Invited Review
Strategic Engineering of Synthetic Microbial Communities (SynComs) for Optimizing Plant Health and Yield in Agriculture 
Author Correspondence author
Molecular Microbiology Research, 2024, Vol. 14, No. 3
Received: 20 Mar., 2024 Accepted: 08 May, 2024 Published: 23 May, 2024
This comprehensive review encapsulates the current state of research on Synthetic Microbial Communities (SynComs) and their burgeoning role in agriculture. The paper aims to elucidate the conceptual framework and developmental milestones of SynComs, tracing their historical evolution from mere scientific inquiry to pivotal agricultural assets. By delving into the synthesis of current literature, this review presents an analytical digest of the advancements in SynCom development, their applications in enhancing plant health, and their integration with existing agricultural practices. The engineered microbial consortia are highlighted for their precise functionality, such as biofilm formation, secondary metabolite production, and induction of plant resistance, structured by ecological theories and phylogenetic organization. The document reviews evidence demonstrating the efficacy of SynComs in bolstering crop resilience, especially under challenging environmental conditions, with case studies exemplifying the protection of wheat against soilborne pathogens and the improvement of soybean yield. Furthermore, it explores the potential of SynCom integration with traditional breeding techniques and plant cultivation management, suggesting that SynComs can complement breeding programs and provide sustainable solutions to biotic stresses. The review concludes by underscoring the promise of SynComs in sustainable agriculture and proposing future research directions that address challenges in microbial colonization, stability, and the harmonization of SynComs with traditional farming methods. This work serves as a cornerstone for developing a new paradigm in precision agriculture where SynComs play a crucial role in crop management for enhanced productivity.
1 Introduction
In recent years, the agricultural sector has witnessed a surge in interest toward a more sustainable and resilient approach to crop production and plant health management (Fang, 2024). One of the most promising frontiers in this quest is the exploration and application of Synthetic Microbial Communities (SynComs), which hold the potential to revolutionize the way we support plant growth and combat agricultural challenges. SynComs are engineered communities of microorganisms specifically designed to provide beneficial effects to plants, such as enhanced nutrient uptake, disease resistance, and stress tolerance (Marín et al., 2021).
The significance of SynComs lies in their ability to mimic and enhance the natural plant-microbe interactions that are critical for plant health and soil fertility (Martins et al., 2023). By understanding and harnessing these relationships, SynComs can be strategically applied to improve agricultural productivity in a manner that is in harmony with the environment (Gopal and Gupta, 2016).
This review aims to consolidate the current body of research regarding the development and application of SynComs with a focus on enhancing plant health and agricultural productivity. Our objectives are multifold and we intend to gain a deep understanding of the concept and historical development of SynComs, provide a comprehensive summary of the progress made in this field, examine the potential for integration with traditional breeding techniques, and discuss the ways in which SynComs can be combined with plant cultivation management to unlock new possibilities in agriculture.
The integration of SynComs into agricultural systems offers a window into a future where plants can thrive with reduced chemical inputs, where soil health is actively managed through microbial interventions, and where crop yields can be sustained or enhanced despite the growing challenges of climate change. It is through this lens that we will explore the current landscape of SynComs research and its implications for the future of plant health and agricultural productivity.
2 The Concept of Synthetic Microbial Communities (SynComs)
2.1 Definition and engineering of SynComs
Synthetic Microbial Communities, commonly referred to as SynComs, represent a significant breakthrough in the intersection of microbial ecology and agricultural biotechnology. These are intentionally constructed consortia of microbial species, meticulously selected and engineered to perform specific functions beneficial to plant health and productivity (Gopal and Gupta, 2016). SynComs are not random assemblages but are designed to emulate and optimize the natural beneficial traits observed in plant-associated microbiomes. The key functions these microbial consortia are engineered for include biofilm formation, which can protect plant roots, the production of secondary metabolites, which can deter pathogens or attract beneficial insects, and the induction of plant resistance mechanisms, enhancing the plant’s innate ability to fend off diseases (Marín et al., 2021).
The rationale behind the precise composition of a SynCom lies in the desired outcome or function intended for the plant host. For instance, one SynCom may be tailored to improve nitrogen fixation, directly influencing the nutritional uptake of the plant, while another may be designed to induce systemic resistance to specific pathogens, thereby fortifying the plant’s defensive capabilities. Martins et al. (2023) describe these communities as meticulously engineered based on an understanding of how specific microbial species interact with each other and with their plant hosts, demonstrating the purpose-driven nature of SynComs .
2.2 Design of SynComs based on ecological theories of plant-microbiome interactions
The design of SynComs is not merely an act of biological engineering but is deeply rooted in ecological theories. These theories propose that plant-associated microbial communities are not arbitrary in their composition; rather, they possess a defined phylogenetic structure which is the result of complex community assembly rules. These rules dictate the interactions, co-existence, and functions of microbes within the community, which, in turn, impact the health and growth of the plant. SynComs are therefore constructed by simulating these natural organizational patterns, ensuring that the synthetic communities can integrate seamlessly into the plant’s ecosystem and perform their functions effectively.
According to Martins et al. (2023), the creation of SynComs takes into account the intricate network of interactions within the rhizosphere, the region of soil in the immediate vicinity of plant roots. In this densely populated microbial hub, the selection of species for inclusion in a SynCom is guided by their known roles and interactions in the natural soil microbiome. By aligning with ecological theories, designers of SynComs can anticipate how these microbes will behave in conjunction with the plant and its native microbiome, establishing a stable and supportive environment that promotes plant health and growth .
In summary, the development of SynComs marks a proactive stride towards harnessing microbial processes for agricultural advancement. It is a prime example of how scientific knowledge, especially the understanding of ecological and phylogenetic principles, can lead to practical applications that enhance the sustainability and productivity of crop systems.
3 Historical Overview of the SynCom Concept
3.1 Evolution of the SynCom concept alongside microbial ecology
The journey of Synthetic Microbial Communities (SynComs) is closely tied to the advancements in microbial ecology. Initially, the study of microbial communities was challenged by the complexity and variability of the environment. As microbial ecology progressed, the introduction of SynComs became a revolutionary approach. This allowed for a more controlled and systematic exploration of microbial functions and their contributions to plant health. SynComs simplified the complex interactions in natural microbial assemblages, thereby providing a clearer picture of the contributions and dynamics within microbial communities. This transition marked a significant shift from studying individual microbe-plant interactions to understanding the collective impact of microbial consortia.
3.2 Insights into plant-microbe regulation mechanisms through SynComs
SynComs have bridged the gap in understanding the intricate regulation mechanisms between plants and their associated microbiomes. By employing a reductionist approach, researchers have been able to construct simplified versions of microbial communities to study the core interactions that govern the plant-microbiome relationship. This method has provided valuable functional and mechanistic insights, revealing how plants may influence the composition and function of their microbiomes and vice versa. Through studies employing SynComs, scientists like Liu et al. (2019) have demonstrated that plants can recruit specific microbial species from the environment, which in turn can modulate the plant's health and growth. This research underscores the potential of SynComs to dissect complex biological interactions into more manageable and observable phenomena, offering a clearer understanding of the symbiotic relationships at play .
4 Research Progress in SynComs
4.1 Exploring plant root microbiomes: diverse methodologies for comprehensive understanding
In 2021, Marín et al. detail three investigative strategies for studying the root microbiome in plants (Figure 1). The Reductionist Approach, also known as Bottom-up, starts with the analysis of single microbial strains through culture-dependent techniques, offering precise insights into individual plant-microbe interactions with the benefit of simpler experimentation and high certainty in identifying specific microbial species. In contrast, the Holistic Approach or Top-down method delves into the complexities of wild microbial communities by utilizing culture-independent 'omics' techniques. While this approach embraces the dynamic nature of the rhizosphere, it trades off specificity for broader ecological insights, discerning patterns through correlational rather than causal analyses.
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Figure 1 Different approaches to understand the role of the root microbiome in plants. Schematic representation of information processing strategies (top-down and bottom-up) and the approaches that stand on the edges of them (reductionist and holistic) (Adopted from Marín et al., 2021) |
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Bridging these methodologies is the Synthetic Community (SynCom) Experimentation. This intermediate method combines the clarity of the Reductionist Approach with the encompassing perspective of the Holistic Approach. SynCom experiments deploy specially designed microbial communities of known composition, allowing researchers to manage experimental complexity more effectively and gain deeper understanding of microbe-microbe and plant-microbe interactions (Marín et al., 2021).
Framework of Marín et al. (2021) demonstrates the necessary balance between experimental complexity, certainty in microbial identification, and the depth of insights when researching plant root microbiomes. Their schematic underscores the need for both targeted and comprehensive strategies to fully grasp the intricate web of interactions in the microbiome that significantly influence plant health.
4.2 Recent studies highlighting SynComs' role in crop resiliency and environmental stress adaptation
The development of Synthetic Microbial Communities (SynComs) represents a significant advancement in agricultural biotechnology. Research has increasingly focused on how these engineered communities can bolster crop resilience, especially under challenging environmental conditions. In a pivotal study, Souza et al. (2020) detailed the design of SynComs that bolstered plant traits linked to improved stress tolerance, demonstrating a notable enhancement in crop resiliency.
This body of work underpins a new paradigm in which the deliberate assembly of microbial species can be tailored to address specific agricultural challenges. By employing SynComs, scientists are able to invoke precise microbiome functions, such as enhanced stress response mechanisms in plants, which are crucial for maintaining productivity amidst climatic and environmental adversities.
4.3 Case studies: protection against soilborne pathogens, nutrient efficiency, and plant growth promotion
Several case studies have underlined the effectiveness of SynComs in protecting crops against soilborne pathogens. Yin et al. (2022) illustrated how wheat crops benefitted from SynComs sourced from rhizosphere soil, which offered protection against fungal pathogens, thereby reducing the dependency on chemical fungicides .
Beyond pathogen defense, SynComs have been recognized for their role in optimizing nutrient uptake and utilization. Wang et al. (2021) reported that certain functionally assembled SynComs could substantially improve nutrient efficiency and yields in soybean crops. Such findings suggest that SynComs could lead to reduced fertilizer use, contributing to more sustainable agricultural practices.
Additionally, there is an emerging interest in the use of SynComs derived from compost-derived microbes. Tsolakidou et al. (2018) explored this domain, revealing that these specialized microbial pools could consistently enhance plant growth and health . These developments highlight the versatile nature of SynComs in various agricultural contexts, from boosting growth to ensuring crop survival under biotic and abiotic stressors.
The research progress in SynComs indicates a promising trend towards developing more resilient agricultural systems that can withstand the test of changing global environmental conditions. The potential of SynComs to revolutionize crop management practices is immense, paving the way for a future where sustainable and resilient agriculture is the norm.
5 Integration with Traditional Plant Breeding
5.1 How SynCom principles assist in traditional plant breeding
The integration of Synthetic Microbial Communities (SynComs) with traditional breeding techniques represents a pioneering approach to enhancing crop production and resilience. Traditional breeding has focused primarily on the genetic manipulation of plant genomes to select for desirable traits. However, the principles of SynComs extend this paradigm by considering the microbial environment's role in expressing these traits. According to Souza et al. (2020), plant-associated microbiomes significantly influence phenotypic traits, such as disease resistance, yield, and stress tolerance. By strategically using SynComs, breeders can now target these microbiome-influenced traits. This approach could lead to a new era of breeding strategies where the selected microbial consortia are used to steer the expression of plant genotypes, thereby facilitating the breeding of crops with improved performance and adaptability to a range of environmental conditions.
5.2 Breeding for specific plant traits influenced by the microbiome
The precise targeting of plant traits influenced by the microbiome is an innovative use of SynComs in traditional plant breeding. This process involves identifying key microbial species that interact with plant genomes to affect specific traits. For example, certain microbes can enhance nutrient uptake, promote growth under stress conditions, or increase resistance to pathogens. By incorporating SynComs into the breeding process, it is possible to promote these beneficial interactions and select for plants that not only possess the genetic capacity for these traits but also have an optimized microbiome that ensures their expression in various environments. Souza et al. (2020) suggest that designing SynComs for improved crop resiliency can serve as a blueprint for breeding programs looking to exploit the full potential of the plant microbiome . This presents an opportunity for breeders to develop crops that are better equipped to thrive in suboptimal conditions, ultimately leading to sustainable agriculture and enhanced food security.
5.3 New strategies in plant breeding: microbiome selection
Although plants are stationary, they have evolved unique strategies to cope with biotic and abiotic stresses through symbiosis with microbes. Plants not only select their required microbiomes from the soil but also carry a diverse microbial community in their seeds, which serves as a primary source for microbial inoculation in crop cultivation. Gopal and Gupta (2016) discussed in detail how plant microbiomes help maintain plant health and provide crucial genetic diversity, a potential that has yet to be utilized in traditional breeding strategies. Undoubtedly, selecting microbiomes will become a strategy for the next generation of plant breeding. Gopal and Gupta (2016) introduced a novel plant breeding approach through microbiome selection, developing new generation crops that rely less on inorganic inputs, are resistant to pests and diseases, and can adapt to climate changes. The authors suggest that future plant breeding strategies should consider the plant and its microbial symbionts as co-propagated partners (Gopal and Gupta, 2016).
6 Combination with Plant Cultivation Management
6.1 Sustainable application of SynComs in plant disease stress management
The integration of Synthetic Microbial Communities (SynComs) into plant cultivation management offers a sustainable solution to mitigate biotic stresses faced by crops. SynComs have been engineered to enhance plant resilience against a range of pathogens by optimizing the plant's own defense mechanisms. Utilizing SynComs as a part of an integrated disease management strategy can reduce reliance on chemical pesticides, thereby minimizing environmental impact and preserving beneficial soil microbiota. This approach aligns with sustainable agriculture principles, focusing on maintaining long-term soil health and crop productivity. As outlined by Pradhan et al. (2022), the strategic application of SynComs can combat biotic stresses by reinforcing the plant's innate immune responses and inducing systemic resistance.
6.2 Application of SynComs in seed treatment
Applying SynComs to seeds represents a significant advance in agricultural practices. This method effectively engineers the seedling microbiota from the very start of plant development, potentially leading to healthier and more resilient plants. The inoculation of seeds with SynComs has been demonstrated to alter the recruitment and assembly of microbial communities in both the seedlings and the surrounding rhizosphere. By doing so, it can create a more favorable microbiological environment that supports growth and combats pathogenic organisms. Arnault et al. (2023) illustrate the effectiveness of this technique in shaping seedling microbiota, thereby influencing subsequent plant-microbe interactions that are crucial for plant development .
6.3 Impact of SynComs on planting and rhizosphere microbial communities
The deployment of SynComs has a profound impact on the microbial communities associated with planted crops and their rhizosphere. By deliberately assembling and introducing beneficial microbial consortia, SynComs can significantly alter the diversity and function of the microbiome in favor of the plant's health. The targeted modification of microbial communities through SynComs can lead to improved nutrient uptake, enhanced stress tolerance, and suppression of harmful pathogens. This modification is not only beneficial for the individual plant but can also have positive implications for the overall agricultural ecosystem, promoting a more robust and sustainable cultivation practice as described by Arnault et al. (2023) in their exploration of seed microbiota engineering.
In conclusion, the combination of SynComs with plant cultivation management is a promising area that aligns well with the emerging needs for sustainable agriculture. The continued research and application of SynComs in this manner not only advance our understanding of plant-microbe interactions but also pave the way for innovative strategies to bolster crop resilience and productivity.
7 Discussion and Prospects
7.1 Prospects of SynComs as a strategy to enhance plant health and agricultural productivity
Synthetic Microbial Communities (SynComs) have emerged as a cutting-edge strategy with significant potential to enhance plant health and boost agricultural productivity. The synergy among the microbial species within these communities can be harnessed to form a stable and efficacious tool for improving crop resilience and yields. Studies have shown that SynComs can successfully increase the natural defense mechanisms of plants, leading to healthier crops that can withstand various environmental stresses (Yin et al., 2022; Martins et al., 2023). This synergy is crucial not just for plant growth but also for enabling the sustainable intensification of agriculture needed to meet the global food demand.
7.2 Future research directions including challenges in microbial colonization and stability
Despite their promise, the application of SynComs in agriculture faces significant challenges, especially in the aspects of microbial colonization and stability. Future research should prioritize developing methodologies that enhance the successful colonization of beneficial microbes in the plant microbiome. Additionally, ensuring the long-term stability of these communities within the plant's ecosystem is essential to provide enduring benefits (Tsolakidou et al., 2018; Souza et al., 2020). Research should also investigate the resilience of SynComs against competing native microflora and their ability to adapt to different plant varieties and environmental conditions (Wang et al., 2021).
7.3 Sustainable integration of SynComs with traditional agricultural practices
Integrating SynComs with conventional agricultural practices offers a sustainable path to improve crop management. Traditional practices and the innovative use of SynComs can complement each other, creating a holistic approach to agriculture. SynComs can be applied in tandem with traditional soil and seed treatments to engineer robust seedling microbiomes, thus enhancing the plants' capacity to regulate their rhizosphere microbiota (Arnault et al., 2023). This integration can result in improved nutrient uptake, better stress tolerance, and ultimately, higher yields. Moreover, aligning SynComs with sustainable agricultural practices could contribute to reducing the reliance on chemical inputs, promoting biodiversity, and preserving ecological balances (Shayanthan et al., 2022; Pradhan et al., 2022).
In conclusion, SynComs hold the key to unlocking a new era of sustainable agriculture. With focused research on overcoming current challenges and strategic integration with traditional farming techniques, SynComs have the potential to revolutionize how we cultivate crops, leading to a more resilient and productive agricultural landscape.
Funding
This research was funded by the Hainan Provincial Natural Science Foundation of China (321RC545, 320MS040); The Innovation Platform for Academicians of Hainan Province (YSPTZX202130); National Key Research and Development Program of China (2021YF C3201600).
Acknowledgments
I extend my thanks to the two anonymous peer reviewers for their valuable feedback on this manuscript.
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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