Molecular Microbiology Research 2024, Vol.14 http://microbescipublisher.com/index.php/mmr © 2024 MicroSci Publisher, an online publishing platform of Sophia Publishing Group. All Rights Reserved. Sophia Publishing Group (SPG), founded in British Columbia of Canada, is a multilingual publisher.
Molecular Microbiology Research 2024, Vol.14 http://microbescipublisher.com/index.php/mmr © 2024 MicroSci Publisher, an online publishing platform of Sophia Publishing Group. All Rights Reserved. Sophia Publishing Group (SPG), founded in British Columbia of Canada, is a multilingual publisher. Publisher MicroSci Publisher Editedby Editorial Team of Molecular Microbiology Research Email: edit@mmr.microbescipublisher.com Website: http://microbescipublisher.com/index.php/mmr Address: 11388 Stevenston Hwy, PO Box 96016, Richmond, V7A 5J5, British Columbia Canada Molecular Microbiology Research (ISSN 1927-5595) is an open access, peer reviewed journal published online by MicroSci Publisher. The journal publishes all the latest and outstanding research articles, letters and reviews in all areas of molecular microbiology, including original articles, reviews and brief reports in microbiology, bacteriology, mycology, molecular and cellular biology and virology at the level of gene expression and regulation, genetic transfer, cell biology and subcellular organization, pathogenicity and virulence, physiology and metabolism, cell-cell communication and signalling pathways as well as the interactions between the various cell systems of microorganisms including the interrelationship of DNA, RNA and protein biosynthesis. All the articles published in Molecular Pathogens are Open Access, and are distributed 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. MicroSci Publisher uses CrossCheck service to identify academic plagiarism through the world’s leading plagiarism prevention tool, iParadigms, and to protect the original authors’ copyrights. MicroSci Publisher is an international Open Access publisher specializing in microbiology, bacteriology, mycology, molecular and cellular biology and virology registered at the publishing platform that is operated by Sophia Publishing Group (SPG), founded in British Columbia of Canada.
Molecular Microbiology Research (online), 2024, Vol. 14 ISSN 1927-5595 http://microbescipublisher.com/index.php/mmr © 2024 MicroSci Publisher, an online publishing platform of Sophia Publishing Group. All Rights Reserved. Sophia Publishing Group (SPG), founded in British Columbia of Canada, is a multilingual publisher. Latest Content 2024, Vol.14, No.5 【Review Article】 Microbial Predators as Biocontrol Agents: Potential and Challenges 208-217 Liangwei Lü, Zhongqi Wu DOI: 10.5376/mmr.2024.14.0023 Cooperative Symbiosis: New Opportunities for Enhancing Tree Stress Resistance through Rhizosphere Microbes 218-225 Chunyan Tan, Chunyang Zhan DOI: 10.5376/mmr.2024.14.0024 【Research Perspective】 Conservation and Diversity of Seed-Associated Endophytes in Zea 226-235 Jiamin Wang, Yunchao Huang DOI: 10.5376/mmr.2024.14.0025 【Research Insight】 Enhancing Rice Stress Tolerance: New Insights into the Synergistic Roles of Roots and Rhizosphere Microbes 236-247 Xianyu Wang, Qian Zhu, Juan Li, Hanqi Li, Jiang Qin, Hang Yu, Dongsun Lee, Lijuan Chen DOI: 10.5376/mmr.2024.14.0026 【Feature Review】 Rhizosphere Microbial Interactions and Their Impact on Kiwifruit Health 248-258 Yiwei Li, Jin Zhang, Liyu Liang, Bolun Chen, Yunwu Huang, Xin Jiang, Yun Liu, Jikui Huang, Xi Wang DOI: 10.5376/mmr.2024.14.0027
Molecular Microbiology Research 2024, Vol.14, No.5, 208-217 http://microbescipublisher.com/index.php/mmr 208 Review Article Open Access 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 Corresponding author: zhongqi.wu@jicat.org Molecular Microbiology Research, 2024, Vol.14, No.5 doi: 10.5376/mmr.2024.14.0023 Received: 15 Jul., 2024 Accepted: 26 Aug., 2024 Published: 08 Sep., 2024 Copyright © 2024 Lü and Wu, 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. Preferred citation for this article: Lü L.W., and Wu Z.Q., 2024, Microbial predators as biocontrol agents: potential and challenges, Molecular Microbiology Research, 14(5): 208-217 (doi: 10.5376/mmr.2024.14.0023) 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.
Molecular Microbiology Research 2024, Vol.14, No.5, 208-217 http://microbescipublisher.com/index.php/mmr 209 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). 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
Molecular Microbiology Research 2024, Vol.14, No.5, 208-217 http://microbescipublisher.com/index.php/mmr 210 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. Figure 1 Bacterial origin of cytotoxic benzolactones fromM. verticillatacultures (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 bacteriumGynuella 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)
Molecular Microbiology Research 2024, Vol.14, No.5, 208-217 http://microbescipublisher.com/index.php/mmr 211 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
Molecular Microbiology Research 2024, Vol.14, No.5, 208-217 http://microbescipublisher.com/index.php/mmr 212 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. 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).
Molecular Microbiology Research 2024, Vol.14, No.5, 208-217 http://microbescipublisher.com/index.php/mmr 213 Figure 2 Illustration of the use and impact of probiotics in aquaculture systems (Adopted from Srirengaraj et al., 2023) 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.
Molecular Microbiology Research 2024, Vol.14, No.5, 208-217 http://microbescipublisher.com/index.php/mmr 214 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.
Molecular Microbiology Research 2024, Vol.14, No.5, 208-217 http://microbescipublisher.com/index.php/mmr 215 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 solanacearumand 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. References Banks E., Lambert C., Mason S., Tyson J., Radford P., McLaughlin C., Lovering A., and Sockett R., 2023, An MltA-like lytic transglycosylase secreted by Bdellovibrio bacteriovorus cleaves the prey septum during predatory invasion, Journal of Bacteriology, 205(4): e00475-22. https://doi.org/10.1128/jb.00475-22 Bielza P., Balanza V., Cifuentes D., and Mendoza J., 2020, Challenges facing arthropod biological control: identifying traits for genetic improvement of predators in protected crops, Pest Management Science, 76(11): 3517-3526. https://doi.org/10.1002/ps.5857 Blackburn D., Shapiro-Ilan D., and Adams B., 2016, Biological control and nutrition: food for thought, Biological Control, 97: 131-138. https://doi.org/10.1016/J.BIOCONTROL.2016.03.007 Bratanis E., Andersson T., Lood R., and Bukowska-Faniband E., 2020, Biotechnological potential of Bdellovibrio and like organisms and their secreted enzymes, Frontiers in Microbiology, 11: 662. https://doi.org/10.3389/fmicb.2020.00662
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Molecular Microbiology Research 2024, Vol.14, No.5, 218-225 http://microbescipublisher.com/index.php/mmr 218 Review Article Open Access Cooperative Symbiosis: New Opportunities for Enhancing Tree Stress Resistance through Rhizosphere Microbes Chunyan Tan, Chunyang Zhan Hainan Institute of Biotechnology, Haikou, 570206, Hainan, China Corresponding author: chunyang.zhan@hibio.org Molecular Microbiology Research, 2024, Vol.14, No.5 doi: 10.5376/mmr.2024.14.0024 Received: 27 Jul., 2024 Accepted: 06 Sep., 2024 Published: 20 Sep., 2024 Copyright © 2024 Tan and Zhan, 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. Preferred citation for this article: Tan C.Y., and Zhan C.Y., 2024, Cooperative symbiosis: new opportunities for enhancing tree stress resistance through rhizosphere microbes, Molecular Microbiology Research, 14(5): 218-225 (doi: 10.5376/mmr.2024.14.0024) Abstract Tree rhizosphere microbes interact with plants through various mechanisms, promoting nutrient uptake, enhancing stress resistance, and improving soil structure. Their diversity and functions play a crucial role in plant ecosystems, helping to maintain ecological balance and improve forest health and productivity. This study analyzes the various stress factors faced by trees and highlights the importance of rhizosphere microbes in promoting plant health. It provides an overview of the diversity of rhizosphere microbes, including bacteria, fungi, and actinomycetes, as well as their key functions in soil and plant health. Furthermore, it explores how rhizosphere microbes enhance trees' resistance to environmental stress through mechanisms such as facilitating nutrient uptake, modulating hormones and signaling, and inducing systemic resistance. This research provides guidance for future studies and applications aimed at utilizing rhizosphere microbes to improve tree health and adaptability. Keywords Rhizosphere microbes; Stress resistance; Nutrient uptake; Plant health; Ecological balance 1 Introduction Trees, as long-lived organisms, are subjected to a variety of stress factors throughout their lifespans. These stressors can be broadly categorized into biotic and abiotic factors. Biotic stressors include pathogens such as soil-borne fungi and insects, which can significantly impact tree health and productivity. Abiotic stressors encompass environmental conditions such as drought, salinity, heavy metal contamination, and extreme temperatures, all of which can adversely affect tree growth and survival (Khan et al., 2021). The increasing frequency and intensity of these stress factors, exacerbated by climate change, pose a significant threat to forest ecosystems and necessitate the development of innovative strategies to enhance tree resilience. The rhizosphere, the narrow region of soil influenced by root secretions and associated microbial activity, plays a crucial role in plant health. Rhizosphere microbes, including bacteria, fungi, and archaea, form complex interactions with plant roots that can enhance nutrient uptake, improve soil structure, and increase resistance to both biotic and abiotic stresses (Andargie et al., 2023). Symbiotic relationships, such as those formed with arbuscular mycorrhizal (AM) fungi and plant growth-promoting rhizobacteria (PGPR), are particularly beneficial. These microbes can improve plant access to essential nutrients like phosphorus and nitrogen, modulate plant hormone levels, and induce systemic resistance to pathogens (Cumming et al., 2015; Wang et al., 2020; Ho-Plágaro and García-Garrido, 2022). Understanding and harnessing these interactions offer promising avenues for enhancing tree stress resistance. This study will analyze various biotic and abiotic stress factors that affect trees and the role of rhizosphere microorganisms in alleviating these stresses. It will discuss the mechanisms by which rhizosphere microorganisms, especially arbuscular mycorrhizal (AM) fungi and plant growth-promoting rhizobacteria (PGPR), enhance tree health and stress resistance, and focus on introducing the latest research results on the interaction between trees and rhizosphere microorganisms and their impact on forest management and protection. Furthermore, future research directions will be proposed to optimize the use of rhizosphere microorganisms to enhance trees' adaptability to environmental stress.
Molecular Microbiology Research 2024, Vol.14, No.5, 218-225 http://microbescipublisher.com/index.php/mmr 219 2 Rhizosphere Microbes: Diversity and Functions 2.1 Types of rhizosphere microbes The rhizosphere, the narrow region of soil influenced by root secretions and associated soil microorganisms, hosts a diverse array of microbes including bacteria, fungi, and actinomycetes. These microbial communities play crucial roles in plant health and soil fertility. Rhizosphere bacteria are highly diverse and include beneficial genera such as Pseudomonas, Rhizobium, and Bacillus. These bacteria can promote plant growth by fixing nitrogen, solubilizing phosphorus, and producing plant growth-promoting hormones (Wu et al., 2021). They can act as biocontrol agents against soil-borne pathogens. Mycorrhizal fungi, particularly arbuscular mycorrhizal (AM) fungi, form symbiotic relationships with plant roots, enhancing nutrient uptake, especially phosphorus and nitrogen, and improving plant stress tolerance (Shi et al., 2022). These fungi also play a role in structuring the rhizosphere microbiome, which can further influence plant health and stress resistance (Figure 1) (Hao et al., 2021). These filamentous bacteria are known for their ability to decompose complex organic materials and produce antibiotics that suppress soil pathogens. Genera such as Streptomyces and Arthrobacter are commonly found in the rhizosphere and contribute to plant health by promoting nutrient cycling and inhibiting harmful microbes. The study by Hao et al. (2021) demonstrated that arbuscular mycorrhizal fungi promote tolerance to the harmful heavy metal lanthanum by regulating the structure of the rhizosphere microbial community. They help plants cope better with adverse environments by enhancing nutrient absorption and inducing the enrichment of beneficial microorganisms. Figure 1 PCoA of unweighted UniFrac distances for the rhizosphere bacteria (a) and fungi (b) of different treatments on OTUs level. Co-occurrence network analysis for the rhizosphere bacteria (c) and fungi (d) of different treatments on OTUs level with abundance more than 50 (Adopted from Hao et al., 2021)
Molecular Microbiology Research 2024, Vol.14, No.5, 218-225 http://microbescipublisher.com/index.php/mmr 220 2.2 Key functions of rhizosphere microbes in soil and plant health Rhizosphere microbes perform several key functions that are essential for soil health and plant growth. These functions include nutrient cycling, enhancing plant stress resistance, and acting as a barrier against pathogens. Rhizosphere microbes are integral to the cycling of essential nutrients such as nitrogen, phosphorus, and potassium. For instance, AM fungi facilitate the uptake of phosphorus and other nutrients by plants, while nitrogen-fixing bacteria convert atmospheric nitrogen into forms that plants can use (Fu et al., 2023). This nutrient exchange is crucial for maintaining soil fertility and promoting plant growth. Rhizosphere microbes can significantly enhance plant resistance to various abiotic stresses such as heavy metals, drought, and salinity. For example, AM fungi have been shown to improve plant tolerance to heavy metal stress by altering the rhizosphere microbiome and promoting the enrichment of beneficial microbes. Similarly, co-inoculation with rhizobia and AM fungi can enhance plant resistance to cadmium stress by modifying the rhizosphere microbial community. The rhizosphere microbiome acts as a protective barrier against soil-borne pathogens. Beneficial microbes can outcompete pathogens for resources, produce antimicrobial compounds, and induce systemic resistance in plants (Hu et al., 2020; Lazcano et al., 2021; Li et al., 2021). For instance, certain bacterial genera such as Pseudomonas and Burkholderia are associated with increased resistance to fungal pathogens in strawberry cultivars. 3 Mechanisms of Stress Resistance Enhancement 3.1 Nutrient uptake facilitation by rhizosphere microbes 3.1.1 Enhanced phosphorus solubilization Rhizosphere microbes, particularly arbuscular mycorrhizal fungi (AMF) and phosphate-solubilizing bacteria, play a crucial role in enhancing phosphorus (P) availability to plants. AMF, such as Claroideoglomus etunicatum, have been shown to significantly increase the uptake of phosphorus in maize, even under stress conditions like heavy metal contamination (Hao et al., 2021). Similarly, phosphate-solubilizing bacteria can convert insoluble phosphorus into forms that are readily available for plant uptake, thereby improving plant growth and nutrient content. For instance, co-inoculation with diazotrophic and P-solubilizing bacteria has been demonstrated to enhance phosphorus content and biological nitrogen fixation in wheat. 3.1.2 Nitrogen fixation and mobilization Nitrogen fixation and mobilization are critical processes facilitated by rhizosphere microbes. Plant growth-promoting rhizobacteria (PGPR) such as Bacillus subtilis can enhance nitrogen fixation and mobilization, thereby improving plant growth and stress resilience. The synergistic application of diazotrophic bacteria and P-solubilizing bacteria has been shown to significantly increase nitrogen content in both plant tissues and soil, further promoting plant health and growth. 3.1.3 Iron chelation and availability Iron availability is another essential factor for plant growth, often limited by its low solubility in soil. Rhizosphere microbes, including Bacillus species, produce siderophores that chelate iron, making it more available to plants. This process not only enhances iron uptake but also suppresses the growth of soil-borne pathogens, contributing to overall plant health and stress resistance (Hashem et al., 2019; Li et al., 2020). 3.2 Hormonal modulation and stress signaling Rhizosphere microbes can modulate plant hormonal levels and stress signaling pathways, thereby enhancing plant stress resistance. For example, Bacillus subtilis produces various phytohormones and stress-related metabolites that help plants cope with biotic and abiotic stresses. These microbes can induce systemic resistance in plants, leading to the activation of stress-response genes and the production of antioxidants (Tsotetsi et al., 2022). The co-inoculation of rhizobia and AMF has been shown to increase antioxidant enzyme activities in plants, mitigating stress-induced damage (Wang et al., 2021).
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