Archna Suman*
Venkadasamy Govindasamy
Balasubramanian Ramakrishnan
K. Aswini
J. SaiPrasad
Pushpendra Sharma
Devashish PathakKannepalli Annapurna- Division of Microbiology, ICAR-Indian Agricultural Research Institute (IARI), New Delhi, India
Interactions among the plant microbiome and its host are dynamic, both spatially and temporally, leading to beneficial or pathogenic relationships in the rhizosphere, phyllosphere, and endosphere. These interactions range from cellular to molecular and genomic levels, exemplified by many complementing and coevolutionary relationships. The host plants acquire many metabolic and developmental traits such as alteration in their exudation pattern, acquisition of systemic tolerance, and coordination of signaling metabolites to interact with the microbial partners including bacteria, fungi, archaea, protists, and viruses. The microbiome responds by gaining or losing its traits to various molecular signals from the host plants and the environment. Such adaptive traits in the host and microbial partners make way for their coexistence, living together on, around, or inside the plants. The beneficial plant microbiome interactions have been exploited using traditional culturable approaches by isolating microbes with target functions, clearly contributing toward the host plants’ growth, fitness, and stress resilience. The new knowledge gained on the unculturable members of the plant microbiome using metagenome research has clearly indicated the predominance of particular phyla/genera with presumptive functions. Practically, the culturable approach gives beneficial microbes in hand for direct use, whereas the unculturable approach gives the perfect theoretical information about the taxonomy and metabolic potential of well-colonized major microbial groups associated with the plants. To capitalize on such beneficial, endemic, and functionally diverse microbiome, the strategic approach of concomitant use of culture-dependent and culture-independent techniques would help in designing novel “biologicals” for various crops. The designed biologicals (or bioinoculants) should ensure the community’s persistence due to their genomic and functional abilities. Here, we discuss the current paradigm on plant-microbiome-induced adaptive functions for the host and the strategies for synthesizing novel bioinoculants based on functions or phylum predominance of microbial communities using culturable and unculturable approaches. The effective crop-specific inclusive microbial community bioinoculants may lead to reduction in the cost of cultivation and improvement in soil and plant health for sustainable agriculture.
Introduction
Cultivated soils are one of the most diverse microbial ecosystems, harboring bacteria, fungi, archaea, viruses, protists, and many others and supporting various biogeochemical cycles and plant growth. Soil microbial communities are critical to plant health and adapt rapidly to different abiotic and biotic stresses (Abdul Rahman et al., 2021). The soils and their microbial members provide humans with 98.8% of the plant foods we eat (FAO, 2018; Kopittke et al., 2019; Soto-Giron et al., 2021). The Food and Agriculture Organization (FAO) predicts that soil erosion could result in between 20 and 80% losses in agricultural yields due to human activities and climate change events. This erosion of topsoil could result in variable agricultural yields, depending on the soil type and the resource use pattern (Kopittke et al., 2019; Christy, 2021). The agrarian management of soils depends on many synthetic chemical inputs for increasing profitability and productivity. Unfortunately, intensive use of these chemical inputs has led to adverse environmental consequences from regional to global scales. To reduce chemical inputs and their associated undesirable effects in the soil and environment, microbial interventions as biological products are becoming an integral part of plant nutrient management programs and pest and disease management practices.
Microbial communities associated with plants, presently referred to as the plant microbiome, extend the host plant genome and their functions (Figure 1). Many studies demonstrate that these microbiomes are the key determinants of plant development, health, and productivity (Conrad et al., 2006; Bulgarelli et al., 2012; Lundberg et al., 2012; Turner et al., 2013; Williams, 2013). The recent investigations have unraveled the complex network of genetic, biochemical, physical, and metabolic interactions among the plant host, the associated microbial communities, and the environment. These interactions shape the microbiome assembly and modulate beneficial traits such as nutrient acquisition and plant health (Trivedi et al., 2021). Nutrient acquisition by plants is mediated by diverse mechanisms that include (i) augmenting the surface area accessed by plant roots for uptake of water and nutrients, (ii) through nitrogen fixation, (iii) P-solubilization, (iv) the production of siderophore and HCN production, and other unknowns. Furthermore, their contributions in protection against biotic (pests and diseases) and abiotic stresses directly or through modulating intrinsic resistance/tolerance have been reported (Pii et al., 2015; Govindasamy et al., 2020; Abiraami et al., 2021). The basis of this review is to highlight strategic approaches for designing novel bioinoculants based on the plant microbiome data generated from both culturable and unculturable approaches. Such plant microbiome-based specific bioinoculants may function in a better way as compared to the conventional bioinoculants with non-specific microbial isolates. The agricultural bioinoculant market is a fast-growing sector with a compound annual growth rate (CAGR) of 6.9% with a predicted value of over 12 billion US dollars by 2025. The growth of the market is driven by increasing health concerns and awareness among consumers, resulting in the inclination toward organic farming practices or low-chemical-input agriculture. Hence, the bioinoculant technology will move forward toward reducing the cost of cultivation while improving soil and plant health for sustainable agriculture.
Figure 1. Microbial colonization depicted in different plant niches: Rhizosphere, phyllosphere and endosphere of root, stem, leaf, and grain.
Plant-Microbiome-Mediated Adaptive Functions
The microbiome is playing a significant role, throughout the plant life cycle, in altering the physiologies, and development through phytohormones, metabolites, signals, responses, nutrients, and induction of systemic resistance against pathogens as well as tolerance mechanisms against abiotic stresses such as drought, salinity, or contaminated soils (Mendes et al., 2013; Marag and Suman, 2018; Compant et al., 2019). At the community level, the microbiome functional capability is more than the sum of its individual microbial components as individual microbial species in the microbiome may interact to form a complex network, which interrelates with the host plant(s) in a mutualistic, synergistic, commensalistic, amensalistic, or parasitic mode of relationship. These interactions influence each member of the complex network for their survival, fitness, and propagation. The sum of all these interactions influences plant health vis-a-vis soil fertility (Berg et al., 2020). The advancement in the molecular methods and affordable sequencing has led to a greater understanding of the microbiome composition; however, translating species or gene composition into microbiome functionality still remains a challenge. Using community ecology concepts, Saleem et al. (2019) have indicated that more than individual functions, the overall microbiome biodiversity is critical as the driver of plant growth, soil health, and ecosystem functioning. By meta-analysis of numerous publications on microbial biodiversity and ecosystem functioning (BEF), they indicated that the impacts can be classified into (i) biodiversity effects (negative, no (or unknown), and positive effects of biodiversity on microbial derived services), (ii) assessed functions (nutrient cycling, protection from different stresses, etc.), and (iii) underlying mechanisms (cooperation, mutualism, etc.). Higher diversity can increase the number and resilience of plant-beneficial functions that can be co-expressed and can unlock the expression of plant-beneficial traits that are hard to obtain from any species in isolation. Therefore, the maintenance and modulation of desired microbial activities (functional pools) in the vicinity of the plant system may have more significant potential to provide crops with required nutrition and other protection systems (Figure 2).
Figure 2. Beneficial functions of Plant associated microbiome. N, Nitrogen; P, Phosphorous; K, Potassium; Zn, Zinc; Fe, Iron; S, Sulfur; IAA, Indole Acetic Acid; GA, Giberrelic Acid; CK, Cytokinin; ACC, 1-AminoCyclopropane Carboxylate; HCN, Hydrocyanic Acid.
With increasing knowledge of plant microbiome vis-à-vis plant performance, approaches are being devised for tapping the potential of plant-growth-promoting (PGP) isolates, by employing both culturable and unculturable approaches. The advent of “omics” technologies understandably provides the tools for a broader understanding of microbial ecosystems and their dynamic interaction with their hosts. These techniques and methods enable the screening of large microbial populations and easily identify the individual or groups of taxa with functional capabilities. Large-scale genomic analyses of plant-associated bacteria have indicated that the bacteria from phyla Actinobacteria, Bacteroidetes, Firmicutes, and Proteobacteria are dominant in different plant niches (Levy et al., 2018a,b). The exhaustive investigations on wheat seeds followed by rhizospheric, epiphytic, and endophytic bacterial diversity, growing in six diverse agro-climatic zones in India, led to more than 200 diverse bacterial isolates with PGP traits (Suman et al., 2016; Verma et al., 2016, 2019; Verma and Suman, 2018; Sai Prasad et al., 2021). The PGP rhizobacteria (PGPR) can adapt easily to adverse conditions and protect the host plants from the deleterious effects of specific environmental stresses (Glick et al., 1997). Several bacteria like Bacillus sp., Azospirillum, Herbaspirillum, and pink-pigmented methylotrophic bacteria have been shown to mitigate stress conditions in maize, wheat, and other crops (Chakraborty et al., 2013; Vurukonda et al., 2016; Curá et al., 2017; Ahlawat et al., 2018). Various factors related to host, microbes, and the environment influence the community composition and diversity of plant microbiome (Dastogeer et al., 2020). Our knowledge on the underlying mechanism(s) of microbiome assemblages and how they influence the host plants is still lacking. How the entire assembly of microbial communities interfere with the host fitness and health remains largely unknown. Connecting the microbiome composition comprising PGP as well as plant-growth-compromising activities and diversity to their function is a great challenge for future research.
These fundamental, microbial-mediated adaptive functions can help address the significant challenges in sustainable food production under the changing climatic conditions. Likewise, the strategic application of microbial communities rather than as individual isolates to improve plant production offers enormous potential, particularly under adverse environmental conditions. Their applications can serve multiple purposes, such as reducing climate change impact and avoiding excessive reliance on chemical fertilizers and pesticides. Earlier studies solely based on culture-dependent techniques have overlooked the benefits of collective microbial functional and genetic diversity and the advantages of the culture-independent methods (Banik and Brady, 2010; Stewart, 2012; Turner et al., 2013; De Souza et al., 2016; Waigi et al., 2017; Armanhi et al., 2018; Mourad et al., 2018).
The cultivable isolates of the microbial community members such as plant probiotics, biofertilizers, or agricultural bioinoculants have shown their distinct influences on plant growth, fitness, and stress resilience but with certain limitations. The developed formulations containing one or more beneficial microorganism strains (or species) can mediate the cycling of several elements from the soil and transform them into the more readily available form of nutrients for plant uptake. Not only do the probiotic action of these formulations increase the growth, yield, and quality of plants, but they are also a tool to produce high-quality functional foods. The use of microbial-based agricultural inputs has a long history, beginning with broad-scale rhizobial inoculation of legumes in the early twentieth century (Desbrosses and Stougaard, 2011). The “Fresh” Green Revolution, perhaps the Bio-Revolution, needs to be based on fewer intensive inputs with reduced environmental impact. It would be based on biological inputs through utilization of the phytomicrobiome (with inoculants, microbially produced compounds, etc.) and improved crops (by manipulation of the phytomicrobiome community structure) (Timmusk et al., 2017; Backer et al., 2018). With increasing data availability on plant microbiome from different ecological niches, strategic approaches based on the concomitant use of culture-dependent and culture-independent techniques, targeting all the plant-beneficial microbial groups, are necessitated to develop novel biological products in all categories like biofertilizers, biopesticides, bioagents, or bioinoculants and biostimulants.
Potential of Bioinoculants for Field Application
The current knowledge on functions, ecological adaptations, host interactions, and putative beneficial traits of microorganisms associated with the host plants mainly revolves around a handful of cultivable rhizospheric and endophytic bacteria or fungi. Many microbial formulations having individual or mixture of strains are developed and used at present. These biological or bioinoculants are nitrogen fixers, phosphate solubilizers, siderophore producers, photohormone producers, and exopolysaccharide producers. Some of them are involved in lytic enzyme production against pests and pathogens, antibiosis, and induced systemic resistance (Gupta et al., 2015; Sruthilaxmi and Babu, 2017).
The bioinoculants are grouped as either biofertilizers or bioagents depending on the intended purpose of plant growth promotion or protection, respectively. The biofertilizers include the individual species of Azotobacter, Azospirillum, and Rhizobium; phosphate-, potassium-, and zinc-solubilizing bacteria; vesicular–arbuscular mycorrhiza (VAM), and Acetobacter. Crop-specific biofertilizers like Gluconacetobacter diazotrophicus for sugarcane or generic biofertilizers like Pantoea isolates showing multi-PGP activities in several crops have demonstrated benefits in improving crop yield and productivity (Suman et al., 2005, 2008). Not only the rhizosphere-colonizing but also several endosphere-colonizing bacteria have been exploited for their beneficial contributions in sustainable agriculture (White et al., 2019). Presently, bioinoculants are available mostly as single entities (Bashan et al., 2014) but are also being formulated as consortia with multiple bacteria and fungi, which have synergistic PGP traits for improving plant production and productivity. Tables 1, 2 summarize the current status of various microbial formulations developed using single, dual, or multiple isolates as bioinoculants to improve nutrient uptake or protect against various biotic and abiotic stresses.
Table 1. Status of various microbial inoculants developed as synthesized microbial communities in use for improving nutrient uptake and protections against plant pathogens.
Table 2. Fungal inoculants developed as synthesized microbial communities used for improving nutrient uptake and protections against plant pathogens.
Although the biofertilizer/bioinoculant technology has grown into a proven biological or biotechnological innovation, it is still struggling to get acceptability and popularity with farmers, the end-users. The availability and quality of bioinoculants and their inconsistent performances under field conditions have been identified as significant issues in their adoption by the farming community (Martínez-Hidalgo et al., 2019), which requires the attention of the policymakers in different countries. Along with the development, large-scale production, and assured quality of bioinoculants, one of the most promising ways to increase their efficacy is by introducing effective delivery systems. The farmers may repose the faith, buy these products confidently, and compare their usefulness and cost–benefit ratios with conventional fertilizer inputs. Many studies on bioinoculant development and laboratory-based and field studies proving their worth indicate that these microbial resources must be considered a partial replacement as the application of chemicals may not be wholly replaceable or transferable into biologicals or microbials (Sessitsch et al., 2019).
Designing Targeted Synthetic Bioinoculants
The natural microbial communities are composed of a mix of microbes with often unknown functions. A promising way to overcome the difficulties associated with studying natural communities is to create artificial synthetic communities that retain the key features of their natural counterparts. With reduced complexity, synthetic microbial communities behave like a defined system and can act as a model system to assess the role of key ecological, structural, and functional features of communities in a controlled way (Großkopf and Soyer, 2014).
The existing thought process of top-down and bottom-up approaches for synthesizing microbial communities is based on the functional character of the individual microbial isolate and metabolic interactions among isolates, respectively. Basic motifs of commensalism, competition, predation, cooperation, and amensalism are the key metabolic interactions for the common substrate or metabolites leading to the community formations (Großkopf and Soyer, 2014). Several reviews have summarized the study of ecological interactions among microbes in synthetic as well as in natural microbial communities (Faust and Raes, 2012; Mitri and Richard Foster, 2013). Linking the composition of microbial communities with the functions is a central challenge in microbial ecology. It may be linked in some systems, but not in others, as some functions are restricted to certain taxa (e.g., sulfate reduction), but other functions are widespread across diverse groups (e.g., photosynthesis). A microbiome may contain both phylogenetic and functional redundancy. Many novel insights on the microbial community composition and organization of plant microbiomes of several crops have come from metagenomic studies using high-throughput sequencing (Edwards et al., 2015; Beckers et al., 2016; Wagner et al., 2016). Metagenomics enables the study of all microorganisms, cultured or not, through the analysis of genomic data obtained directly from an environmental sample, providing knowledge of the species present and information regarding the functionality of microbial communities in their natural habitat. Functional metagenomics has been utilized, with much success, to identify many novel genes, proteins, and secondary metabolites such as antibiotics with industrial, biotechnological, pharmaceutical, and medical relevance (Culligan and Sleator, 2016).
A microbiome may contain both phylogenetic and functional redundancy. Phylogenetic redundancy occurs when multiple OTUs from the same lineage are present in a microbiome, while functional redundancy occurs when multiple OTUs perform the same action (e.g., nitrogen fixation) within a microbiome (Shade and Handelsman, 2012). Phylogenetic redundancy is important for defining the core microbiome, which may buffer the ecological disturbances and enable the recovery of community functions. Several reports on human microbiome indicate that gut microbiome disturbances due to heavy antibiotics are restored due to the redundancy of the core group only (Antonopoulos et al., 2009). It carries relevance in agriculture as different agri-management systems lead to the disturbances in soil microbiome vis-a-vis plant microbiome. Recently, Berg et al. (2021) summarized the effects of microbial inoculants on the indigenous plant microbiome and termed this unexplored mode of action as “microbiome modulation.”
Synthetic microbial community analysis in gnotobiotic systems is a valuable approach to create reproducible conditions to experimentally test microbial interactions in situ. Such systems have been developed for animal and plant models including the well-studied plant Arabidopsis thaliana. With established huge volume of data on the metagenome of different crops, there is a need for its translation to certain tailored microbiome-based solutions for promoting plant growth under a range of environmental conditions and increasing resilience to biotic and abiotic stresses. The genomic data with taxonomic status, habitat compatibility, and functional trait knowledge including metabolic potential of plant microbiome communities can be followed as the approach for designing effective microbial inoculants. Here, based on phylogenetic or functional redundancy, two approaches for synthesizing microbial-communities-based bioinoculants are discussed.
Community-Based SB
Microbial colonization in the plant root rhizosphere is the outcome of the interplay between roots exuding chemical compounds that microbes capture as signals and on which their survival and perpetuance depend. The differential abundance of colonizing microbes and the establishment of core-microbiome-based microbial communities forms the basis for plant–microbe interactions. The core members remain present throughout the development of the crop, which may be joined by other taxa during the crop growth. The metagenome data about the relative abundance of colonizing phyla/taxa and core microbiome in the plant rhizosphere and endosphere form the basis for developing Community-Based SB (CSB). Microbial isolates representing the abundant phyla can be sourced either from the crop associated culture bank or with targeted culturomics, for developing the synthetic community. The isolates are expected to be rich in community-forming characteristics like motility, chemotaxis ability, quorum sensing, metabolic diversity, and others. This approach is a direct microbiome manipulation where inoculated CSB may serve to reduce the time required for the rhizosphere microbiome to achieve niche saturation and competitive exclusion of pathogens (Bakker et al., 2012).
Taye et al. (2020) reported that in field-grown Brassica napus, rhizosphere core genera found at each growth stage were generally part of the overall core taxa at the 75% prevalence threshold. Arthrobacter, Bradyrhizobium, and an unclassified Acidobacteria in the class Ellin6075 were present in all growth stages, while other genera joined at the flowering or harvesting stage, as the recruitment of the microbiome is governed majorly by the host plant. Metagenome analysis of more than 600 Arabidopsis thaliana plants from eight diverse, inbred accessions growing at different locations indicated that the core endophytic microbiome is less diverse than their corresponding rhizosphere soil microbiomes. The soil types influenced the microbial communities in the A. thaliana rhizosphere, but the endophytic communities were overlapping and less complex with maximum of actinobacteria and selected proteobacteria. Lundberg et al. (2012) concluded that the host plants influenced the bacterial colonization in the rhizosphere which varied between inbred lines of Arabidopsis, but in the endophytic compartment, it remained consistent across different soil types. An extensive bacterial culture collection that captures a large part of the natural microbial diversity of healthy A. thaliana plants was established (Bai et al., 2015). Carlström et al. (2019) conducted dropout and late introduction experiments by inoculating A. thaliana with synthetic communities from a resource of 62 native bacterial strains to test how arrival order shapes community structure and indicated that individual Proteobacteria (Sphingomonas and Rhizobium) and Actinobacteria (Microbacterium and Rhodococcus) strains have the greatest potential to affect community structure as keystone species.
Similar influences of maize inbred lines growing in different soils and agri-management systems suggested the substantial variation in α- or β-bacterial diversity and relative abundances of taxa with a small proportion of heritable variation across fields. Despite significant differences between the microbial community profiles of maize inbreeds, the estimated α- and β-diversity could not define the kinship of the 27 maize inbreeds to supplement the diversification history of maize (Peiffer et al., 2013). Edwards et al. (2015) resolved the distinct nature in the microbiomes associated with rhizosphere, rhizoplane, and endosphere of rice roots, influenced by the growing conditions and genotypes.
The functional diversity within microbial communities enables metabolic cooperation toward accomplishing more complex functions than those possibly exhibited by a single organism. The consortium members or communities can communicate by exchanging metabolites or molecular signals to coordinate their activity through temporal and spatial expression and further execution of required functions. In contrast with monocultures, microbial members at the community level can self-organize to form spatial patterns, as observed in biofilms or soil aggregates. This self-organization enables them to adapt to the gradient changes, improve resource interception, and exchange metabolites more effectively (Zhang and Wang, 2016; Ben Said and Or, 2017). Hence, the selection and sourcing of microbial members are very important for the construction of CSBs, and they can be from the microbial communities specific to plant niches like rhizosphere (Huang et al., 2018), endosphere, and phyllosphere (Kong and Glick, 2017). Kong et al. (2018) reviewed the strategies for developing synthetic microbial consortium (SMC) and suggested that the crops with good quality can be a good origin of SMC. Based on next-generation sequencing and network analysis, the core microbes can be isolated from the rhizospheric soils or the plant roots using the web-based platform KOMODO (Known Media Database). Herrera Paredes et al. (2018) designed synthetic bacterial communities based on predominant phyla and demonstrated their effect on developing specific and predictable phenotypes in A. thaliana. Using the plant–bacterium binary-association assays, the effect of bacterial community manipulation was observed on the plant response to phosphate (Pi) starvation. This approach might contribute to microbial communities’ rational design and deployment to improve the host response to biotic and nutritional stresses.
In vitro techniques have demonstrated that the host genotypes and abiotic factors influence the composition of plant microbiomes. At the in vivo level, it is a challenge to define the mechanisms controlling the community dynamicity, its assembly, and the beneficial effects on the plant hosts. In an earlier study, the host-mediated natural selection of bacteria by maize roots was employed to select a simplified synthetic bacterial community consisting of seven strains (Enterobacter cloacae, Stenotrophomonas maltophilia, Ochrobactrum pituitosum, Herbaspirillum frisingense, Pseudomonas putida, Curtobacterium pusillum, and Chryseobacterium indologenes) representing the dominant phyla such as Proteobacteria and Actinobacteria (Niu et al., 2017). By assessing the functional role of these bacterial community combinations using axenic maize seedlings, E. cloacae was identified as the keystone member in this model ecosystem. This model community inhibited the phytopathogenic fungus Fusarium verticillioides, both in vitro and in planta, indicating a stronger benefit to the host plant. The reductionist approaches to disentangle the inherent complexity of microbial communities’ interactions have also been suggested for SynComs to be used as inoculants for a given host to decipher their key functions under the gnotobiotic system (Vorholt et al., 2017). Thus, these recent reports support the strategy of combining unculturable and culturable methods, giving the possibility of assembling a representative, yet simplified, bacterial synthetic communities from the pool of dominant genera present in the system. Figure 3 represents an outline for developing CSB based on the metagenome data and bioinformatic applications for predominant taxa and core microbiome. The key functions for developing such communities are collection of available individual isolates representing predominant taxa or isolating them using culturomic tools. Furthermore, such communities can be strengthened by their ecological interactions and probable functional annotations under gnotobiotic conditions.
Figure 3. Schematic depiction of different steps for the development of microbial community based synthetic bioinoculants (CSB) by employing metagenomic and bioinformatic techniques.
Function-Based SB
Due to high organic matter, soils with dynamic microbial ecologies typically have lower fertilizer requirements than conventionally managed soils (Bender et al., 2016). Focusing on the functional groups of microorganisms rather than on taxonomic relatedness and manipulating their activities (functional pools) in the vicinity of the plant ecosystem have more significant potential for providing nutrients and stress protection requirements of crops. Further exploration into the mechanisms and specificity of plant growth promotion from these key microorganisms will refine their specific use and maximize the potential inherently possessed by the microbiomes of plants or soils (Parnell et al., 2016). As only a limited proportion of microbial diversity is cultured, there is much scope for culturomics to identify, culture, and include important taxa for their beneficial exploitation (Sarhan et al., 2019). Few commercial products have emerged that take advantage of combining different biofertility products. A bacterial consortium Mammoth P™ consisting of Comamonas testosteroni, P. putida, E. cloacae, and Citrobacter freundii has been reported to enhance phosphate mobility and improve crop productivity twofold (Baas et al., 2016). The combined abilities of Bacillus amyloliquefaciens and the filamentous fungus Trichoderma virens marketed under the trade name QuickRoots® (Monsanto BioAgAlliance, 2015), when applied to field corn, show positive yield improvements ranging from 220 to 500 kg ha–1. Similarly, several microbial consortia have been reported to improve host plants’ nutrition (Shukla et al., 2008; Suman et al., 2008; Dal Cortivo et al., 2018). The synthetic microbial community of P. putida KT2440, Sphingomonas sp. OF178, Azospirillum brasilense Sp7, and Acinetobacter sp. EMM02 has been shown to improve drought stress tolerance in maize (Molina-Romero et al., 2017). Two synthetic microbial communities (SynComs 1 and 2) of known antagonistic Bacillus and other isolates from compost-rich soils inhibited Fusarium wilt symptoms and promoted tomato growth (Tsolakidou et al., 2019). Menéndez and Paço (2020) have explored synergies between rhizobial and non-rhizobial bacteria for beneficial effects on different crops. Woo and Pepe (2018) described Trichoderma and Azotobacter as anchorage microorganisms for developing their respective consortia for promoting plant health and mitigating stress conditions. The established arbuscular mycorrhizal fungi (AMF) system, mainly known for P transport, is also a carrier of endophytes in the plant system, can induce systemic resistance to pathogens, and assists in moisture conservation (Cameron et al., 2013; Rouphael et al., 2015). Through the genomic approach of using multiplex amplicon sequencing of the community-based culture collection, Xu et al. (2016) identified the four most representative genera, Bacillus, Chitinophaga, Rhizobium, and Burkholderia, for the development of bioinoculants. Armanhi et al. (2018) gave a novel methodology for developing a PGP community-based culture collection (CBC) from sugarcane microbiomes, particularly roots and stalks. The CBC recovered 399 unique bacteria, representing 15.9% of the rhizosphere core microbiome and 61.6–65.3% of the endophytic core microbiomes of sugarcane stalks. This synthetic community of highly abundant genera was tested for colonization of maize as the test crop. The inoculated synthetic community efficiently colonized plant organs (53.9%) and improved plant biomass production, indicating their beneficial effects. Hence, the steps for designing Function-Based SB (FSB) essentially involve identifying and culturing the core microbes, selecting the microbes for plant growth functions, optimizing the microbial interactions according to their compatibility and suitable conditions, and assessing the efficacy of these FSBs under in vitro and in vivo conditions for the final release of the formulated product for farmers (Figure 4). Therefore, the FSBs can be foreseen as a small subset of the community from the natural existing microbial communities. Although the FSB may be similar to many other microbial consortia used in different crops, the fundamental difference lies in the functional analysis of the microbiome and the subsequent selection and formulation.
Figure 4. Schematic depiction of different steps for the development of microbial Function based Synthetic Bioinoculants (FSB) using functional characteristics of cultured isolates.
Harmony of Bioinoculants With Sustainable Agriculture Goals
The UN framework of the “2030 Agenda” for 17 Sustainable Development Goals (SDGs) has been adopted by the 193 member states to develop their vision, strategy, and targets for achieving SDGs by effectively making them part of their policies. In its sustainability framework to realize the goal of ending hunger (SDG2), India has several initiatives that include the management of soil health. Successful organic cultivation and integrated agriculture will be highly dependent on the efficient microbiome-based bioinoculants for plant nutrient management and, more importantly, the recycling of crop residues for soil health (Vision 2030, DARE, India). In contrast, many other practices affect the abundance of microbial taxa involved in pest and soil disease suppression and nutrient cycling (Lupatini et al., 2017). The importance of microbiome-based solutions is gaining attention in the interrelated systems of environmental management, sustainable food, and fuel production, and human/animal health (FAO, 2019). There is a strong need for integrated research among soil and microbial scientists, growers, extension clienteles, ecologists, and policymakers to develop strategies to preserve and utilize microbial resources for soil health and crop production (Saleem et al., 2019). The microbiome research also leads to a paradigm shift in preserving axenic samples in culture collections to preserving complex communities such as “microbiome biobanks” with their functional perspectives (Ryan et al., 2021). D’Hondt et al. (2021) have summarized the key role of microbiomes in contributing policies interfacing the SDGs globally and emphasized the investments, collaborations, regulatory changes, and public outreach for innovations in microbiome-based bioeconomies.
Conclusion
The sustainability of the modern agriculture system is critical to feed the continuously growing human and animal populations, wherein the guided use of microbiomes has an inevitable role in promoting plant growth, development, productivity, and nutrient value. The current biofertilizers are based on individual bacterial cultures with specific traits such as N fixation or the solubilization of P or K. But with the detailed diversity and functional analyses of plant-associated microorganisms, a better understanding has emerged that the plant-associated microbiomes have a tremendous and so-far untapped potential to improve the acquisition of nutrients and resilience to abiotic and biotic stresses and, ultimately, the crop yields. The options of generating synthetic communities using taxonomy abundance alone or with functionally annotated predominant taxa are now available for the improved use of microbial resources in crop cultivation. Nevertheless, developing any microbial community requires a collection of promising functionally annotated and compatible isolates in hand, rather than only microbiome data. Hence, it will be appropriate to holistically use the knowledge of unculturable microbiome generated through structural and functional genomics tools and culturable approaches to get the common and rare taxa for synthetic community preparations. The rational workflow for developing community and function-based bioinoculant preparations has been described, which can be used for developing formulations with the targeted functions of nutrient supplementation and stress management in sustainable agriculture.
Author Contributions
AS conceptualized and wrote the manuscript. VG helped in the finalization of tables and figures. KAn and BR gave intellectual input and edited the manuscript. KAs, JS, PS, and DP contributed in data search for the content and table formulation. All authors contributed to the article and approved the submitted version.
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s Note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Acknowledgments
For this review formulation, authors acknowledge working in ICAR-IARI project “Integrated crop and resource management for enhanced productivity and profitability” under activity “Inquisition, functional annotation and evaluation of endophytic microflora for improved moisture and temperature stress tolerance” (Project 15610190062/1010512) and the DST-SERB project “Exploring seed microbiome of wheat from varied agro-climatic zones to develop synthetic microbials” (Project CRG/2019/002146). The authors acknowledge the NAHEP-CAAST for funding student work. AS acknowledges Joyce S. Khanuja for the figure drawings and the mentor “FloraFauna” foundation for critical suggestions.
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Keywords: bioinoculants, PGPRs, plant microbial communities, novel biologicals, microbiome
Citation: Suman A, Govindasamy V, Ramakrishnan B, Aswini K, SaiPrasad J, Sharma P, Pathak D and Annapurna K (2022) Microbial Community and Function-Based Synthetic Bioinoculants: A Perspective for Sustainable Agriculture. Front. Microbiol. 12:805498. doi: 10.3389/fmicb.2021.805498
Received: 30 October 2021; Accepted: 29 December 2021;
Published: 11 March 2022.
Edited by:
Prem Lal Kashyap, Indian Institute of Wheat and Barley Research (ICAR), IndiaReviewed by:
Ahmed Elhady, Institute for Epidemiology and Pathogen Diagnostics, Julius Kühn-Institute, GermanyPratiksha Singh, Guangxi University for Nationalities, China
Copyright © 2022 Suman, Govindasamy, Ramakrishnan, Aswini, SaiPrasad, Sharma, Pathak and Annapurna. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Archna Suman, YXJjaHN1bWFuQHlhaG9vLmNvbQ==