Deciphering metabolomics mechanism explaining the role of secondary metabolites as an aid in improving the agronomic traits and tolerance against several stress

doi:10.21203/rs.3.rs-4406625/v1

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Deciphering metabolomics mechanism explaining the role of secondary metabolites as an aid in improving the agronomic traits and tolerance against several stress

https://doi.org/10.21203/rs.3.rs-4406625/v1

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Bacillus pumilus plays an essential role in agricultural applications as a biological control and for biosafety concerns. However, the underlying mechanisms of B. pumilus strains remain unclear. In our previous study, B. pumilus SH-9 was isolated and shown to be a causal agent of drought stress tolerance and enhanced agronomic traits. Bacillus pumilus SH-9 was isolated from the rhizosphere soil of Artemisia vulgaris. NGS (next generation sequencing) was performed for the strain to gain new insights into the molecular mechanisms underlying plant-microbial interactions. NGS revealed 3,910 genes, 3294 genes with protein-coding, and 11 functional genomic regions related to diverse agronomic traits. Several gene clusters related to the biosynthesis of phytohormones, stress tolerance, and agricultural diversification were predicted. The genome provides insights into the possible mechanisms of this bacterium and its future applications. The genomic organization of SH-9 revealed several hallmarks of its plant growth promotion and pathogen suppression activities. Our results provide detailed genomic information for the SH-9 strain and reveal its potential stress tolerance mechanisms, which lays the foundation for the development of effective biocontrol strategies against abiotic stress. Graphical abstract

Biological sciences/Physiology

Biological sciences/Plant sciences

SH-9

NGS

Food security

Secondary metabolites

Host plants harbor a symbiotic relationship with the microbes. Beneficial microbes are important in enhancing the physiological traits and plant stress tolerance against several stresses [1]. The agricultural industry has to face dual stress: one is to meet the needs of the hungry population, and the other is environmental stress. Both biotic and abiotic stress reduce the crop production negatively [2]. However, several conventional approaches are being practiced to enhance agriculture production. Among them, the most recent approach is the application of beneficial microbes in enhancing agronomic traits and stress reticence. Beneficial microbes, especially bacteria and fungi, are known for their Plant growth-promoting potential (PGP) without causing symptoms to the plant cells [3]. They can colonize plants and exert their beneficial effect on plants to facilitate the growth and development of the plant. The promotion of plant growth by beneficial microbes has been observed to be facilitated in several ways, such as the production of secondary metabolites and enzymes, gene modulation, and defense-related constitution in host cells. Moreover, microbes can affect the host by regulating the antioxidant defense system [4, 5].

SH-9 was first isolated from the rhizosphere soil of an arid medicinal plant, A. vulgaris (Pohang Beach, South Korea), and was subsequently found to increase the growth and stress tolerance of rice and soybean. It has been suggested that SH-9 has the ability to induce the production of phytohormones, organic acids, and biofilms [6]. It belongs to the genus Bacillus, and members of the Bacillus genus are rod-shaped and sprout in nature. These are gram-positive, chemoheterotrophic, and aerobic microbes. An increasing trend has been observed in the use of microbes such as Bacillus for abiotic stress tolerance [7]. B. pumilus sp. has been isolated from several different environments; however, only a few reports have described their effect on Plant abiotic stress tolerance [8]. Bacillus sp. have mostly been reported for their roles in various pollutants and the overexpression of metallothionein in host cells, which alleviates heavy metal toxicity in plants [9]. This species can also improve salinity [10], drought [11], and hydrogen peroxide [12] stress by regulating the endogenous phytohormones and antioxidant defense system. In addition, this species can produce bioactive metabolites [13]. Previous studies have suggested that the B. pumilus SH-9 strain can be used for PGP [14].

DNA-based investigations of the microbes are highly valuable in answering the aforementioned queries. The agronomic potential and genetic traits of beneficial microbes can be understood through metabolomics investigations of entire microbial colony genome analyses through NGS. This RNA-based research clarified the detailed mechanism of action and regulatory process of the microbes. NGS technologies are significantly possible to answer previously unanswerable issues, mostly about plant-microbial interaction [15]. Consequently, studying plant-microbe relationships more quickly and thoroughly than ever before is possible [16].

This study was performed to determine the complex biological mechanisms by characterizing and identifying the genomic regions. In addition, candidate genes (with agronomic traits that allow plant-microbial interaction) were identified via genome sequencing. It will provide a platform to understand the complex plant-microbial interaction against environmental stress. It also provides the evolutionary changes within the genus.

Media cultivation and isolation

The B. pumilus SH-9 culture was grown from the original stock archived at the Crop Physiology Laboratory at Kyungpook National University, Daegu, South Korea. The cells from the stock were streaked on L.B. agar plates and incubated at 27°C–30°C until colonies appeared. A single colony was inoculated in 5 mL of L.B. broth and, cultured overnight at 30°C and agitated at 400 rpm. This procedure was followed according to the method described by [17].

DNA extraction and genomic sequencing

Genomic DNA was extracted from 1-mL culture aliquots using the Maxwell 16 DNA/RNA Extraction System (Solgent Company, South Korea). Genomic DNA was extracted for complete genome sequencing using a Qiagen kit (Qiagen, Hilden, Germany). For NGS, the single molecular real-time technique was used by Pacific Bioscience (Pac Bio, Menlo Park, CA, USA). The methodology used was followed according to that described by [18].

Genome annotation

The NCBI prokaryotic genome annotation pipeline (PGA) was used to perform the complete genome annotation. Rapid annotation using subsystem technology version 3.0 and an integrated microbial genome platform were used for the gene prediction. The assembled and annotated sequences were submitted to GenBank with the accession number (ON753949.1), and the information is available online in the Genome online database. The annotation was performed as described by [19].

Genome assembly statistics

NGS was performed at Kyungpook National University, South Korea, and the genome assembly statistics were performed using the build 6494 software. The NGS center at Kyungpook National University, South Korea, provided the annotation. The annotation pipeline used was the NCBI PGA. The adopted annotation methods were the best-placed reference per set and GeneMarkS-2. They provided us with the gene, coding sequence (CDS), rRNA, and tRNA data. The entire protocol was followed as described by [20].

Statistical data analysis

The statistical software SPSS (22.0) for Windows (SPSS, Chicago, IL, USA) was utilized to perform a one-way analysis of variance and the general linear technique on the experimental data. In order to compare mean data and identify treatment differences, Tukey's test (p ≤ 0.05) was employed. Five replicates, on average, were used for each treatment value.

The details of the genomic annotation for the SH-9 strain are presented in Fig. 1. However, the sequence assembly and analysis revealed that B. pumilus SH-9 has a large genome size of 3.7 Mb. This B. pumilus SH-9 strain is a new member of the Baccillaceae family. Its sequence has been submitted to NCBI GenBank with the gene accession number ON753949.1, and the obtained nucleotide sequence can be viewed at https://www.ncbi.nlm.nih.gov/nuccore/ON753949. The partial sequence of SH-9 can be viewed in (Supplementary Fig. 1).

Using the gene accession number and the available close species nucleotide sequences mentioned in supplementary Fig. 1, the phylogenetic tree was constructed using the neighbor-joining method in Mega 11 software. The phylogenetic tree was constructed using 18 nucleotide bases with 1000 bootstrap replications at the 70% cutoff value. The optimum tree is shown in (Fig. 2) When SH-9 was observed under an electron microscope, the shape and presence of some exopolysaccharides were observed. Further analysis of the SH-9 strain genome revealed the total number of genes as well as the available protein genes (Fig. 3A and 3B, respectively).

Gene prediction and annotation summary

To investigate the stress tolerance mechanisms of B. pumilus SH-9, we screened the potential metabolic regions and their corresponding genes. The results revealed that the SH-9 strain contains several coding- and pseudogenes, as shown in Fig. 3. Total genes, CDSs, and protein-coding genes were prevalent with close to 3.8 kb of data, as shown in Fig. 3A. However, the total pseudogenes and CDSs without proteins were prolific. The total RNA genes, rRNA, complete rRNA, tRNA, and ncRNAs were present in insignificant amounts in SH-9, as shown in Fig. 3A. NGS also revealed that it has metabolic regions that produce secondary metabolites. All metabolic regions (n = 11) can enhance plant agronomic traits and stress tolerance via several gene modulations.

The results are shown in Fig. 4. The list of identified genes is presented in Table 1.

Genomic regions associated with agronomic traits

Sequence analysis of the rhizosphere Bacillus sp. SH-9 and its potential for the enhancement of plant growth. A genomic area has a biological function if it has reproducible biochemical activity, such as transcriptional activity or certain chromatin states, which can be observed. In Fig. 5 functional genomic regions of the SH-9 strain, production of secondary metabolites and the total number of metabolic regions in the SH-9 strain genome were shown. NGS has been extensively used in recent years to identify genomic regions and candidate genes for agronomic traits in microbes, and its crosstalk has several diversification qualities [21, 22]. Numerous candidate genes and quantitative regions are associated with agronomic traits [23].In Table 2. agronomic traits were shown. This study revealed that SH-9 has 11 functional genomic regions, as shown in Table 1. At genomic region 1, non-ribosomal peptides (NRPs) 64,076–139,868 and type 1 polyketides (TIPKS) were found with 22% similarity to the known cluster of Zwittermicin A. These are a class of secondary peptide metabolites. These are extraordinarily diverse and have various biological and pharmacological features. They are frequently responsible for siderophore and pigment production in plants and also act as a biocontrol agent against plant stress [24, 25]. Similarly, in region 11, they contain NRPs, which has 85% similarity with Lichenysin.

In terms of both structure and biological function, TIPKS represent a diverse class of chemicals. These substances, which include macrolides, polyethers, polyols, and aromatics, are frequently strongly oxygenated. They have various biological effects, including antibacterial, anticancer, antifungal, antiphrastic, and immunosuppressive [26, 27]. Polyketides are present in genomic region 1. The genomics region 2 contains the Rev response element (RRE) nucleotides from 323,310–344,032. This is a specialized and cooperative complex of Revs, and the cellular export machinery utilizes RRE as a scaffolding platform for assembly. Creating a high-affinity, export-competent complex depends on the cooperativity that is governed by the RRE structure and sequence [28].

At genomic region 3, terpene NI siderophores were found from 490,298–518,868, which has a 60% similarity with Schizokinenn. Because of their diverse properties, terpenes are essential natural compounds that are important for pollination, fragrance, and biological control. Terpenes are also precursors of gibberellic acid (GA). This genomic region is important because GA is produced here. GA is an important phytohormone that is responsible for the elongation of cells and, ultimately, the growth of plants [29, 30]. Similarly, in the genomic region 5, the production of terpenes was also found. From this region, siderophores are secreted, which can induce iron chelation [31].

At genomic regions 4 and 7, betalactone is produced with a 53% similarity to fungicide. It acts as a potent, irreversible antagonist of strigolactone receptors. When the Plant is exposed to stressful conditions, betalactone works antagonistically to inhibit branching [32].

At genomic region 8, ribosomal synthesized and post-translationally modified peptides (RiPPs) are abundant from 2,720,609–2,730,899. These diverse peptide classes are responsible for several biological translation processes and their post-modification in response to stress [33, 34].

In genomic region 10, NRPS metallophores are present from 3,030,569–3,079,137, which shows an 80% similarity with bacilibactin. This diverse class of microbes can chelate metals and be used for heavy metal stress tolerance [35, 36].

Metabolic regions and their potential to enhance agronomic traits

Reactive oxygen species (ROS) accumulation is enhanced in plants in response to stress conditions, such as oxidative stress. Metabolic reprogramming is performed to reduce stress (Baxter[37, 38]. However, it is challenging to cope with stress when the duration of stress increases and metabolic reprogramming fails. In this scenario, beneficial microbes produce several secondary metabolites. In this study, SH-9 was screened by NGS for the production of secondary metabolites, and the results revealed that in metabolic region one, T1PKS is produced, which can lower oxidative stress and work as an antioxidant. T1PKS also works as an antimicrobial agent. Several studies have suggested that T1PKS has the potential to lower ROS levels, and our results are in agreement that it can lower oxidation stress.

In metabolic region 6, type 3 polyketides are present that can activate the TCA cycle. One of the intermediary steps of cellular respiration is the Krebs cycle. Carbohydrates are a group of substrates in which some energy is generated by oxidizing acetyl-CoA and is also obtained by breaking down respiratory substrates such as fats and proteins.

In metabolic region 10, a metallophone is present that remediates heavy metal stress tolerance. In regions 8 and 10, RiPP and NRPS are present, and they are involved in several metabolic and enzymatic processes in plant cells.

Metabolic region 5 is important because it contains terpenes, which are important secondary metabolites. Terpenes are converted into diterpenoids and triterpenoids, which are subsequently converted into xanthroin, a precursor of abscisic acid (ABA). Diterpenoid also converts into geranyl diphosphate, which produces gibberellins. ABA and GA are important phytohormones that enhance stress tolerance and improve plant growth even under stressed conditions [39].

Higher plants are sessile and are exposed to stress throughout their lives. The plant uses several cellular events to protect itself in response to this stress (biotic and abiotic). All plants adopt nonspecific strategies, depending on the stress and duration. However, the general mechanism produces ROS and activates the antioxidant defense system [40]. The ROS acts as a signaling molecule that initiates several metabolic processes in plants to combat stress, such as the production of phytohormones, secondary metabolites, activation of some genes and modulation in physio-biochemical processes. However, plants activate their metabolic reprogramming to alleviate stress, but it is up to a certain limit [41]. After, a specific limit, the plant shows some symptoms of stress. Several techniques are being practiced, such as breeding techniques, agrochemicals, intercropping, and application of plant growth regulators and phytohormones. Bio stimulants are getting more attention because of their eco-friendliness and minimal side effects. The application of beneficial microbes is a promising food and energy security approach. Beneficial microbes induce the plant microbial interaction. Plant-microbial interaction facilitates plants' biological processes and improves plant stress tolerance [42].

Several recent studies significantly impacted plant growth and stress tolerance capacities. Recently, our research team conducted experimental work on beneficial microbes (SH-9) and showed excellent results regarding plant growth promotion and stress tolerance capacities [43]. The results gave us the idea to unravel the hidden mechanism of plant-microbial interaction. In the present study, we did the next-generation sequencing of the microbe SH-9. The results showed that in response to stress, the SH-9 genome encodes several genes that protect against stress. Different genomic regions are responsible for different stress conditions from different genomic regions. The NGS study revealed the presence of 3910 genes with 11 functional genomic regions. A genomic region is the presence of a functional component within the gene responsible for some specific function.

Whenever a plant is exposed to stress, there is a rapid accumulation of ROS that enhances the oxidative stress. Oxidative stress increases the oxidation burst that impedes the damage to the cellular organelles [44]. In response to oxidative stress, the SH-9 genome encodes ten genes at different regions, namely cdr, rnr, resE, rapA-5, qoxb, ychF, ggt, cyPB, adhA-2, and fhs, to regulate the oxidative stress. The presence of these genes further confirms that SH-9 significantly counteracts the generation of ROS. These findings suggest that the strong antioxidative mechanisms of SH-9 alleviate the oxidative onslaught.

Four genes, namely rnr, Sa1A, SrfAB-1, and g1tA, are found in the genome of SH-9 and are responsible for abiotic stress tolerance. Abiotic stress is a most common phenomenon that limits plant production. Abiotic stress reduces the global yield of plants to 70%. The presence of metabolic regions that contain the genes that enhance abiotic stress tolerance is a vital characteristic of beneficial microbes [45]. The presence of these genes on the SH-9 plasmid is surprising. This is a promising approach toward stress tolerance and a potentially profitable approach to enhancing plant agronomic traits.

Iron and magnesium are important micronutrients required for Plant's physiological growth. Under nutritional or other stressed conditions, the plant faces iron and magnesium deficiency [46]. Therefore, to cope with this stress, the plasmid of the SH-9 genome encodes for the genes uxaA, dos, and FadF that can bind iron and magnesium. Therefore, it is an essential character of the beneficial microbe to encode the relevant genes that enhance their solublisation. In plant-microbial interactions, biofilm plays a substantial role in facilitating the interaction and alleviating plant stress. Biofilm acts as an interacting medium for plant-microbial interaction. It enhances the plant growth promotion and production. It also facilitates several biochemical processes [47, 48]. SH-9 encodes for the gene estA to facilitate this mutualistic interaction, which produces glycolipids. Phosphorus is another major molecule that is involved in plant growth and production [49]. The genome of SH-9 encodes for the six genes Dxs, resE, tagF, SasA-1, CarB-1, and CarB-2 that aid in phosphate solubilization. An important plant growth-promoting trait enhances plant growth and regulation. Microbes can convert insoluble phosphorus to soluble phosphorus and improve plant phosphorus nutrition.

Secondary metabolites are important compounds that are produced in response to stress.That enhances plant growth and improves stress tolerance [50]. The SH-9 genome also encodes the genes that facilitate metabolite transportation where they are needed. The SH-9 genome encodes for the six genes Csbc, YYCB-1, fruA-1, mdtc, YdfJ, and CYPB, which facilitate the metabolite transportation system. In response to stress, plant-microbial interactions produce several secondary metabolites, such as glycine, betaine, and proline [39]. These genes are responsible for enhancing the ease of transportation. The SH-9 genome encodes BgIF-1 and mainly acts as a signaling molecule to initiate mutualistic interaction with plant microbes. Signaling molecules act as mainstream to transmit information between microbes and plant cells, activating the cascades of events such as metabolomics expression corresponding to the stress tolerance mechanism [51].

Moreover, the nuclease process is also fundamental in bringing the genetic stability that is being incorporated due to the stress, i.e., oxidation stress.[52] Under oxidation stress, the entire genetic modulation impairs plant cells' cellular function. The SH-9 genome also encodes for ten genes rnr, leus, va1S, cdr, resE, Sa1A, YhaN, addB, addA2, and ctaD that are directly involved in the nuclease process (DNA and RNA) and improve the genetic stability.

The two most important genes that are encoded by the SH-9 genome are dxs and Acsa-1, which modulate plant phytohormones. Phytohormones are essential for stress tolerance and in several biological processes in plants. Genomic regions 3 and 5 are the most important and responsible for the production of phytohormones. Phytohormones reduce the plant stress and improve the plant production. In genomic regions 3 and 5, terpene has been reported as a major precursor of GA and ABA [41]. ABA is an important phytohormones that acts as a signaling molecule in response to stress. In addition, it is a versatile hormone that has a role in the stomatal closure in response to stress and reserves the plant activity to combat the level of stress. Moreover, it also has several functions in the physiological process of plants. Gibberellic acid is also an important class of phytohormones that stimulates plant growth, organ development, and cell proliferation [53]. Our results confirmed that the genome of SH-9 encodes the genes that are liable to respond to stress and improve plant productivity. The results of genomic sequencing and the proposed stress tolerance mechanism are given in graphical abstract.

The present study utilized NGS to obtain a comprehensive view of the mechanisms of the B. pumilus SH-9 strain and the functional diversity that is associated with stress tolerance and improving agronomic traits. The results revealed that SH-9 genome encodes the 3910 genes at 11 different genomic regions that are responsible for agronomical traits and stress tolerance via plant microbial interaction.

NGS

next generation sequencing

NRP

non-ribosomal peptide

TIPKS

type 1 polyketides

T3PKS

type 3 polyketides

RRE

Rev response element

RiPP

ribosomal synthesized and post-translationally modified peptide

Competing interests

The authors declare that they have no competing interests.

Author Contribution

Shifa Shaffique conceptualize and write the original draft as the part of her project brain Korea BK21,4TH phase . Dr. Anis ali shah did the critical review editing. Shankarappa Sridhara reviewed the manuscript. Sang –Mo kang and peter odonkara did the software manipulation. Prof In-Jung Lee validated the results and supervised the entire project.Hosam O. Elansary, Shankarappa Sridhara are contributed, data interpretation, study design, manuscript editing and ensured the accuracy and integrity of the research.

Acknowledgments

This study was supported by the NRF (National Research Foundation) of Korea grant funded by the Korean Government (MIST) No. 2022R1A2C1008993. The authors extend their appreciation to the Researchers Supporting Project number (RSP2024R118) of King Saud University, Riyadh, Saudi Arabia.

Data Availability

The datasets used and/or analyzed during the current study available from the corresponding author on reasonable request.

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Table 1 and 2 are available in the Supplementary Files section.

No competing interests reported.

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Deciphering metabolomics mechanism explaining the role of secondary metabolites as an aid in improving the agronomic traits and tolerance against several stress

Status:

Version 1

Abstract

Figures

Introduction

Materials and methods

Media cultivation and isolation

DNA extraction and genomic sequencing

Genome annotation

Genome assembly statistics

Statistical data analysis

Results

Gene prediction and annotation summary

Genomic regions associated with agronomic traits

Metabolic regions and their potential to enhance agronomic traits

Discussion

Conclusion

Abbreviations

Declarations

Competing interests

Author Contribution

Acknowledgments

Data Availability

References

Tables

Additional Declarations

Supplementary Files

Status:

Version 1