Review Article

Microbial Predators as Biocontrol Agents: Potential and Challenges  

Liangwei Lü , Zhongqi Wu
Institute of Life Science, Jiyang College of Zhejiang A&F University, Zhuji, 311800, Zhejiang, China
Author    Correspondence author
Molecular Microbiology Research, 2024, Vol. 14, No. 5   
Received: 15 Jul., 2024    Accepted: 26 Aug., 2024    Published: 08 Sep., 2024
© 2024 BioPublisher Publishing Platform
This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract

This study explores the primary predation mechanisms of bacterial and fungal predators, including direct predation and secretion of lytic enzymes, and analyzes their interactions with host microbiomes. It also examines the role of microbial predators in integrated pest management, their potential applications in animal health, and the ecological impacts, resistance development, and other challenges faced in this field. Although microbial predators hold great promise in biological control, their promotion and application still face technical, regulatory, and commercialization barriers. With advancements in genetic engineering and high-throughput screening technologies, the development and application of microbial predators are moving toward greater precision and efficiency. This study expects to overcome current challenges through innovative technologies and strategies, facilitating the widespread application of microbial predators in biocontrol.

Keywords
Microbial predators; Biological control; Predation mechanisms; Integrated pest management; Genetic engineering

1 Introduction

Microbial predators, including bacteria, fungi, and viruses, are organisms that prey on other microorganisms. These predators are found in diverse environments such as soil, water, and plant surfaces. They play a crucial role in maintaining microbial balance and can be harnessed for their biocontrol potential against various pathogens. For instance, Myxococcus xanthus, a type of myxobacteria, has shown significant antagonistic activity against the plant pathogen Ralstonia solanacearum, which causes tomato bacterial wilt (Dong et al., 2022). Similarly, predatory bacteria like Bdellovibrio bacteriovorus are being explored for their ability to control foodborne and plant pathogens (Olanya and Lakshman, 2015; Herencias et al., 2020).

 

The use of microbial predators as biocontrol agents offers a sustainable and eco-friendly alternative to chemical pesticides. These predators can target specific pathogens without harming beneficial microorganisms or the environment. For example, the combination of soil-dwelling predators and microbial agents has been shown to effectively control the western flower thrips, a significant pest in agriculture (Saito and Brownbridge, 2016). Microbial consortia, which involve multiple strains of biocontrol agents, have been found to improve the efficacy of disease suppression in soil-borne plant diseases. The integration of microbial community studies into biocontrol research, facilitated by advancements in high-throughput sequencing technologies, is opening new avenues for innovative biocontrol methods (Massart et al., 2015; Niu et al., 2020).

 

This study will provide a comprehensive overview of the potential and challenges of using microbial predators as biological control agents. It summarizes the current state of research on microbial predators and their mechanisms of action in biological control, discusses the advantages and limitations of using microbial predators in agricultural and food safety applications, and highlights recent advancements and future trends in the development and application of microbial predators in biological control, ultimately promoting sustainable agricultural practices and food safety.

 

2 Types of Microbial Predators

2.1 Bacterial predators

Bacterial predators are a diverse group of microorganisms that prey on other bacteria, often through complex and specialized mechanisms. One prominent example is the deltaproteobacteria group, which includes Bdellovibrio and Bacteriovorax species. These Gram-negative bacteria are known for their ability to prey on other Gram-negative bacteria, making them potential biocontrol agents against foodborne and plant pathogens such as Escherichia coli, Salmonella spp., and Pseudomonas spp.. Bdellovibrio bacteriovorus, in particular, has been highlighted for its potential as a "living antibiotic" due to its ability to lyse pathogenic bacteria (McNeely et al., 2017; Herencias et al., 2020).

 

Another group of bacterial predators includes the myxobacteria, such as Myxococcus xanthus. These bacteria employ a generalist predatory mechanism involving the secretion of antibiotic metabolites and hydrolytic enzymes, which can lyse a wide range of prey organisms, including both Gram-negative and Gram-positive bacteria as well as fungi (Sydney et al., 2021). The facultative predatory Actinomycetota spp. also exhibit diverse predation strategies, including epibiotic and wolfpack attacks, which involve the production of secondary metabolites to lyse prey cells (Ibrahimi et al., 2023).

 

2.2 Fungal predators

Fungal predators, on the other hand, often employ different strategies to control their prey. For instance, certain soil-dwelling fungi, such as Mortierella species, form symbiotic relationships with toxin-producing bacteria that live within their hyphae. These bacterial endosymbionts produce anthelmintic metabolites that protect the fungi from nematode attacks, thereby enhancing their survival and efficacy as biocontrol agents (Figure 1) (Büttner et al., 2021).

 

 

Figure 1 Bacterial origin of cytotoxic benzolactones from M. verticillata cultures (Adopted from Büttner et al., 2021)

Image caption: (A) Cytotoxic lactone compounds assigned to endofungal symbionts from the fungus R. microsporus (1-4), M. verticillata (3-4), Pseudomonas sp. (5), and a tunicate and the bacterium Gynuella sunshinyii (6). (B) Metabolic profiles of extracts from Burkholderia sp. strain B8 and M. verticillata NRRL 6337 as symbiont or cured strain as total ion chromatograms in the negative mode. (C) Fluorescence micrograph depicting endosymbionts living in the fungal hyphae; staining with Calcofluor White and Syto9 Green. (D) Phylogenetic relationships of Mortierella symbionts, Burkholderia sp. strain B8, and other bacteria based on 16S rDNA. BRE, Burkholderia-related endosymbiont of Mortierella spp. (E) Metabolic profiles of extracts from M. verticillata NRRL 6337 and other necroxime-negative M. verticillata strains analyzed for endosymbionts in this study as total ion chromatograms in the negative mode. M, medium component. (F) Growth of symbiotic M. verticillata NRRL 6337 in comparison to the cured strain (Adopted from Büttner et al., 2021)

 

The study demonstrated through experiments that fungi without symbiotic bacteria were more vulnerable to attacks when co-cultured with nematodes, resulting in a significant increase in nematode numbers. In contrast, fungi with symbiotic bacteria were able to effectively reduce nematode populations. Further experiments showed that the defensive ability of the fungi could be restored by supplementing with nematode-repelling compounds, indicating that these compounds play a crucial role in the fungi’s defense against predators.

 

Another example of fungal predators includes entomopathogenic fungi like Metarhizium anisopliae and Beauveria bassiana. These fungi are known for their ability to infect and kill insect pests, and their combined use with soil-dwelling predators has shown improved efficacy in controlling pests such as the western flower thrips. Pseudomonas brassicacearum DF41, a biocontrol agent against fungal pathogens, can resist predation by nematodes through the production of toxic metabolites and biofilm formation, which blocks the nematode's feeding structures (Nandi et al., 2016).

 

3 Mechanisms of Predation

3.1 Direct predation mechanisms

3.1.1 Attachment and invasion

Microbial predators employ various strategies to attach to and invade their prey. Bdellovibrio bacteriovorus, for instance, attaches to the exterior of Gram-negative bacteria and invades the periplasmic space, where it replicates and eventually lyses the host cell. This attachment and invasion process is facilitated by specific enzymes, such as lytic transglycosylases, which cleave the prey's peptidoglycan, allowing the predator to enter and establish a niche within the prey cell (Banks et al., 2023).

 

3.1.2 Intracellular digestion

Once inside the prey, microbial predators digest the host's cellular contents to obtain nutrients. Bdellovibrio bacteriovorus, for example, digests the prey's cellular components within the periplasmic space, utilizing a variety of hydrolytic enzymes to break down complex molecules (Negus et al., 2017; Bratanis et al., 2020). Myxococcus xanthus also secretes hydrolytic enzymes, including peptidases, lipases, and glycoside hydrolases, to lyse prey cells and release nutrients into the extracellular environment.

 

3.1.3 Overcoming host defenses

Predatory bacteria have evolved mechanisms to overcome the defenses of their prey. For instance, Bdellovibrio bacteriovorus can evade the immune responses of its prey by expressing few surface epitopes, making it less recognizable to the host's immune system. Prey organisms like Pseudomonas aeruginosa have developed resistance strategies, such as effective metal/oxidative stress systems and mechanisms for detoxifying antimicrobial peptides, to protect themselves from predation (Sydney et al., 2021).

 

3.2 Secretion of lytic enzymes

The secretion of lytic enzymes is a common strategy among microbial predators to break down the cell walls of their prey. Bdellovibrio and like organisms (BALOs) secrete a range of enzymes, including lytic transglycosylases, which target the peptidoglycan layer of Gram-negative bacteria, facilitating invasion and digestion. Myxococcus xanthus also secretes a variety of lytic enzymes that degrade the cell walls of its prey, contributing to its broad prey range (Dong et al., 2022).

 

3.3 Interaction with host microbiome

Microbial predators can influence the structure and function of host-associated microbiomes. For example, Halobacteriovorax, a genus of predatory bacteria, is prevalent on the surface of reef-building corals and preys on potential coral pathogens, thereby potentially protecting the host by regulating the microbiome composition (Welsh et al., 2015). Similarly, the presence of predatory bacteria like Bdellovibrio bacteriovorus can transform the landscape and community assembly of biofilms, impacting the spatial ecology of microbial communities (Wucher et al., 2021; Tang, 2024).

 

4 Potential Applications in Agriculture

4.1 Control of soil-borne pathogens

Soil-borne pathogens pose a significant threat to crop yield and quality, leading to substantial economic losses in agriculture. The use of microbial predators as biocontrol agents offers a promising solution to manage these pathogens in an environmentally friendly manner. Beneficial microorganisms, such as certain bacterial and fungal species, can inhibit the growth of soil-borne pathogens through various mechanisms, including antibiosis, competition for nutrients, and enzymatic degradation (Niu et al., 2020; Tariq et al., 2020). For instance, the application of Trichoderma species has been shown to effectively suppress soil-borne fungal pathogens by producing a range of metabolites that inhibit pathogen growth. The use of multi-strain microbial consortia can enhance the efficacy of biocontrol by leveraging the synergistic interactions among different microbial species.

 

4.2 Biocontrol in crop rhizosphere

The rhizosphere, the narrow region of soil influenced by root secretions and associated microbial activity, is a critical zone for plant health. Microbial predators in the rhizosphere can play a vital role in promoting plant growth and protecting against pathogens. Rhizosphere bacteria, such as plant growth-promoting rhizobacteria (PGPR), can enhance plant growth by producing growth hormones, solubilizing phosphate, and fixing nitrogen (Saeed et al., 2021). These bacteria also exhibit biocontrol properties by producing antibiotics, siderophores, and hydrolytic enzymes that inhibit pathogenic microbes. For example, the amendment of soil with Metarhizium species has been shown to increase the abundance of beneficial microbes in the rhizosphere, thereby enhancing plant growth and disease resistance. The complex interactions between microbial predators, plant roots, and other soil microbes in the rhizosphere are crucial for the successful implementation of biocontrol strategies (Shahriar et al., 2022).

 

4.3 Use in integrated pest management

Integrated pest management (IPM) is a holistic approach that combines biological, cultural, physical, and chemical methods to control pests in an environmentally sustainable manner. Microbial predators can be an integral component of IPM by providing a natural means of pest suppression. For instance, soil predatory mites can be conserved and utilized to control plant-parasitic nematodes and arthropod pests, thereby reducing the reliance on chemical pesticides (Rueda-Ramírez et al., 2022). The use of biocontrol agents, such as Streptomyces spp., can also be integrated into IPM programs to manage fungal and bacterial phytopathogens while promoting plant growth (Vurukonda et al., 2018). The effectiveness of biocontrol agents in IPM can be enhanced through the manipulation of environmental conditions, formulation improvements, and the integration with other pest management strategies. By incorporating microbial predators into IPM, it is possible to achieve sustainable pest control and improve overall agricultural productivity.

 

5 Potential Applications in Aquaculture and Animal Health

5.1 Control of aquatic pathogens

Aquaculture, a rapidly growing sector, faces significant challenges due to the prevalence of aquatic microbial diseases, which can severely impact production performance. Traditional methods, such as the use of antibiotics, have led to the emergence of antibiotic-resistant bacteria, necessitating alternative approaches for disease control (Cabello et al., 2016).

One promising strategy involves the use of probiotics, which are live microorganisms that confer health benefits to the host. Probiotics have been shown to improve the growth, survival, and health status of aquatic livestock by protecting them from pathogens and enhancing their immune responses (Figure 2) (Tan et al., 2016; Hossain et al., 2017). For instance, the genus Streptomyces has been identified as a potential probiotic candidate in aquaculture, capable of protecting fish and shrimp from pathogens and promoting their growth.

 

 

Figure 2 Illustration of the use and impact of probiotics in aquaculture systems (Adopted from Srirengaraj et al., 2023)

 

Microalgal biotechnology also offers potential solutions for disease control in aquaculture. Microalgae can serve as nutritional supplements due to their high content of proteins, lipids, and essential nutrients. Some microalgal species possess natural antimicrobial compounds or biomolecules that act as immunostimulants, further enhancing the health of aquatic animals. Emerging genetic engineering technologies in microalgae could lead to the development of functional feed additives containing specific bioactives, such as fish growth hormones and antibacterials, which could significantly improve disease resistance in aquaculture (Charoonnart et al., 2018).

 

Synbiotic agents, which combine probiotics, prebiotics, and postbiotics, have also been explored as natural alternatives to synthetic drugs and antibiotics in aquaculture. These agents help maintain a healthy microbial environment, modulate gut microbiota, reinforce immune responses, and improve growth performance in aquatic animals (Srirengaraj et al., 2023). By promoting a balanced and healthy microbiome, synbiotics can effectively reduce the incidence of disease outbreaks and enhance the overall sustainability of aquaculture practices.

 

5.2 Application in Livestock Disease Prevention

In livestock production, the overuse of antibiotics has similarly led to the emergence of antibiotic-resistant bacteria, posing a significant threat to animal and human health. Probiotics have been proposed as an alternative antimicrobial strategy to mitigate this issue. By reducing zoonotic pathogens in the gastrointestinal tract of animals, probiotics can prevent the transmission of these pathogens through food, thereby enhancing food safety and animal health.

 

The use of bacteriophages, which are natural predators of bacteria, represents another innovative approach for controlling bacterial pathogens in livestock. Bacteriophages are harmless to humans and animals and can specifically target and eliminate pathogenic bacteria without affecting beneficial microbes. This specificity makes them a promising tool for enhancing microbial safety in food production and preventing the spread of antibiotic-resistant bacteria (Cabello et al., 2016; Endersen and Coffey, 2020).

 

Furthermore, the integration of probiotics, prebiotics, and synbiotics into livestock feed can improve gut health, boost immune responses, and enhance overall animal performance. These functional feed additives offer a sustainable and eco-friendly alternative to traditional antibiotics, contributing to the prevention of livestock diseases and the promotion of animal welfare (Hossain et al., 2017).

 

6 Challenges and Limitations

6.1 Ecological impact and non-target effects

The introduction of microbial predators as biocontrol agents can have significant ecological impacts, particularly concerning non-target effects. Generalist predators, which do not exclusively target specific pests, pose a risk to non-target species, potentially disrupting local ecosystems. For instance, the presence of alternative prey can reduce the efficacy of biocontrol agents, as seen with the notonectid Anisops debilis, which showed a preference for daphniid prey over mosquito larvae, thereby diminishing its impact on the target mosquito population (Cuthbert et al., 2020). The establishment and dispersal of biocontrol agents in new environments require careful risk assessments to evaluate their potential non-target effects and ecological impacts. The complexity of microbial interactions within biofilms and the broader microbial community further complicates the prediction of ecological outcomes, as seen with Bdellovibrio and like organisms (BALOs).

 

6.2 Development of resistance in target organisms

The development of resistance in target organisms is a significant challenge in the use of microbial predators as biocontrol agents. Just as pathogens can develop resistance to chemical pesticides, they can also evolve mechanisms to evade biocontrol agents. For example, the use of bacteriophages in food safety highlights the potential for bacterial pathogens to develop resistance to phage predation, which could undermine the long-term efficacy of phage-based biocontrol strategies (Endersen and Coffey, 2020). Similarly, the interactions between microbial predators and their prey in biofilms suggest that prey organisms may develop resistance mechanisms that could reduce the effectiveness of biocontrol agents over time. Therefore, continuous monitoring and adaptive management strategies are essential to mitigate the risk of resistance development.

 

6.3 Regulatory and commercialization barriers

Regulatory and commercialization barriers present another significant challenge to the widespread adoption of microbial predators as biocontrol agents. The regulatory framework for the approval and registration of biocontrol agents is often complex and stringent, requiring extensive risk assessments and evidence of safety and efficacy (Loomans, 2020). This can be particularly challenging for generalist predators, which require specific risk assessments due to their broad host range. The commercialization of biocontrol agents is hindered by economic factors, such as the cost of mass production, quality control, and distribution (Blackburn et al., 2016). The lack of efficient, commercially available biocontrol agents further limits the large-scale implementation of biocontrol strategies. Overcoming these barriers requires coordinated efforts between researchers, regulatory bodies, and industry stakeholders to streamline the approval process and enhance the commercial viability of biocontrol agents (Lenteren et al., 2018).

 

7 Advances in Research and Technology

7.1 Genetic engineering of microbial predators

Genetic engineering has emerged as a powerful tool to enhance the efficacy of microbial predators as biocontrol agents. For instance, Bdellovibrio bacteriovorus, a predatory bacterium, has shown potential in targeting Gram-negative bacteria, including antibiotic-resistant pathogens. Recent studies have identified and characterized genes essential for predation, paving the way for the genetic modification of these predators to improve their killing rates and specificity towards certain bacterial species (Duncan et al., 2019). Synthetic riboswitches have been developed to control gene expression in B. bacteriovorus, enabling the regulation of predation kinetics and enhancing its practical applications as a biocontrol agent (Dwidar and Yokobayashi, 2017). These advancements highlight the potential of genetic engineering to optimize microbial predators for more effective biocontrol strategies.

 

7.2 High-throughput screening for effective strains

High-throughput screening (HTS) techniques have revolutionized the identification of effective microbial strains for biocontrol. HTS enables the rapid and comprehensive exploration of diverse microbial libraries to identify strains with desired traits. For example, HTS has been employed to screen bacterial strains for antifungal properties, providing quantitative measures of biocontrol efficiency and distinguishing highly effective strains from less potent ones (Kjeldgaard et al., 2022). HTS has been used to map the genetic determinants of phage resistance in E. coli, uncovering host factors that confer resistance to various phages and informing the design of phage-based biocontrol strategies (Mutalik et al., 2020). These techniques facilitate the discovery of potent biocontrol agents and enhance our understanding of microbial interactions, ultimately leading to more effective and targeted biocontrol solutions.

 

7.3 Development of formulation and delivery systems

The development of effective formulation and delivery systems is crucial for the successful application of microbial predators as biocontrol agents. Advances in this area include the integration of microbial community studies with traditional biocontrol approaches, which can inform the formulation and timing of biocontrol agent applications (Massart et al., 2015). The use of synthetic microbial communities constructed and screened through platforms like the kChip allows for the identification of multispecies consortia with robust biocontrol properties (Kehe et al., 2019). These consortia can be formulated to enhance the stability and efficacy of biocontrol agents under various environmental conditions. Furthermore, the genetic improvement of biocontrol agents to enhance their resilience to environmental stresses and compatibility with agricultural practices can lead to more reliable and effective biocontrol formulations (Bielza et al., 2020). These advancements in formulation and delivery systems are essential for maximizing the impact of microbial predators in biocontrol applications.

 

8 Concluding Remarks

Microbial predators have shown significant potential as biocontrol agents across various domains, including agriculture and food safety. For instance, Myxococcus xanthus R31 has demonstrated high efficacy in controlling tomato bacterial wilt by preying on Ralstonia solanacearum and secreting extracellular lyase proteins. Similarly, bacteriophages have been recognized for their ability to enhance microbial safety in food production by targeting specific bacterial pathogens. The integration of microbial community studies with traditional biocontrol approaches has opened new avenues for innovative biocontrol methods, leveraging the interactions between microbial communities, host plants, and pathogens. Additionally, the use of predatory bacteria such as Bdellovibrio bacteriovorus has shown promise in reducing bacterial burdens in mammalian systems, highlighting their potential as novel biocontrol agents.

 

Future research should focus on the genetic improvement of biocontrol agents to enhance their performance under various environmental conditions. Identifying key traits such as resistance to toxins, adaptation to extreme temperatures, and increased fitness on non-prey food sources could significantly improve the efficacy of biocontrol agents. Moreover, the development of innovative dispersal strategies, such as entomovectoring, where microbial biocontrol agents are dispersed via pollinators, holds great promise for enhancing plant health and mitigating plant diseases. The integration of high-throughput sequencing technologies with biocontrol research will further our understanding of microbial interactions and help develop more effective biocontrol strategies.

 

To overcome the challenges associated with the inconsistent performance of microbial biocontrol agents, it is essential to focus on improving their establishment and spread in field conditions. This can be achieved through the development of novel formulations and dispersal methods, such as spray-dried powders and pollinator-dispersal systems. Addressing the technical errors and biases in microbiome research, enhancing bioinformatics capabilities, and adapting experimental schemes will be crucial for the successful implementation of microbiome-based biocontrol approaches. Increasing research on the predatory mechanisms of bacteria and their interactions with prey will provide valuable insights for developing new biocontrol agents and improving existing ones.

 

By addressing these challenges and exploring new directions, microbial predators can be effectively harnessed as biocontrol agents, offering sustainable and environmentally friendly solutions for managing plant diseases and ensuring food safety.

 

Acknowledgments

We would like to thank Professor S. Lu from Zhejiang A&F University for her invaluable guidance, insightful suggestions, and continuous support throughout the development of this study.

 

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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Molecular Microbiology Research
• Volume 14
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