Review and Progress
Integrated Pest Management Strategies Incorporating Bacillus spp. for Control of Meloidogyne enterolobii ![](https://microbescipublisher.com/templates/images/OA.gif)
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Bt Research, 2024, Vol. 15, No. 3
Received: 08 Mar., 2024 Accepted: 19 Apr., 2024 Published: 06 May, 2024
The emergence of Meloidogyne enterolobii as a significant agricultural pest has necessitated the development of novel and sustainable pest management strategies. This study explores the potential of incorporating Bacillus spp. as a biological control agent within an Integrated Pest Management (IPM) framework for the control of M. enterolobii. Building on previous research that demonstrated the efficacy of Bacillus spp. against Meloidogyne spp., this review evaluates the specific mechanisms through which Bacillus spp. can manage M. enterolobii populations in agricultural settings. The research utilizes a combination of in planta assays, split root assays, RT-qPCR, and qPCR to assess the direct antagonistic capabilities of Bacillus spp. against M. enterolobii and their systemic effects on host plants. Results indicate that certain Bacillus strains, such as B. amyloliquefaciens QST713 and B. firmus I-1582, can effectively colonize plant roots and induce systemic resistance through the jasmonic acid (JA) and salicylic acid (SA) pathways, thereby reducing nematode population density and enhancing plant defense mechanisms. Additionally, the study compares the performance of Bacillus spp. with chemical nematicides, highlighting the potential for these bacteria to not only suppress nematode populations but also promote plant growth and yield, as evidenced in tomato plants. The findings suggest that Bacillus spp. could be a viable component of IPM strategies, offering a sustainable alternative to chemical nematicides for the management of M. enterolobii in agricultural systems.
Meloidogyne enterolobii, commonly known as the guava root-knot nematode, is a highly virulent pest that poses a significant threat to global agriculture. Since its initial description in 1983, M. enterolobii has been recognized for its ability to infect a wide range of economically important crops, leading to substantial yield losses and jeopardizing food security, especially in regions like sub-Saharan Africa (Collett et al., 2021). The nematode's resilience and adaptability make it a formidable adversary for farmers and researchers alike, necessitating the development of effective and sustainable management strategies.
The urgency to find sustainable pest management solutions is driven by the growing awareness of the environmental and health risks associated with conventional chemical nematicides. These concerns have catalyzed the search for eco-friendly alternatives that can be integrated into pest management programs with minimal ecological impact. Biological control agents, particularly those belonging to the genus Bacillus, have emerged as promising candidates in this regard (Yin et al., 2021).
Bacillus spp. are well-known for their biocontrol properties, including the ability to form protective biofilms, produce antimicrobial compounds, and induce systemic resistance in plants. For instance, Bacillus cereus strain Bc-cm103 has demonstrated remarkable efficacy against Meloidogyne incognita, a close relative of M. enterolobii, by causing high mortality rates in nematode juveniles and reducing egg hatching. Moreover, this strain has been shown to activate defense-responsive genes in host plants, providing an additional layer of protection against nematode infection (Yin et al., 2021). These findings underscore the potential of Bacillus spp. as biocontrol agents and pave the way for their application in integrated pest management (IPM) strategies against M. enterolobii.
This review paper aims to explore the integration of Bacillus spp. into IPM strategies for the control of M. enterolobii. By examining the current state of research, we will assess the viability of these biological control agents and discuss their potential role in sustainable agriculture. The need for innovative and environmentally conscious approaches to pest management has never been greater, and Bacillus spp. may hold the key to safeguarding crop production against the pervasive threat of M. enterolobii.
1 Bacillus spp. as Biocontrol Agents
1.1 General characteristics of Bacillus spp. that contribute to their biocontrol potential
Bacillus species are well-recognized for their biocontrol potential, primarily due to their ability to produce a wide array of antimicrobial compounds. These compounds are effective against various plant pathogens, including fungi, bacteria, and nematodes. The biocontrol efficacy of Bacillus spp. is also attributed to their capacity to form endospores, which are highly resistant to environmental stresses, allowing them to survive in adverse conditions. This resilience facilitates their persistence in the soil and rhizosphere, providing long-term protection for plants against pathogens. Additionally, Bacillus spp. can promote plant growth by producing phytohormones and facilitating nutrient uptake, which indirectly enhances plant defense mechanisms against pests and diseases.
1.2 Historical perspective on the use of Bacillus spp. in biocontrol
The use of Bacillus spp. as biocontrol agents has a rich history, with early reports dating back to the 20th century. Initially, the focus was on Bacillus thuringiensis due to its insecticidal properties, but over time, other Bacillus species have been explored for their nematicidal capabilities. For instance, Bacillus cereus has been identified as a potent biocontrol agent against root-knot nematodes, such as Meloidogyne incognita. Studies have shown that certain strains of B. cereus can cause significant mortality of nematode juveniles and reduce egg hatching rates, as well as form biofilms on plant roots, which protect the plants from nematode infection (Yin et al., 2021). The historical progression in the use of Bacillus spp. reflects a growing interest in sustainable and environmentally friendly pest management strategies, which are crucial in the face of increasing resistance to chemical nematicides and the need to preserve soil health.
2 Mechanisms of Action of Bacillus spp. against Meloidogyne spp.
2.1 Overview of the direct antagonistic capabilities of Bacillus spp.
Bacillus spp. have demonstrated significant direct antagonistic capabilities against Meloidogyne spp., particularly Meloidogyne incognita. Studies have shown that certain strains of Bacillus, such as B. firmus I-1582, can directly manage nematode populations by increasing mortality rates of second-stage juveniles (J2s) to above 75% (Gattoni et al., 2023). Similarly, B. cereus strain S2 has been found to cause high mortality rates in M. incognita, with the production of nematicidal compounds like sphingosine contributing to this effect (Gao et al., 2016). Another strain, B. cereus Bc-cm103, has been reported to cause 100% mortality of J2s within 12 hours and to decrease egg hatching rates (Yin et al., 2021). These findings indicate that Bacillus spp. can directly antagonize Meloidogyne spp. through the production of bioactive metabolites and other mechanisms.
2.2 Systemic resistance induced by Bacillus spp. and its role in plant defense
Bacillus spp. are not only capable of direct antagonism but also play a crucial role in inducing systemic resistance within host plants. B. amyloliquefaciens QST713 and B. firmus I-1582 have been shown to stimulate systemic resistance in plants, leading to the upregulation of defense-related genes (Gattoni et al., 2023). B. cereus S2 has also been reported to induce systemic resistance in tomato plants, enhancing the activity of defense-related enzymes (Gao et al., 2016). Furthermore, B. firmus I-1582 has been found to induce systemic resistance in tomato plants, with the dynamic regulation of genes related to the salicylic acid (SA) and jasmonic acid (JA) pathways (Ghahremani et al., 2020).
2.3 The role of salicylic acid and jasmonic acid pathways in systemic resistance
The salicylic acid (SA) and jasmonic acid (JA) pathways are critical components of plant defense mechanisms, and Bacillus spp. have been found to interact with these pathways to enhance systemic resistance against Meloidogyne spp. For instance, B. amyloliquefaciens QST713 and B. firmus I-1582 have been shown to upregulate genes involved in the initial stages of the JA synthesis pathway, suggesting the stimulation of an intermediate molecule, likely OPDA, rather than JA itself in the short-term systemic response (Gattoni et al., 2023). Additionally, these Bacillus spp. stimulated a SA-responsive defense-related gene after one week, indicating the involvement of SA in long-term systemic defense (Gattoni et al., 2023). B. firmus I-1582 also primed SA and JA-related genes in tomato plants at different times after nematode inoculation (Ghahremani et al., 2020). These interactions with the SA and JA pathways underscore the complex role of Bacillus spp. in plant defense against nematode infections.
Obviously, Bacillus spp. exhibit a multifaceted approach to managing Meloidogyne spp. through direct antagonism and the induction of systemic resistance, with the SA and JA pathways playing a significant role in the latter. These mechanisms highlight the potential of Bacillus spp. as biocontrol agents in integrated pest management strategies against root-knot nematodes.
3 Efficacy of Bacillus spp. in Controlling Meloidogyne spp. in Agricultural Settings
3.1 Case study 1: control of Meloidogyne incognita in cotton using Bacillus spp.
Meloidogyne incognita represents a significant threat to cotton production, particularly in the south-eastern United States, where it is considered the most economically damaging pathogen. The nematode's wide host range, extensive geographical distribution, and the severe damage symptoms it causes, coupled with its complex biology and life cycle, make it a formidable pest to manage (Davis and Kemerait, 2021).
Recent advances in integrated pest management (IPM) have highlighted the potential of Bacillus spp. as biological control agents against M. incognita. Studies evaluating the efficacy of Bacillus spp. reveal that certain strains, such as B. amyloliquefaciens QST713 and B. firmus I-1582, can manage nematode populations effectively. These strains have been shown to exhibit both direct antagonistic capabilities and systemic activity against M.incognita (Gattoni et al., 2023).
The direct antagonistic effect of B. firmus I-1582, for instance, has been demonstrated through in vitro assays, where extracted metabolites from the bacterium significantly increased the mortality rate of M. incognita's second-stage juveniles. This indicates a potential for these metabolites to be used in nematode management strategies (Gattoni et al., 2023).
Systemic resistance is another critical aspect of the biological control exerted by Bacillus spp. Split root assays have shown that both B. amyloliquefaciens QST713 and B. firmus I-1582 can induce systemic resistance in cotton plants, leading to a decrease in nematode population density. Interestingly, the systemic activity observed was associated with the upregulation of genes involved in the jasmonic acid (JA) synthesis pathway, suggesting that an intermediate molecule, likely OPDA, is stimulated by the bacteria rather than JA itself in the short-term response. Furthermore, after one week, a salicylic acid (SA)-responsive defense-related gene was upregulated, indicating that SA also plays a role in the long-term systemic defense response(Gattoni et al., 2023).
The ability of these Bacillus spp. to colonize cotton roots effectively and maintain their population over time is crucial for their success as biological control agents. Quantitative PCR (qPCR) assays have confirmed that B. amyloliquefaciens QST713 and B. firmus I-1582 can successfully colonize cotton roots, with their concentration remaining stable over a 24-day period (Gattoni et al., 2023).
This case demonstrates that the integration of Bacillus spp. into IPM strategies offers a promising avenue for the control of M. incognita in cotton. The dual action of direct antagonism and induced systemic resistance provided by strains such as B. amyloliquefaciens QST713 and B. firmus I-1582 represents a sustainable and effective approach to managing this pervasive nematode pest (Davis and Kemerait, 2021; Gattoni et al., 2023).
3.2 Case study 2: biocontrol of Meloidogyne sp. on tomato plants by selected Bacillus spp.
Integrated Pest Management (IPM) strategies are crucial for sustainable agriculture, and the use of biocontrol agents, such as Bacillus spp., has gained attention for their potential to control plant-parasitic nematodes like Meloidogyne spp. This case focuses on the efficacy of selected Bacillus strains in suppressing Meloidogyne spp. on tomato plants.
Research has shown that individual Bacillus strains can significantly reduce the infestation of Meloidogyne incognita on tomato roots. Strains BMH and INV, closely related to Bacillus velezensis, were individually capable of reducing the number of galls and eggs by more than 90% (Cruz-Magalhães et al., 2021). However, when these strains were combined, the suppression of M. incognita and the promotion of tomato shoot weight were not as effective as when applied separately (Cruz-Magalhães et al., 2021). This suggests that while individual strains have strong biocontrol potential, their combination does not necessarily enhance their biocontrol activity.
Another study evaluated a dual-strain combination of B. paralicheniformis FMCH001 and B. subtilis FMCH002, which exhibited nematicidal properties in the pre-infection phase. This combination decreased egg hatching, juvenile survival, and attractiveness to the roots of tomato plants. Moreover, it impaired nematode establishment, gall formation, and giant cell development, indicating interference with the nematode's Morphogenetic mechanisms (Díaz-Manzano et al., 2023). The dual-strain combination also effectively reduced nematode reproduction, regardless of the application mode, and was effective against other plant-parasitic nematodes and in different crops (Díaz-Manzano et al., 2023).
Furthermore, other Bacillus spp. have been identified as effective biocontrol agents against Meloidogyne spp., enhancing the growth and yield of tomato plants. These strains not only reduced the number of galls, egg masses, and nematodes in the soil but also promoted plant growth and yield, offering an alternative to chemical nematicides (Habazar et al., 2021). Although chemical treatments were more effective in controlling nematode populations, Bacillus spp. provided the added benefit of promoting plant health (Habazar et al., 2021).
It can be seen from this case study that Bacillus spp. offer a promising alternative for the biocontrol of Meloidogyne spp. in tomato plants. While individual strains have shown significant biocontrol potential, the effectiveness of strain combinations may vary. The multifunctional nature of Bacillus spp., including their role as plant growth promoters, makes them an integral part of IPM strategies for sustainable agriculture (Cruz-Magalhães et al., 2021; Habazar et al., 2021; Díaz-Manzano et al., 2023).
4 Overview of Bacillus strains with Nematicidal Activity
The genus Bacillus has been recognized for its role in the biological control of plant-parasitic nematodes, particularly Meloidogyne incognita. Several Bacillus strains have been identified to possess nematicidal properties, offering a sustainable alternative to chemical nematicides.
Bacillus cereus strain S2 has been reported to exhibit high nematicidal activity against M. incognita, with mortality rates reaching up to 90.96% in laboratory conditions. The strain produces sphingosine, a compound that has been identified as lethal to nematodes, and has shown to induce systemic resistance in tomato plants (Gao et al., 2016).
Another strain, Bacillus firmus YBf-10, has demonstrated systemic nematicidal activity, reducing nematode damage in tomato plants and promoting plant growth. The biocontrol efficacy of this strain is attributed to its secondary metabolites (Xiong et al., 2015).
Bacillus cereus strain Bc-cm103 has been used as a biological control agent due to its production of volatile organic compounds (VOCs) that exhibit fumigation activity against M. incognita. The VOCs produced by Bc-cm103, including dimethyl disulfide, have shown high mortality rates in nematodes (Yin et al., 2020).
Bacillus amyloliquefaciens Y1 produces the dipeptide cyclo (d-Pro-l-Leu), which has been identified for the first time as having nematocidal activity. This strain significantly reduces the count of eggs and galls on tomato plant roots and enhances plant growth parameters (Jamal et al., 2017).
Two strains of Bacillus thuringiensis, LBIT-596 and LBIT-107, have been characterized for their nematicidal activity. These strains produce spore-crystal complexes that are lethal to nematodes and have shown to decrease the number of galls caused by M. incognita in tomato plants (Verduzco-Rosas et al., 2021).
Bacillus subtilis strain Bs-1, isolated from rhizospheric soil, has strong nematicidal effects, causing egg hatching inhibition and repellence of M. incognita. This strain has been effective in reducing root galls and promoting the growth of cucumber in both pot and field experiments (Cao et al., 2019).
The efficacy of Bacillus cereus strain Bc-cm103 against M. incognita has been confirmed in pot, split-root, and field tests, where it significantly reduced the appearance of root galls. The strain also activates defense-responsive genes in cucumber (Yin et al., 2021).
Bacillus aryabhattai MCCC 1K02966, a deep-sea bacterium, has shown nematicidal and fumigant activities against M. incognita. The VOC methyl thioacetate produced by this strain exhibits multiple nematicidal activities, including contact nematicidal, fumigant, and repellent activities (Chen et al., 2021).
Native Bacillus thuringiensis strains have been investigated for their potential against M. incognita. Certain strains have been found to inhibit juvenile emergence and exhibit biocontrol potential by suppressing nematode reproduction in tomato plants (Ramalakshmi et al., 2020).
Lastly, the purL gene of Bacillus subtilis has been associated with nematicidal activity. Strains OKB105 and 69 have been used to treat various nematodes, with high mortality rates observed, indicating the potential role of the purL gene in nematicidal activity (Xia et al., 2011).
In conclusion, Bacillus spp. offer a diverse arsenal of biological control agents against M. incognita, with various strains producing different nematicidal compounds and mechanisms. These findings support the integration of Bacillus-based biocontrol strategies into pest management programs for sustainable agriculture.
5 Challenges and Limitations
The integration of Bacillus spp. into pest management strategies, particularly for controlling the aggressive Meloidogyne enterolobii, presents a promising avenue. However, several challenges and limitations still need to be addressed to optimize their effectiveness and ensure sustainable use.
5.1 Limitations in the current understanding of Bacillus spp. mechanisms of action
While Bacillus spp. are known to exert nematicidal effects, the detailed mechanisms underlying these interactions remain inadequately characterized. Several strains, such as Bacillus thuringiensis and Bacillus subtilis, have demonstrated potential in secreting bioactive compounds that affect nematodes adversely. These compounds include enzymes, toxins, and various secondary metabolites which can disrupt the nematode's cuticle, affect its digestive system, or impede its neural functions. However, the specific pathways and the molecular targets of these bioactive substances in nematodes are not fully elucidated. This gap in knowledge hampers the ability to predict and enhance the effectiveness of Bacillus-based formulations against specific nematode pests like Meloidogyne enterolobii.
5.2 Challenges in the application and consistency of Bacillus spp. as biocontrol agents
The application of Bacillus-based biocontrol agents in the field faces several practical challenges. First, the environmental persistence and activity of Bacillus spores can be highly variable, influenced by soil type, moisture, temperature, and the presence of other microorganisms. These factors can lead to inconsistent results in field applications, where efficacy might not replicate the success seen in controlled, laboratory conditions. Moreover, the formulation of Bacillus products needs to ensure that the bacterial spores remain viable and capable of germination upon application. This requires sophisticated formulation technologies that can protect these spores from desiccation, UV degradation, and other environmental stresses.
5.3 The potential for resistance development in nematodes
Like any biological or chemical control agent, there is a potential for the target pests to develop resistance against Bacillus spp. Although cases of nematode resistance to microbial biocontrol agents are less documented compared to chemical nematicides, the risk cannot be ignored. The repeated use of a single strain or a specific bioactive compound could select for resistant nematode populations over time. This potential for resistance underscores the need for a diversified approach in integrated pest management strategies, incorporating multiple Bacillus strains or combining these biological agents with other control measures. This diversification could help in managing resistance development and prolonging the efficacy of biocontrol agents.
Undoubtedly,the integration of Bacillus spp. into the management of Meloidogyne enterolobii presents a viable, environmentally friendly alternative to traditional nematicides. However, overcoming the outlined challenges and limitations is crucial for achieving consistent and sustainable control. Continued research into the mechanisms of action, improved formulations, and comprehensive field studies are essential to harness the full potential of Bacillus spp. as effective biocontrol agents.
6 Future Directions
As the agricultural community continues to seek sustainable solutions for pest management, particularly for the resilient Meloidogyne enterolobii, the role of Bacillus spp. within Integrated Pest Management (IPM) strategies is poised for significant advancements. Addressing current research gaps and exploring innovative applications are key to enhancing the utility and effectiveness of Bacillus-based biocontrol.
6.1 Research gaps and future studies needed to optimize the use of Bacillus spp. in IPM
Current research into Bacillus spp. as biocontrol agents primarily focuses on their nematicidal effects, but comprehensive studies on their interactions with plant hosts and the broader ecosystem are needed. Future studies should aim to map the interaction networks between Bacillus spp., plants, and nematodes to understand the systemic effects of these biocontrols. Additionally, there is a need for long-term field trials to evaluate the consistency and longevity of Bacillus-based treatments under various agricultural conditions. These studies should also investigate the optimal application timings, dosages, and methods to maximize efficacy and cost-effectiveness.
6.2 The potential for genetic engineering of Bacillus spp. to enhance biocontrol efficacy
Advancements in genetic engineering offer promising avenues to enhance the biocontrol capabilities of Bacillus spp. By understanding the genetic basis of the bioactive compounds and mechanisms that these bacteria use to combat nematodes, researchers can potentially engineer strains with enhanced nematicidal properties or broader spectrum activity. Genetic modifications could also improve the environmental resilience and persistence of these microbes, ensuring they remain effective in the soil for longer periods. However, any genetically modified organism (GMO) approach must be rigorously tested for safety and environmental impact before deployment.
6.3 Integration of Bacillus spp. with other IPM strategies for holistic pest management
To achieve holistic and sustainable pest management, Bacillus spp. should be integrated with other IPM strategies. This includes combining biological control with cultural practices such as crop rotation, soil health enhancement, and resistant cultivars. The synergistic use of Bacillus spp. with physical controls like soil solarization and organic amendments can also improve overall pest management outcomes. Additionally, exploring the combined use of Bacillus with other biological agents, such as fungi or predatory nematodes, could provide multiple modes of action against pests, reducing the likelihood of resistance development.
7 Concluding Remarks
In the pursuit of sustainable agricultural practices, the potential of Bacillus spp. as biocontrol agents against the root-knot nematode Meloidogyne enterolobii has been highlighted through various studies. The research has consistently demonstrated the efficacy of different Bacillus strains in suppressing nematode populations and promoting plant growth. For instance, Bacillus velezensis strain YS-AT-DS1 has shown promising results in enhancing tomato growth and reducing infection rates of Meloidogyne incognita in plants (Hu et al., 2022). Similarly, Bacillus cereus strain Bc-cm103 has been effective in causing mortality of nematode juveniles and reducing egg hatching rates, alongside activating defense-responsive genes in plants (Yin et al., 2021). These findings are supported by other studies that have reported the biocontrol efficacy of Bacillus spp. against Meloidogyne spp., indicating their potential as a sustainable alternative to chemical nematicides (Seo et al., 2012; Habazar et al., 2021).
The importance of further research cannot be overstated, as it is essential to fully harness the capabilities of Bacillus spp. in sustainable agriculture. While the current body of work provides a solid foundation, there are still gaps in our understanding of the mechanisms through which Bacillus spp. exert their biocontrol effects. For example, the role of secondary metabolites and the specific pathways involved in inducing systemic resistance in plants need to be elucidated (Xiong et al., 2015; Shahid et al., 2021). Additionally, the interaction between Bacillus spp. and plant hosts in various environmental conditions warrants further investigation to optimize the application of these biocontrol agents in different agricultural settings.
In conclusion, Bacillus spp. represent a promising avenue for the development of integrated pest management strategies that are both effective and environmentally friendly. Continued research is crucial to refine the application of these biocontrol agents and to ensure that they can be integrated seamlessly into existing agricultural practices, thereby contributing to the sustainability and resilience of food production systems worldwide.
Conflict of Interest Disclosure
The authors affirm 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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