroughs into landscape-level agricultural sustainability.

The rhizosphere microbiome represents a critical interface for plant-environment interactions, with emerging evidence highlighting its pivotal role in sustainable agricultural systems (Fig. 1). Advances in analytical methodologies have transformed our understanding of these microbial communities, particularly under abiotic stress. Recent studies in summer maize systems reported a 51.7% reduction in aboveground biomass under combined drought–heat stress, alongside a 34.5% decrease in root biomass and a significant enrichment of stress-responsive Gemmatimonadota [31]. While these shifts suggest adaptive microbial strategies—such as potential enhancement of nitrogen assimilation via L-valine secretion—mechanistic causality remains to be fully elucidated, highlighting the need for controlled experiments to define functional roles.

Modern molecular techniques have largely overcome the limitations of traditional culture-based methods [32]. For example, high-throughput sequencing—such as Illumina-based 16S rRNA gene amplicon sequencing [33,34]—coupled with advanced bioinformatics tools [35], now enables precise monitoring of microbial community shifts under different agricultural practices. Although older techniques like PCR-denaturing gradient gel electrophoresis (PCR-DGGE) are still useful for rapid fingerprinting of microbial diversity [36], metagenomic sequencing [37] provides deeper insights into the functional gene repertoire of the rhizosphere microbiome. Furthermore, innovative cultivation strategies based on ribosomal RNA operon copy number [34] are now emerging to close the microbial cultivation gap and expand the reservoir of strains for bioinoculant development.

Environmental factors play a decisive role in shaping rhizosphere community architecture through complex, interacting mechanisms (Fig. 2). Soil physicochemical parameters exert primary control; for example, moisture fluctuations can reduce bacterial richness by 15% under variable wetting regimes [38], and pH strongly influences phosphatase activity. Organic matter content is another key modulator, boosting microbial abundance by up to 30% via nutrient supply [39]. Notably, soil multifunctionality correlates strongly with microbial network complexity across soil profiles [40], underscoring the importance of soil health in agricultural sustainability.

Plant–microbe interactions are central to rhizosphere engineering strategies. Corn seedlings co-inoculated with root exudates and Azospirillum brasilense Ab-V5 showed a 50% expansion in root area and a 19% increase in bacterial enrichment [41], demonstrating the potential for targeted microbial recruitment. Root exudate-mediated chemoattraction [42] facilitates the establishment of beneficial consortia that improve nutrient acquisition and stress resilience [43]. Growth-stage-dependent exudation patterns [44] further enable dynamic microbial adjustments to environmental stressors, particularly under phosphorus or nitrogen limitation.

Microbial community dynamics are governed by complex interaction networks with direct agricultural relevance. For instance, an airlift partial nitritation-anammox system achieved 95.1% nitrogen removal efficiency at optimal C/N ratios [45], illustrating how microbial synergies can enhance nutrient cycling. Competitive exclusion and symbiotic cooperation [46] drive community succession, with mycorrhizal associations offering particular promise for improving soil structure [47]. There is also emerging evidence that microbial consortia can adapt to climate extremes; drought-tolerant communities, for example, increased soil organic carbon by 12% in maize systems [48,49].

The rhizosphere microbiome functions as an integrated, self-regulating system where environmental parameters, plant physiology, and microbial ecology converge (Table 1). Key operational mechanisms include optimizing nutrient cycling via enzymatic activity modulation, transmitting stress signals through phytohormone networks, suppressing pathogens through competitive exclusion, and enhancing soil structure via polysaccharide production. Together, these functions position rhizosphere engineering as a cornerstone of sustainable agricultural intensification.

Current applications focus on developing bioinoculants for specific stress tolerance, implementing precision microbiome management through farming practices, enhancing carbon sequestration via microbial consortia, and optimizing nutrient-use efficiency. Future research should prioritize understanding eco-evolutionary feedbacks under climate change [58] and developing predictive models for plant–microbe–environment interactions. Integrating multi-omics approaches with agronomic evaluations will be essential to translate insights from microbial ecology into field-scale applications, ultimately realizing the potential of microbiome-driven sustainable agriculture.

Rhizosphere growth-promoting microorganisms are vital drivers of sustainable agriculture, orchestrating multifaceted interactions with plant root systems (Fig. 3). Their mechanisms of action operate through three primary pathways: (1) enhancing nutrient assimilation and soil health, (2) regulating phytohormone biosynthesis and homeostasis, and (3) directly stimulating plant growth via hormone-mediated processes involving gibberellins, auxins, and cytokinins [59]. These microbes synthesize and degrade plant hormones such as auxins and gibberellins, while also producing regulatory compounds like choline and eugenol that optimize metabolic pathways in crops and woody plants through enhanced cell division and elongation [60]. For example, applying alginate oligosaccharides (2.5 g L⁻¹) under moderate moisture conditions increased citrus yield by 15–20%, improved water use efficiency by 12–13%, and reduced irrigation demand by 620–700 m³ ha⁻¹, demonstrating benefits for both crop productivity and soil health [61].

PGPR exemplify these roles by decomposing organic matter to release nutrients, enhancing soil moisture retention and aeration, and increasing crop yields by up to 40% under abiotic stress [57]. Beyond nutrient provision, PGPR produce antimicrobial compounds that suppress soil-borne pathogens such as Phytophthora spp., reducing disease incidence by 60–70% [62]. However, their application requires caution due to potential risks of antibiotic resistance gene transfer to native microbiota, highlighting the need for long-term ecological assessments [63].

The rhizosphere microbiome further strengthens agroecosystem resilience by modulating root architecture through volatile organic compounds (VOCs) and optimizing photosynthetic efficiency via endogenous hormone regulation [64]. Microbial consortia, particularly within the Firmicutes and Pseudomonadota groups, exhibit dual functionality—stimulating plant growth while suppressing pathogens through metabolite production [63]. For instance, Pseudomonas sp. ST-TJ4 emits 1-undecene (75.97%), effectively inhibiting fungal pathogens and reducing root rot incidence by 70% [53].

Pathogen management remains a critical challenge, with fungal and nematode interactions posing significant threats. Omics technologies have advanced our understanding of fungal pathogenicity mechanisms—including toxin production and nutrient disruption—while also revealing the symbiotic potential of arbuscular mycorrhizal fungi [65]. Conversely, root-knot nematodes can be suppressed through eco-friendly biocontrol strategies using antagonistic microbes, which enhance systemic resistance and reduce crop losses by 40–50% [66].

Despite these advances, translating laboratory successes to field applications remains difficult. Heterogeneous soil conditions often reduce inoculant survival rates below 20%, and regulatory frameworks have not kept pace with microbial biotechnology innovations [67]. A key ecological barrier is colonization resistance: resident soil microbial communities, shaped by organic carbon chemistry, prime plant immunity and create biochemical barriers against introduced inoculants [68]. By harnessing the multifunctional roles of rhizosphere microorganisms, agriculture can achieve sustainable intensification that balances productivity with ecological stewardship. Future efforts should prioritize scalable microbial formulations, interdisciplinary research on plant–microbe–environment interactions, and policy integration to bridge the gap between discovery and implementation.

Rhizosphere microorganisms critically enhance crop nutrient acquisition, thereby supporting sustainable agricultural productivity (Fig. 4). Among these, nitrogen-fixing microbes convert atmospheric N₂ into plant-available forms such as ammonia and nitrate. In legume systems, symbiotic nitrogen fixation and rhizodeposition significantly elevate soil nitrogen levels, a process functionally analogous to the general role of rhizosphere microbes in facilitating crop nutrient uptake [69]. Microbial transformations—including ammonification and nitrification—convert organic nitrogen into inorganic forms, contributing up to 144 kg N ha⁻¹ from crop residues and an additional 50 kg N ha⁻¹ yr⁻¹ via biological nitrogen fixation [52]. Thus, these microorganisms directly supply nitrogen to plants while enhancing soil N availability and driving the nitrogen cycle.

Beyond nitrogen, these microbes improve overall soil structure and fertility. Integrative application of organic and chemical fertilizers, including phosphorus-solubilizing agents like Trichoderma and phosphate-solubilizing bacteria (PSB), boosts yields in systems such as maize-wheat [70]. Microbial synthesis of organic compounds further stabilizes soil aggregates, improving aeration and stability. For example, extracellular polymeric substances (EPS) from Microcystis aeruginosa show high heavy-metal sorption capacity (44.81 mg g⁻¹ for Ni²⁺ and 37.06 mg g⁻¹ for Cu²⁺), illustrating a dual role in soil health and environmental remediation [71]. Additionally, through the production of bacteriocins and secondary metabolites, beneficial rhizosphere microbes inhibit pathogens and enhance crop resilience to abiotic stresses such as drought and heat [72]. Selected sugarcane rhizobacteria, for instance, exhibit substantial nitrogenase (up to 26.59 nmol C₂H₄ mg protein⁻¹ h⁻¹) and ACC deaminase activities (up to 75.63 μmol mg protein⁻¹ h⁻¹), underscoring their potential to improve growth, nutrient availability, and disease resistance [73].

Phosphate-solubilizing microorganisms (PSB and fungi) increase soil phosphorus availability by converting insoluble forms into plant-accessible phosphate via acidolysis and enzymolysis [74]. Co-composting phosphate rocks with rhizosphere soil enhances labile P, correlated with activity of phosphate-solubilizing fungi and alkaline phosphatase (phoD) [75]. Inoculation with strains such as Pseudomonas moraviensis, Bacillus safensis, and Falsibacillus pallidus has been shown to increase wheat yield by up to 14.42%, raise labile soil P by >122%, and reduce stable P by 46.89% [76]. These microbes secrete organic acids and enzymes that solubilize nutrients and can form synergistic associations with plant roots, further improving P uptake [77].

Rhizosphere microbes also regulate micronutrient bioavailability. They enhance iron acquisition through siderophore production and facilitation of Fe³⁺ reduction, supporting biofortification strategies [78]. Siderophore-producing genera such as Rhizobium and Pseudomonas improve Fe and P availability under abiotic stress [24]. Similarly, zinc-solubilizing bacteria secrete metabolites that mobilize soil zinc, offering a sustainable biofortification pathway in Zn-deficient soils [79]. Copper and manganese uptake are also positively influenced: some bacteria modify copper oxidation states or activate Mn-detoxifying enzymes, increasing their plant-available forms [80].

Collectively, these microbial mechanisms—ranging from macro- and micronutrient solubilization to heavy-metal immobilization and stress mitigation—demonstrate the integral role of the rhizosphere microbiome in advancing nutrient-efficient, sustainable agriculture.

Rhizosphere microorganisms play a pivotal role in protecting plants against abiotic and biotic stresses through a suite of cellular and molecular mechanisms. This section synthesizes current knowledge on how microbes themselves survive extreme conditions and how they, in turn, enhance plant stress tolerance at the tissue and cellular levels, particularly in roots.

Stress-adapted rhizobacteria and fungi employ multiple cellular strategies to withstand adverse environments: Alteration of membrane lipid composition (e.g., increased unsaturated fatty acids) maintains membrane fluidity under temperature extremes and osmotic stress. Production of exopolysaccharides (EPS) forms biofilms that retain water, chelate toxins, and create stable microhabitats. This mechanism is directly linked to the 15–25% improvement in soil aggregate stability reported in meta-analyses [81]. Accumulation of compatible solutes (e.g., K⁺, glutamate, trehalose, glycine betaine) balances osmotic pressure and stabilizes proteins under drought or salinity. Enhanced expression of superoxide dismutase, catalase, and peroxidases enables microbes to scavenge reactive oxygen species generated under stress.

Stress-tolerant microbes confer resilience to plants through direct and indirect mechanisms: Microbial biofilms stabilize soil aggregates around roots, improving water availability, aeration, and root penetration—a tissue-level environmental buffer. ACC deaminase produced by PGPR cleaves the ethylene precursor 1-aminocyclopropane-1-carboxylate, reducing stress-induced ethylene accumulation in roots and preventing growth inhibition and senescence [82]. Simultaneously, microbial synthesis of auxins (IAA), cytokinins, and gibberellins promotes root elongation and branching. Stress-adapted phosphate-solubilizing bacteria and K-solubilizing bacteria continue to release organic acids and enzymes under low pH or moisture deficit, ensuring nutrient supply to root epidermal and cortical cells. Microbial elicitors (flagellin, lipopolysaccharides, peptidoglycans) are perceived by root pattern-recognition receptors, triggering mitogen-activated protein kinase cascades and upregulation of defense-related genes. This priming leads to faster and stronger activation of induced systemic resistance (ISR) upon subsequent pathogen attack [83].

Linking these cellular mechanisms to agronomic performance, field trials demonstrate that microbial inoculants increase drought and salinity tolerance in tomato and rice by 50%, and nano-encapsulation improves survival from 14% to 68% under drought stress [29,84]. However, the establishment of introduced strains is often limited by colonization resistance—a phenomenon whereby resident soil organic carbon chemistry modulates plant immune status and the native microbiome, creating a barrier to exotic inoculants [85]. Future research must dissect the molecular dialogue between inoculants and resident communities to design synthetic consortia capable of overcoming this resistance.

Rhizosphere microorganisms function as effective biofertilizers and play a crucial role in advancing sustainable agriculture (Fig. 5). Growing emphasis on environmental protection and sustainable farming has heightened interest in microbial fertilizers. The technology for their production continues to evolve. Traditional methods, which depend on cultivating selected strains and optimizing culture media, are limited by high costs and potential risks such as pest-transmitted microorganisms. To overcome these challenges, novel preparation approaches are being explored. Advances in genetic engineering have enabled the development of hyper-producing microbial strains that enhance biosurfactant synthesis and activity while lowering production costs [86]. Solid-state fermentation has emerged as a promising biofertilizer production method, reducing water use and substantially improving microbial survival rates [87]. In China, solid-state fermentation technologies have cut production costs by 40% [88]. Policy incentives, such as subsidies for biofertilizer adoption, are vital for encouraging farmer uptake in developing regions.

The efficacy and practical application of microbial fertilizers are receiving considerable research attention. Monitoring phosphate-solubilizing bacteria in the rhizosphere helps optimize microbial fertilizer formulations and promote crop growth by improving phosphorus availability [89]. On newly cultivated land, amendments that include microbial fertilizers significantly enhance soil physicochemical properties and reshape microbial community structure [55], leading to higher maize yield and quality, improved nutrient use efficiency, and more sustainable farming practices. These fertilizers also strengthen crop resilience against pests and salt stress, underscoring their agricultural potential.

The use of rhizosphere microorganisms represents a key advance in microbial fertilizer technology. A comprehensive strategy—encompassing careful strain selection, development of microbial consortia, and rigorous field validation—is essential to improve the consistency, effectiveness, and practical deployment of soil inoculants [90]. Combining traditional isolation with molecular and ecological techniques allows efficient screening of superior strains. Employing indigenous microbial consortia together with genetically engineered inoculants offers a promising rhizosphere-engineering strategy [91], one that boosts crop yields while fostering environmental sustainability through improved plant–microbiome interactions and long-term soil health.

Applying microbial fertilizers at optimal times, rates, and methods—tailored to crop growth stages and soil conditions—maximizes their impact. Precise dosing that matches crop nutrient demand, existing soil nutrient status, and inoculant concentration is critical for enhancing nutrient uptake, minimizing environmental leakage, and improving nitrogen-use efficiency [92]. For example, foliar application of nano-iron particles (FeNPs) increased broad-bean plant height by 35.01%, fresh weight by 47%, and pod number by 47.9% compared to untreated controls, demonstrating a sustainable solution for iron deficiency in sandy arid soils [93]. Similarly, integrating native PGPR strains (BA-3, BA-6, BA-7) with diammonium phosphate (DAP) and farmyard manure (FYM) improved wheat growth, achieving a 1000-grain weight of 55.1 g, a biological yield of 8209 kg ha⁻¹, and an economic yield of 4572 kg ha⁻¹, along with elevated soil total nitrogen (1.68 μg mL⁻¹), phosphorus (0.38%), and potassium (1.33%) [94].

Microbial fertilizers—a major practical application of rhizosphere microorganisms—have been widely studied and implemented in agriculture. Organic amendments enriched with microbial inoculants not only increase soil microbial diversity and function but also drive crop yields, highlighting the central role of microbial diversity in sustainable agriculture [95]. Integrating reduced chemical fertilizers with bio-organic fertilizers improves soil health and microbial diversity while boosting crop yield and quality [96].

A key advantage of microbial fertilizers is their ability to enhance soil fertility. Beneficial microorganisms, particularly Bacillus species, can improve soil health, stimulate plant growth, and reduce dependence on synthetic fertilizers and pesticides [97]. Microbial biocontrol agents, especially plant growth-promoting rhizobacteria and fungi, offer considerable potential for sustainable farming by raising crop yield and quality while diminishing reliance on chemical pesticides [98]. Beyond promoting plant growth, microbial fertilizers improve soil structure, increase nutrient availability, and strengthen erosion resistance [99]. Nevertheless, quality control remains a significant challenge. Optimizing cultivation and preservation techniques is essential to ensure consistent product quality, enhance microbial diversity, and increase crop productivity—all critical for sustainable agriculture [100].

Rhizosphere microorganisms function as versatile biocontrol agents in agriculture, offering sustainable alternatives to conventional chemical inputs. One promising approach involves the use of metal-based nanoparticles, which exhibit strong antimicrobial properties and can suppress pathogens directly or indirectly by priming plant immune responses [101]. Another key mechanism is the production of antibiotics by rhizobacteria. Optimizing synergistic combinations of PGPR represents a strategic avenue for enhancing disease management, though it requires further research into strain selection, synergy quantification, and field adaptation [102] (Table 2).

Competitive exclusion occurs when beneficial microbes outcompete pathogens for limited resources such as nutrients and space. Manipulating the rhizosphere microbiome—through approaches such as creating biased rhizospheres—can enhance crop productivity and reduce disease incidence by favoring beneficial plant-microbe interactions [54]. Induced systemic resistance (ISR) is another important mode of action: rhizosphere microorganisms stimulate the plant’s immune system, leading to the production of defense-related compounds and broad-spectrum pathogen resistance, thereby improving plant health and yield [111]. Additionally, rhizobacteria enhance plant tolerance to abiotic stresses by modulating root architecture, hormone signaling, and nutrient uptake efficiency [112].

Beyond disease suppression, rhizosphere microorganisms play crucial roles in nutrient cycling and availability. Biological nitrogen fixation (BNF), which accounts for over 60% of naturally fixed nitrogen globally, is vital for sustainable agriculture [113]. Enhancing BNF efficiency can significantly reduce dependence on synthetic fertilizers, support crop nitrogen demand, and mitigate environmental impacts. Certain strains also demonstrate direct biocontrol potential; for example, Burkholderia vietnamiensis B418 achieves up to 71.15% control of root-knot nematodes in watermelon while increasing fungal diversity and nifH gene abundance, illustrating its utility in sustainable nematode management through rhizosphere modulation [114] (Table 3).

Rhizosphere microorganisms further contribute to plant growth and stress resilience by producing phytohormones and volatile organic compounds that regulate root development and systemic signaling [64]. Understanding the functional diversity of soil archaea and fungi, along with their ecological interactions, is essential for harnessing their potential in sustainable agroecosystems [126]. However, the denitrification potential of some nitrogen-fixing bacteria must be considered to fully assess their environmental net benefit [127].

These microorganisms, which include bacteria, fungi, and protozoa, coexist with plant roots in the root zone, significantly promoting plant growth and enhancing soil quality. Beneficial bacteria such as Bacillus, Pseudomonas, and Rhizobium, together with fungal communities, enhance nutrient availability, decompose organic residues, and improve soil structure, thereby supporting resilient agricultural systems [128]. Root exudates mediate these interactions and can be strategically managed to suppress soil-borne pathogens and enhance plant immunity under changing climatic conditions [129]. Amendments such as biochar can further strengthen soil disease suppression by fostering beneficial microbes that produce antibiotics and induce plant defense responses [130].

Integrated management practices—including microbial fertilizers and crop diversification—improve soil health, increase crop yield and quality, and reduce negative impacts from excessive chemical inputs [131]. For instance, applying microbial fertilizer (0.24 kg m⁻²) in saline-alkali soil raised organic carbon, available phosphorus, and potassium by 21.50%, 26.14%, and 36.30%, respectively, while reducing pH and electrical conductivity, ultimately increasing sweet sorghum yield by 24.19% [132]. Similarly, amending ginger field soil with tomato compost and Bacillus subtilis increased soil organic matter by 17.34% and boosted activities of key enzymes (urease, phosphatase, sucrase) by 55.89%, 35.59%, and 57.21% [133].

Microbial inoculants and tailored fertilization further enhance agricultural sustainability. Optimized NPK fertilization (600, 120, and 80 mg plant⁻¹, respectively) in chrysanthemum cultivation improved plant growth metrics by 10.6–40.4% and enriched beneficial bacteria such as Proteobacteria, thereby enhancing nutrient cycling and use efficiency [134]. Conversely, soil acidification (pH decline from 7.6 to 5.1) can shift nitrogen competition from microbes to plants, though the overall nitrogen acquired may remain nutritionally insufficient [135]. Prebiotic metabolites offer another avenue by selectively stimulating beneficial rhizosphere colonizers, which in turn suppress pathogens and improve plant health [136]. Strains such as Serratia surfactantfaciens and Bacillus amyloliquefaciens have demonstrated effective biocontrol via hydrolytic enzyme and antibiotic production [137]. Additionally, cyanobacteria provide sustainable alternatives by improving nutrient use, alleviating abiotic stress, and supporting phytoremediation [138].

Collectively, rhizosphere microorganisms—through nitrogen fixation (Fig. 6), phosphate solubilization, hormone production, and pathogen suppression—enhance nutrient-use efficiency by 20–30%, reduce reliance on chemical fertilizers, and contribute to the development of productive and sustainable agricultural systems [139].

Soil type—categorized primarily into sandy, loamy, and clayey textures—fundamentally shapes the physicochemical habitat of rhizosphere microorganisms. Sandy soils, with large particle size and high porosity, provide favorable aeration but exhibit poor water and nutrient retention. In contrast, loamy soils offer a balanced structure with medium-sized particles, rich organic matter content, and optimal water-holding capacity, supporting diverse microbial life. Clayey soils are characterized by fine, cohesive particles that retain moisture effectively but limit gas exchange, influencing microbial activity accordingly.

Soil texture directly modulates microbial diversity and community assembly. For instance, a loam content of 20% was associated with a 10% reduction in prokaryotic operational taxonomic unit richness and a 15% decrease in protist Shannon diversity [140]. Increasing loam proportion to 60% enhanced rhizosphere selectivity, raising the abundance of specific prokaryotic taxa by 0.45%. Sandy soils, under aerated drip irrigation (ADI), showed increased relative abundance of Firmicutes and Gemmatimonadetes (up to 3%) but reduced Proteobacteria and Actinobacteria, while fungal phylum Mortierellomycota increased by up to 25% [141]. These shifts illustrate how irrigation management can optimize microbial communities for improved nutrient cycling in carbon- and phosphorus-enriched soils.

Prolonged drought strongly inhibits enzyme activities and reduces bacterial diversity in sandy soils, whereas loamy soils demonstrate greater resilience, enabling rapid recovery of nitrification and microbial function after rewetting [142]. Soil organic management further enhances microbial biomass [68]; in organic cropping systems, total phospholipid fatty acid (PLFA) reached 43.9 nmol g⁻¹, exceeding levels in conventional (32.8 nmol g⁻¹) and low-input (31.4 nmol g⁻¹) systems [143]. Fungal activity is particularly promoted in microaggregates, where PLFA-C concentration (9.2%) exceeds that in silt-and-clay fractions (6.5%), highlighting microhabitat effects on microbial carbon processing.

Soil texture also governs the distribution of functional microbial groups. In maize rhizospheres, acdS-carrying Actinobacteria were more abundant in sandy soils (46–92%) compared to loam (28–65%), whereas acdS-carrying Proteobacteria dominated in loam (34–72%) over sand (8.6–53.9%) [144]. Such taxon-specific responses underscore the need to consider soil physical properties when designing rhizosphere engineering strategies aimed at enhancing plant stress resilience and nutrient acquisition.

Salinity represents another critical environmental filter. Variations in soil salinity (0.36–6.72 dS m⁻¹) correlate with declines in key soil nutrients and enzymatic activities, including organic carbon, available nitrogen, phosphorus, potassium, and hydrolase functions [145]. Saline-alkaline conditions favor halotolerant taxa such as Proteobacteria and Actinobacteria, while increasing cadmium availability by 34.1–49.7% [146]. Keystone genera like Blastococcus and Gemmatimonas—though comprising <1% of total communities—play vital roles in community adaptation and heavy metal mitigation.

Soil pH further influences microbial dynamics by altering nutrient solubility and ion toxicity. Acidic conditions increase aluminum and manganese availability, inhibiting microbial growth [147]. Nitrogen-induced acidification reduces topsoil fungal diversity by up to 14.7% [148], whereas amendments like acidified biochar can enhance crop growth and promote beneficial bacteria (e.g., Streptococcus, Mycothermus) in saline-alkaline soils. Moderate salinity (~1.5%) may stimulate nitrogen removal by enriching taxa such as Flavobacterium and Paracoccus, but higher salinity disrupts microbial synergy and metabolic function.

Microorganisms actively modify their soil environment through biochemical processes and feedback mechanisms, influencing structure, hydrology, and nutrient availability [149]. Amendments like magnesium-montmorillonite and metal oxide-modified biochars can immobilize heavy metals and reduce phosphorus leaching, with efficacy depending on local soil and microbial community characteristics [150].

In summary, soil texture, salinity, pH, and organic matter interact to shape rhizosphere microbial composition and function. Understanding these relationships is essential for developing tailored management practices that enhance microbial-mediated nutrient cycling, stress tolerance, and overall agroecosystem sustainability.

Different farming practices can significantly alter soil structure and properties, thereby directly or indirectly affecting the quantity and activity of rhizosphere microorganisms (Fig. 7). Modified tillage techniques that incorporate straw at different depths improve soil structure, increase soil organic carbon by up to 11.4%, and enhance subsoil porosity and aggregate stability [151]. Organic amendments not only ameliorate soil structure and carbon dynamics in saline soils but also selectively promote halotolerant microbial species, resulting in a more oxygenated rhizosphere that supports microbial adaptation, nutrient cycling, and potentially higher crop productivity [152]. In contrast, no-tillage (NT) practices preserve soil aggregate integrity, leading to a significant increase in aggregates larger than 1 mm (P < 0.001) and greater bacterial alpha diversity—measured by Shannon and ACE indices—compared to conventional tillage [153]. These findings highlight the capacity of NT to foster beneficial soil microbial communities and enhance soil productivity.

Organic and conventional farming systems differ substantially in their impact on soil ecosystems. Organic farming reduces reliance on chemical pesticides while promoting soil biodiversity and microbial activity. This approach can increase soil organic matter by up to 28% and reduce nitrogen leaching by as much as 50% [154]. The application of organic manure enriches bacterial and fungal communities, particularly Gram-negative bacteria and fungi, while decreasing actinomycetes in alluvial paddy soils, reflecting a shift in indigenous microbial structure [155]. Additionally, manufactured nano-objects (MNOs) present a promising strategy to enhance agricultural sustainability by precisely manipulating the soil microbiome through controlled delivery of active ingredients and regulation of microbial interactions [156].

Intercropping significantly improves soil macro-aggregates (>2 mm) by 15.5–58.6% across various sites and years [157]. This improvement is linked to shifts in microbial communities, including increases in Sordariales and arbuscular mycorrhizal fungi alongside a reduction in Nitrospirae. Long-term crop rotation (LTCR, 30 years) enhances soil quality, as indicated by increased water-stable aggregates (>2 mm), elevated soil organic matter, and microbial biomass carbon reaching 2493 μg g⁻¹. Compared to short-term rotation (STCR, 4 years), LTCR boosts microbial biomass by 58% and alters community composition, with increased abundances of Proteobacteria and Acidobacteria [158]. Enhanced plant holobiomes (EPHs)—formed through symbioses with Rhizobiaceae, arbuscular mycorrhizal fungi, Trichoderma, and Piriformospora indica—can raise crop yields by up to 50% by improving plant growth, nutrient uptake, and stress tolerance. EPHs also contribute to soil organic matter accumulation (up to 15%) and atmospheric CO₂ sequestration [159]. Moreover, intercropping enriches soil biodiversity by enhancing microbial network modularity and functional diversity, enriching nitrogen-cycling genes and microbial taxa, which in turn improves nutrient availability and sustains crop yields 17% higher than in monoculture systems [160].

The climate-water-energy-food (CWEF) nexus offers a holistic framework for evaluating the sustainability of irrigation with desalinated seawater, considering interconnected social, economic, and environmental factors [161]. Optimizing nitrogen application at 160 kg N ha⁻¹ maximizes maize yield (10.6 Mg ha⁻¹) and grain protein while reducing risks of acidification, eutrophication, global warming, and health impacts by 29%, 42%, 35%, and 32%, respectively [162]. Coordinated irrigation (337.3–354.9 mm) combined with nitrogen fertilization (181.2–198.6 kg ha⁻¹) optimizes spring wheat yield, economic returns, and resource efficiency while minimizing soil nitrogen residue [163]. Integrated rhizosphere management strategies, including rhizosphere engineering and plant modification, can mitigate drought stress by improving root architecture, nutrient uptake, and stress tolerance [164]. Precision fertigation reduces nitrogen and phosphorus inputs by 8–25% and potassium by up to 17% without significantly affecting maize growth or yield, thereby increasing nutrient use efficiency by up to 25% and raising net profits [165].

Wheat straw biochar application increases water-holding capacity by 12%, enhances leaf gas exchange by 15%, and improves biomass and potassium content by 18% and 25%, respectively [166]. Sandy soils in young oasis fields show 6.2 times greater deep drainage and 1.65 times higher nitrogen leaching compared to loamy soils in older fields, leading to a 23.9% reduction in crop yield and a 27.2% decrease in nitrogen use efficiency [167]. These results underscore the importance of soil structure management for improving water and nutrient retention. Additionally, waterlogging stress impairs cotton growth by reducing soil oxygen, thereby limiting biomass accumulation and triggering physiological, biochemical, and molecular stress responses [168]. Optimal nutrient management—applying 225 kg N ha⁻¹, 67.5 kg P₂O₅ ha⁻¹, and 225 kg K₂O ha⁻¹ at flowering—maximizes nutrient accumulation rates (up to 6.31, 1.44, and 6.24 kg ha⁻¹ d⁻¹ for N, P, and K, respectively) and recovery efficiency [169].

Introducing chickpeas, lentils, and safflower into rice-fallow systems, together with conservation tillage such as Zero Tillage Direct Seeded Rice with Residue Retention, increases winter crop yields by up to 190%, improves energy use efficiency by 11–20%, and reduces greenhouse gas emissions by 30% compared to conventional puddled transplanting [170]. Incorporating oilseed rape into rice rotations enhances soil microbial diversity by up to 49.7%, enriching key bacterial (e.g., Clostridium, Pedobacter) and fungal (e.g., Mortierella, Ascomycota) groups, while also improving soil fertility through increased total nitrogen (up to 49.7%), available phosphorus, and aggregate stability [171,172].

Rhizosphere microorganisms occupy specific metabolic niches, facilitated by biochemical pathways that support root colonization and pathogen suppression [173]. Intercropping peanut with maize and oilseed rape modifies rhizosphere metabolite profiles and stimulates the growth and nitrogen-fixing activity of free-living and symbiotic bacteria, thereby improving soil nitrogen availability [174]. Nitrogen fertilization markedly alters soil microbial dynamics, reducing bacterial diversity while increasing fungal diversity at a rate of 50 kg N ha⁻¹ year⁻¹, illustrating the intricate relationship among nutrient levels, plant diversity, and microbial functions in nutrient cycling and pathogen suppression [175]. Diversified crop rotations—including cereals, oilseeds, and legumes—reduce the severity of wheat leaf blotch by 20% and lower disease indices compared to monocultures, with particular benefits under no-tillage conditions [176]. Furthermore, maize–soybean intercropping enhances root exudation, increasing amino acid levels by 3.61-fold and boosting arbuscular mycorrhizal fungi colonization by 105.99–111.18%, alongside improvements in soil available nitrogen and phosphorus [177]. These results emphasize the pivotal role of root exudates in mediating plant–microbe interactions and sustaining the advantages of intercropping systems.

The rhizosphere is a hotspot of biological activity where intricate interactions between plants and their associated microbiota critically influence plant growth, health, and ecosystem functioning. These biotic interactions encompass a spectrum of relationships—from mutualistic to competitive—that govern nutrient acquisition, stress resilience, and pathogen dynamics.

Chemical dialogue forms the basis of plant-microbe interactions. Root exudates, comprising sugars, amino acids, organic acids, and secondary metabolites, serve as signaling molecules and nutritional substrates that selectively attract beneficial microbial consortia. Conversely, plants under pathogen attack can recruit biocontrol microbes through altered exudate profiles, demonstrating active rhizosphere management by the host.

Within the rhizosphere, microbial communities engage in complex networks of competition and cooperation that shape community structure and function. Competitive exclusion for resources (e.g., carbon, iron, space) can suppress pathogenic populations; for example, siderophore-producing Pseudomonas outcompetes fungi for iron, reducing disease incidence by 60–80% [178]. Conversely, synergistic interactions enhance community resilience and functionality. Cross-feeding and metabolic cooperation among nitrogen fixers, phosphate solubilizers, and biocontrol agents can increase nutrient use efficiency and plant growth promotion by 20–40% [179]. Biofilm formation further exemplifies cooperation, where polymicrobial aggregates improve stress survival and root colonization through shared extracellular polymeric substances.

The rhizosphere extends beyond bacteria and fungi to include protozoa, nematodes, and microarthropods, forming a multi-trophic food web that regulates microbial turnover and nutrient cycling. Bacterivorous protozoa and nematodes graze on microbial biomass, releasing immobilized nutrients in plant-available forms—a process termed the “microbial loop.” Mycorrhizal fungi also interact with helper bacteria, facilitating hyphal growth and nutrient exchange, thereby creating a tightly linked microbial network that supports plant health.

A major ecological constraint on inoculant success is colonization resistance. Recent work demonstrates that the molecular composition of soil organic carbon modulates plant immune status and the resident microbial community, creating a biochemical barrier that limits establishment of introduced strains [68]. These interconnected biotic relationships translate into measurable agroecological outcomes. Diverse microbial networks enhance soil suppressiveness against pathogens, improve aggregate stability via fungal hyphae and bacterial polysaccharides, and buffer plants against abiotic stress through induced systemic resistance. Understanding and harnessing these interactions—through tailored inoculants, diversified cropping, or microbiome engineering—offers a pathway to more robust and sustainable agricultural systems.

This review synthesizes three decades of research to elucidate how rhizosphere microorganisms enhance sustainable agriculture through nutrient cycling, disease suppression, and stress tolerance. Key advancements include CRISPR-engineered nitrogen fixers, nano-encapsulated inoculants, and synthetic microbial consortia that boost yields by 12–40% while reducing chemical inputs by 30–50%. However, field efficacy remains limited by soil heterogeneity, inoculant survival, and regulatory gaps. Future research must prioritize (1) scalable microbial formulations tailored to soil types, (2) integrated omics and field validation, and (3) policy frameworks incentivizing biofertilizer adoption. By bridging lab-to-field gaps, rhizosphere engineering can align with UN Sustainable Development Goals, ensuring food security while restoring soil health.