1 Introduction

Soil health is a critical component of sustainable agriculture, influencing crop productivity, environmental quality, and the resilience of agricultural systems. Healthy soils support plant growth by providing essential nutrients, water, and a habitat for a diverse range of organisms. However, modern agricultural practices, including the excessive use of chemical fertilizers and pesticides, have led to soil degradation, reduced fertility, and increased vulnerability to climate change (Mabrouk et al., 2018). Sustainable farming practices, such as crop rotation, organic amendments, and the use of biofertilizers, are essential to restore and maintain soil health (Abd-Alla et al., 2023).

Nitrogen is a vital nutrient for plant growth, playing a key role in the synthesis of proteins, nucleic acids, and chlorophyll. While atmospheric nitrogen (N₂) is abundant, it is not directly accessible to most plants. Biological nitrogen fixation (BNF) is a natural process where certain bacteria convert atmospheric nitrogen into ammonia, a form that plants can readily absorb and utilize (Lindström and Mousavi, 2019). This process is particularly important for legumes, which form symbiotic relationships with nitrogen-fixing bacteria, such as Rhizobium, to meet their nitrogen requirements (Dall’Agnol et al., 2013; Allito et al., 2020). By enhancing nitrogen availability, BNF supports plant growth, improves soil fertility, and reduces the need for synthetic nitrogen fertilizers (Santi et al., 2013).

The symbiotic relationship between Rhizobium bacteria and leguminous plants is a cornerstone of sustainable agriculture. Rhizobia infect the roots of legume plants, leading to the formation of root nodules where nitrogen fixation occurs (Thompson and Lamp, 2021). This symbiosis not only provides the host plant with a direct source of nitrogen but also enriches the soil with nitrogen, benefiting subsequent crops in rotation systems (Yang et al., 2021). Effective Rhizobium-legume symbiosis can significantly enhance crop yields, improve soil health, and reduce the environmental impact of agriculture by decreasing the reliance on chemical fertilizers (Yates et al., 2021b). Moreover, certain Rhizobium strains have been shown to tolerate abiotic stresses, such as extreme temperatures and soil acidity, making them valuable for improving crop resilience in challenging environments (Yates et al., 2021a).

This study aims to provide a comprehensive review of the role of Rhizobium in legume nitrogen fixation and its impact on soil health and sustainable agriculture. It will explore the mechanisms underlying Rhizobium-legume symbiosis, the benefits of this symbiotic relationship for soil fertility and crop productivity, and the potential of Rhizobium as a biofertilizer to reduce the need for synthetic nitrogen inputs. Additionally, the study will discuss the challenges and opportunities in optimizing Rhizobium-legume interactions to enhance agricultural sustainability and resilience in the face of climate change. By synthesizing current research findings, this study seeks to highlight the importance of Rhizobium in promoting soil health and sustainable agricultural practices.

2 The Rhizobium-Legume Symbiosis

2.1 Detailed mechanism of Rhizobium infection in legume roots

The infection process of Rhizobium in legume roots is a highly coordinated sequence of events that begins with the recognition of rhizobial Nod factors by the plant (Wang et al., 2018a). This recognition triggers a cascade of responses, including the growth of root hairs and the formation of infection threads through which the bacteria enter the root cells. (Chakraborty et al., 2022) The rhizobia then induce cell division in the root cortex, leading to the formation of nodule primordia (Figure 1) (Yang et al., 2021). The bacteria are eventually enclosed in intracellular compartments called symbiosomes, where they differentiate into bacteroids capable of nitrogen fixation.

The research of Yang et al. (2021) illustrates the stages of nodule organogenesis in Medicago truncatula, highlighting the role of various gene regulatory networks. The process begins with the priming of root cells, especially cortical cells, facilitated by the SHR–SCR module. Key transcriptional complexes activate cell divisions in response to symbiotic signals, leading to the initiation of nodule formation. This is followed by outgrowth, where extensive cell divisions result in the formation of the nodule primordium. Finally, the nodule matures, developing a vascular system and an infection zone, primarily derived from cortical cells. This organized process is crucial for effective symbiosis in legumes.

2.2 Formation and structure of root nodules

Root nodule formation is a complex process that involves several stages. Initially, rhizobia attach to the root hairs and produce Nod factors, which are recognized by the plant, leading to root hair curling and the formation of infection threads (Lindström et al., 2022). These threads guide the bacteria into the root cortex, where they induce cell division and form nodule primordia. The developing nodule then differentiates into a mature structure housing the nitrogen-fixing bacteroids within symbiosomes (Oldroyd et al., 2011). The nodule structure is specialized to facilitate efficient nitrogen fixation, with a well-organized vascular system to transport nutrients and fixed nitrogen between the plant and the bacteria (Andrews and Andrews, 2016).

2.3 Biochemical pathways involved in nitrogen fixation

The biochemical pathways involved in nitrogen fixation are intricate and tightly regulated. Within the symbiosomes, bacteroids convert atmospheric nitrogen (N₂) into ammonia (NH₃) using the nitrogenase enzyme complex (Lepetit and Brouquisse, 2023). This process is energy-intensive and requires a continuous supply of ATP and reducing power, which are provided by the plant in the form of dicarboxylates and other metabolites (Schulte et al., 2021). The plant also regulates oxygen levels within the nodule to maintain the microaerobic conditions necessary for nitrogenase activity. Key metabolic pathways, such as the carbonic anhydrase-phosphoenolpyruvate carboxylase-malate dehydrogenase (CA-PEPC-MDH) pathway, play crucial roles in maintaining the redox balance and facilitating the efficient exchange of nutrients between the plant and the bacteroids (Schwember et al., 2022).

3 Ecological and Agricultural Benefits

3.1 Enhancement of soil nitrogen levels and fertility

Rhizobium bacteria play a crucial role in enhancing soil nitrogen levels through the process of biological nitrogen fixation. This symbiotic relationship between Rhizobium and leguminous plants allows for the conversion of atmospheric nitrogen into a form that plants can utilize, significantly improving soil fertility. For instance, studies have shown that inoculation with effective Rhizobium strains can lead to substantial increases in nitrogen fixation and nutrient uptake in crops like Vicia faba, resulting in improved soil nitrogen balance (Allito et al., 2020). Additionally, the presence of Rhizobium in the rhizosphere can enhance the availability of other essential nutrients, such as phosphorus, further contributing to soil fertility (Mabrouk et al., 2018).

3.2 Reduction in the need for synthetic nitrogen fertilizers

The use of Rhizobium in legume cultivation can significantly reduce the dependency on synthetic nitrogen fertilizers. This is particularly important given the environmental and economic costs associated with the production and application of these fertilizers. By enhancing biological nitrogen fixation, Rhizobium bacteria provide a sustainable alternative to chemical fertilizers. Research indicates that effective management of Rhizobium-legume symbiosis can lead to reduced nitrogen fertilizer use, thereby lowering greenhouse gas emissions and energy consumption associated with fertilizer production (Abd-Alla et al., 2023). This not only benefits the environment but also reduces the input costs for farmers (Kebede, 2021).

3.3 Improvement of soil structure and microbial diversity

Rhizobium bacteria contribute to the improvement of soil structure and the enhancement of microbial diversity. The formation of root nodules and the subsequent nitrogen fixation process can lead to better soil aggregation and stability. For example, the plantation of native legumes like Albizzia julibrissin has been shown to improve soil aggregate formation and enhance the microbial community structure in saline soils (Liu et al., 2021). This improved soil structure facilitates better water retention and root penetration, which are essential for healthy plant growth. Moreover, the presence of Rhizobium and other beneficial microbes in the soil can create a more diverse and resilient microbial ecosystem, promoting overall soil health (AbdElgawad et al., 2020).

3.4 Contribution to sustainable agriculture and environmental health

The integration of Rhizobium-legume symbiosis into agricultural practices is a key component of sustainable agriculture. By reducing the need for synthetic fertilizers and improving soil health, Rhizobium bacteria help create more sustainable farming systems. This approach not only enhances crop yields but also mitigates the environmental impact of agriculture. For instance, the use of biofertilizers like Rhizobium can lead to lower greenhouse gas emissions and reduced soil degradation, contributing to long-term environmental health (Yates et al., 2021b). Furthermore, the adoption of Rhizobium-based practices supports the development of eco-friendly and cost-effective agricultural systems, aligning with global efforts to promote sustainable food production.

The role of Rhizobium in legume nitrogen fixation offers numerous ecological and agricultural benefits, including enhanced soil nitrogen levels, reduced reliance on synthetic fertilizers, improved soil structure, and contributions to sustainable agriculture. These benefits underscore the importance of leveraging Rhizobium-legume symbiosis to boost soil health and promote environmentally sustainable farming practices.

4 Diversity of Rhizobium Strains

4.1 Taxonomy and classification of Rhizobium species

Rhizobium species are taxonomically diverse and are classified within the alpha and beta subclasses of the Proteobacteria. For instance, Mimosa pudica, a tropical invasive weed, has been found to associate with beta-rhizobia, including species within the Burkholderia and Cupriavidus genera. In New Caledonia, the majority of rhizobial strains isolated from M. pudica belonged to Cupriavidus taiwanensis, with a few strains identified as Rhizobium mesoamericanum (Klonowska et al., 2012). This diversity highlights the broad taxonomic range of rhizobia and their ability to adapt to different legume hosts and environmental conditions.

4.2 Specific interactions between different legume species and Rhizobium strains

The interaction between specific legume species and Rhizobium strains can significantly influence nitrogen fixation and plant health (Jēkabsone et al., 2022). For example, in Vicia faba (faba bean), inoculation with specific Rhizobium strains such as NSFBR-12 and NSFBR-15 resulted in the highest nitrogen fixation and nutrient uptake, demonstrating the importance of selecting effective rhizobial strains for enhancing legume productivity (Allito et al., 2020). Additionally, Rhizobium leguminosarum bv. viciae strain 33504-Alex1 not only promoted growth in faba beans but also induced systemic resistance against Bean yellow mosaic virus, showcasing the multifaceted benefits of specific Rhizobium-legume interactions (Figure 2) (Abdelkhalek et al., 2022).

The research of Abdelkhalek et al. (2022) illustrates the levels of various oxidative stress markers (SOD, CAT, APX, and PPO) in faba bean plants under different treatments, including control, Bean yellow mosaic virus (BYMV) infection, Rhizobium soil treatment, and foliar spray treatment. The results indicate that plants treated with Rhizobium before BYMV inoculation (G3) show a significant increase in enzyme activities (SOD, APX, PPO) compared to other groups, suggesting enhanced antioxidant defense. In contrast, the control group (G1) generally exhibits lower levels of these enzymes, highlighting the stress-mitigating effect of the Rhizobium treatment.

4.3 Adaptations of Rhizobium to various environmental conditions

Rhizobium strains exhibit remarkable adaptations to diverse environmental conditions, which can influence their effectiveness in nitrogen fixation (Wang et al., 2018b). For instance, Cupriavidus taiwanensis strains isolated from heavy metal-rich soils in New Caledonia showed various tolerances to metals like Ni, Zn, and Cr, suggesting their adaptation to these specific environments. Moreover, the co-inoculation of Rhizobium with plant growth-promoting rhizobacteria (PGPR) such as Bacillus megaterium has been shown to enhance nodulation and growth of common beans in low phosphorus soils, indicating that Rhizobium can work synergistically with other soil microbes to improve plant health under nutrient-limited conditions (Korir et al., 2017; Jach et al., 2022).

These findings underscore the importance of understanding the diversity, specific interactions, and environmental adaptations of Rhizobium strains to optimize their use in sustainable agriculture and soil health improvement.

5 Factors Influencing Rhizobium Efficiency

5.1 Soil pH, temperature, and moisture

The efficiency of Rhizobium in nitrogen fixation is significantly influenced by soil pH, temperature, and moisture. Optimal soil pH is crucial as it affects the availability of nutrients and the survival of Rhizobium. Acidic or highly alkaline soils can hinder the growth and activity of these bacteria, thereby reducing nitrogen fixation efficiency (Allito et al., 2020). Temperature also plays a vital role; extreme temperatures can lead to protein denaturation and nucleic acid damage in Rhizobium, affecting their ability to fix nitrogen (Owaresat et al., 2023). Soil moisture is another critical factor, as both drought and waterlogging can adversely impact Rhizobium activity and symbiotic efficiency.

5.2 Presence of other soil microorganisms

The presence of other soil microorganisms can either enhance or inhibit the efficiency of Rhizobium. Beneficial microorganisms, such as mycorrhizal fungi, can improve nutrient uptake and create a more favorable environment for Rhizobium. However, competition with native rhizobia and other soil bacteria can reduce the effectiveness of introduced Rhizobium strains. Native strains often outcompete inoculant strains for nodule occupancy, which can lead to lower nitrogen fixation rates if the native strains are less efficient (Mendoza-Suárez et al., 2021). Understanding the interactions between Rhizobium and other soil microorganisms is essential for improving symbiotic efficiency.

5.3 Agricultural practices (e.g., crop rotation, use of cover crops)

Agricultural practices such as crop rotation and the use of cover crops can significantly influence Rhizobium efficiency (Goyal et al., 2021). Crop rotation, especially with legumes, can enhance soil nitrogen levels and improve the overall health of the soil microbiome, creating a more conducive environment for Rhizobium (Fustec et al., 2011). The use of cover crops can also benefit Rhizobium by preventing soil erosion, improving soil structure, and maintaining soil moisture levels. These practices help sustain a healthy population of Rhizobium and other beneficial microorganisms, thereby enhancing nitrogen fixation efficiency.

5.4 Genetic factors in both Rhizobium and legume hosts

Genetic factors in both Rhizobium and their legume hosts play a crucial role in determining the efficiency of nitrogen fixation. The genetic compatibility between specific Rhizobium strains and legume varieties can significantly impact the success of the symbiotic relationship (Pankievicz et al., 2019). Advances in genomics have identified several quantitative trait loci (QTL) and candidate genes associated with symbiotic efficiency in both Rhizobium and legumes (Dwivedi et al., 2015). Breeding programs that focus on improving these genetic traits in both partners can lead to the development of high-yielding, nitrogen-efficient legume cultivars. Additionally, genetic engineering and the use of stress-tolerant Rhizobium strains can further enhance nitrogen fixation under adverse environmental conditions.

6 Advances in Rhizobium Inoculant Technology

6.1 Development and application of commercial Rhizobium inoculants

The development and application of commercial Rhizobium inoculants have significantly advanced over the years, driven by the need to enhance nitrogen fixation and improve crop yields. For instance, the use of peat carrier-based inoculants has been shown to significantly enhance nodulation, nitrogen fixation, and nutrient uptake in Vicia faba L. (Allito et al., 2020). Similarly, the formulation of inoculants based on autochthonous strains, such as Rhizobium leguminosarum bv. phaseoli LCS0306, has demonstrated superior performance in nitrogen fixation and grain yield in common beans, especially when combined with carriers like perlite and biochar (Table 1) (Pastor-Bueis et al., 2019). These advancements underscore the importance of selecting effective rhizobial strains and appropriate carriers to maximize the benefits of inoculation.

6.2 Methods for enhancing inoculant efficiency and effectiveness

Several methods have been explored to enhance the efficiency and effectiveness of Rhizobium inoculants. One approach involves the combined inoculation with arbuscular mycorrhizal fungi (AMF) and rhizobia, which has been shown to significantly increase nodulation, nitrogen, and phosphorus accumulation in common beans (Tajini et al., 2012). Another method includes the use of Fe₃O₄ nanoparticles in conjunction with Rhizobium inoculation, which has been found to improve nodulation, nitrogen fixation, and overall plant growth in common beans (Souza-Torres et al., 2021). Additionally, the selection of native rhizobia isolates that are well-adapted to local conditions can lead to higher symbiotic efficiency and better crop yields, as demonstrated in climbing beans in Kenya.

6.3 Case studies of successful inoculant use in different agricultural systems

Several case studies highlight the successful use of Rhizobium inoculants in various agricultural systems. In Egypt, the inoculation of faba beans with effective Rhizobium strains significantly improved seed yield and nitrogen uptake under low fertility sandy soil conditions, outperforming inorganic nitrogen fertilizers (Youseif et al., 2017). In another study, the inoculation of common beans with a combination of AMF and Rhizobium tropici CIAT899 resulted in enhanced phosphorus use efficiency and improved plant growth parameters. Furthermore, the use of native rhizobia isolates in climbing beans in Eastern Kenya led to significant improvements in nodulation, growth, and seed yields, demonstrating the potential of these isolates to enhance nitrogen fixation and bean production (Koskey et al., 2017). These case studies illustrate the diverse applications and benefits of Rhizobium inoculants in different agricultural contexts.

7 Challenges and Limitations

7.1 Environmental and soil constraints affecting Rhizobium performance

The performance of Rhizobium in legume nitrogen fixation is significantly influenced by environmental and soil conditions. Low pH and infertile soils present a major challenge, as they can hinder the formation of effective symbioses between legumes and rhizobia. For instance, research has shown that the symbiotic relationship between legumes and Rhizobium leguminosarum biovar viciae can be unreliable in low pH, dry soils, which are common in regions experiencing climate variability (Yates et al., 2021b). Additionally, soil phosphorus levels and pH can affect nutrient uptake and nitrogen fixation efficiency, as observed in Vicia faba inoculated with specific Rhizobium strains (Allito et al., 2020). The presence of competitive but inefficient resident rhizobia in the soil can also reduce the effectiveness of inoculants, as seen in common bean cultivation (Pastor-Bueis et al., 2019).

7.2 Issues with inoculant formulation and application

The formulation and application of rhizobial inoculants face several challenges. One major issue is the survival and persistence of inoculant strains in the field. For example, the survival of Rhizobium strains in dry soil conditions is a significant concern, as dry sowing practices can reduce the effectiveness of inoculants (Yates et al., 2021a). Additionally, the competition between inoculant strains and native rhizobia for nodule occupancy can limit the success of inoculants. Native rhizobia often outcompete inoculant strains, leading to lower nodule occupancy and reduced nitrogen fixation (Mendoza-Suárez et al., 2021). The formulation of inoculants with appropriate carriers, such as peat or biochar, can enhance the survival and effectiveness of rhizobial strains, but this requires careful selection and testing (Souza-Torres et al., 2021).

7.3 Economic and practical barriers to widespread adoption

Economic and practical barriers also hinder the widespread adoption of rhizobial inoculants. The cost of developing and producing high-quality inoculants can be prohibitive, especially for small-scale farmers. Additionally, the application of inoculants requires specific knowledge and practices, which may not be readily available to all farmers. For instance, the need for precise application rates and methods, such as soil or foliar application, can complicate the use of inoculants (Abdelkhalek et al., 2022). Furthermore, the economic benefits of using rhizobial inoculants may not be immediately apparent, as the initial investment in inoculants and the required changes in farming practices can be substantial (Youseif et al., 2017). Despite these challenges, the potential for improved crop yields and reduced reliance on chemical fertilizers makes the adoption of rhizobial inoculants a promising strategy for sustainable agriculture (Yakubu et al., 2011; Castellano-Hinojosa et al., 2022).

8 Future Perspectives and Research Directions

8.1 Genetic engineering of Rhizobium for improved nitrogen fixation

Genetic engineering of Rhizobium strains holds significant promise for enhancing nitrogen fixation efficiency. By manipulating genes responsible for nodulation and nitrogenase activity, researchers can develop strains that perform better under various environmental conditions, including high nitrate concentrations which typically inhibit nodule formation and nitrogen fixation (Nguyen et al., 2019). Additionally, novel strains that exhibit superior nodulation and nitrogen fixation even under challenging conditions, such as low pH and high nitrate levels, have been identified, suggesting that genetic modifications could further optimize these traits (Yates et al., 2021a; 2021b).

8.2 Integration of Rhizobium inoculants with other soil health practices

Integrating Rhizobium inoculants with other soil health practices can amplify their benefits. For instance, co-inoculation with plant growth-promoting rhizobacteria (PGPR) has been shown to enhance nodulation, nitrogen fixation, and nutrient uptake in legumes grown in low phosphorus soils (Matse et al., 2020). Similarly, the combination of Rhizobium with Fe₃O₄ nanoparticles has demonstrated improved nodulation and nitrogen fixation in common beans, suggesting that such integrative approaches can significantly boost plant growth and soil health (Souza-Torres et al., 2021). Moreover, the use of Rhizobium in conjunction with arbuscular mycorrhizal fungi has been found to increase phosphorus use efficiency, further enhancing nitrogen fixation and overall plant health (Tajini et al., 2012).

8.3 Potential for using Rhizobium in non-legume crops

Exploring the potential of Rhizobium in non-legume crops could revolutionize agricultural practices by extending the benefits of biological nitrogen fixation beyond legumes. While traditionally associated with legumes, certain Rhizobium strains may have the potential to form symbiotic relationships with non-legume crops, thereby improving their nitrogen uptake and reducing the need for chemical fertilizers. This approach could be particularly beneficial in low-fertility soils where conventional nitrogen sources are less effective (Youseif et al., 2017).

8.4 Long-term sustainability and environmental impact assessments

Assessing the long-term sustainability and environmental impacts of using Rhizobium inoculants is crucial for their widespread adoption. Studies have shown that effective Rhizobium strains can significantly improve soil nitrogen balance and nutrient uptake, which can lead to reduced reliance on chemical fertilizers and enhanced soil health (Allito et al., 2020; Abdelkhalek et al., 2022). However, comprehensive environmental impact assessments are needed to evaluate the potential risks and benefits over extended periods. This includes monitoring the persistence and ecological interactions of introduced Rhizobium strains in various soil types and climatic conditions to ensure they do not disrupt native microbial communities or lead to unintended consequences.

9 Concluding Remarks

The role of Rhizobium in legume nitrogen fixation is pivotal for enhancing soil health and promoting sustainable agriculture. Various studies have demonstrated that specific Rhizobium strains significantly improve nodulation, nitrogen fixation, and nutrient uptake in leguminous plants, thereby enhancing soil nitrogen balance and overall soil fertility. The symbiotic relationship between Rhizobium and legumes not only reduces the need for synthetic nitrogen fertilizers but also mitigates environmental impacts such as greenhouse gas emissions and soil degradation. Additionally, Rhizobium strains have shown potential in improving plant growth under various abiotic stresses, making them valuable for modern agricultural practices.

Rhizobium bacteria play a critical role in promoting soil health by facilitating biological nitrogen fixation, which converts atmospheric nitrogen into a form that plants can utilize. This process is essential for the growth of leguminous plants and contributes to the enrichment of soil nutrients, particularly nitrogen and phosphorus. The symbiotic relationship between Rhizobium and legumes enhances soil fertility, reduces the dependency on chemical fertilizers, and supports sustainable agricultural practices. By improving nitrogen fixation efficiency and nutrient uptake, Rhizobium strains help maintain soil health and promote the growth of healthy crops, which is crucial for sustainable food production and environmental conservation.

Despite the significant advancements in understanding the Rhizobium-legume symbiosis, further research is needed to optimize the use of Rhizobium strains in agriculture. Future studies should focus on identifying and developing more efficient and resilient Rhizobium strains that can thrive under diverse environmental conditions and enhance nitrogen fixation and nutrient uptake. Additionally, research should explore the molecular mechanisms underlying the symbiotic relationship to improve the effectiveness of Rhizobium inoculants. There is also a need for field trials and practical applications to validate the benefits of Rhizobium-based solutions in different agricultural settings. By investing in research and development, we can harness the full potential of Rhizobium to promote sustainable agriculture and ensure food security.

Acknowledgments

Thanks to the two anonymous peer reviewers for their feedback on the manuscript.

Conflict of Interest Disclosure

The author affirms that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

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