Next Article in Journal
Comparative Study of Mycobacterium bovis and Mycobacterium avium subsp. paratuberculosis In Vitro Infection in Bovine Bone Marrow Derived Macrophages: Preliminary Results
Previous Article in Journal
Select Cover Crop Residue and Soil Microbiomes Contribute to Suppression of Fusarium Root and Crown Rot in Barley and Soybean
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Microorganisms
Volume 12
Issue 2
10.3390/microorganisms12020405
microorganisms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Fungal-Bacterial Combinations in Plant Health under Stress: Physiological and Biochemical Characteristics of the Filamentous Fungus Serendipita indica and the Actinobacterium Zhihengliuella sp. ISTPL4 under In Vitro Arsenic Stress

by
Neha Sharma
1,
Monika Koul
2,
Naveen Chandra Joshi
1,
Laurent Dufossé
3,* and
Arti Mishra
2,4,*
1
Amity Institute of Microbial Technology, Amity University, Noida 201313, India
2
Department of Botany, Hansraj College, University of Delhi, Delhi 110007, India
3
Chemistry and Biotechnology of Natural Products, CHEMBIOPRO, Université de La Réunion, ESIROI Agroalimentaire, 15 Avenue René Cassin, CS 92003, CEDEX 9, F-97744 Saint-Denis, France
4
Umeå Plant Science Center, Department of Plant Physiology, Umeå University, 90187 Umeå, Sweden
*
Authors to whom correspondence should be addressed.
Microorganisms 2024, 12(2), 405; https://doi.org/10.3390/microorganisms12020405
Submission received: 12 January 2024 / Revised: 1 February 2024 / Accepted: 6 February 2024 / Published: 17 February 2024
(This article belongs to the Section Microbial Biotechnology)
Browse Figures
Versions Notes

Abstract

:
Fungal-bacterial combinations have a significant role in increasing and improving plant health under various stress conditions. Metabolites secreted by fungi and bacteria play an important role in this process. Our study emphasizes the significance of secondary metabolites secreted by the fungus Serendipita indica alone and by an actinobacterium Zhihengliuella sp. ISTPL4 under normal growth conditions and arsenic (As) stress condition. Here, we evaluated the arsenic tolerance ability of S. indica alone and in combination with Z. sp. ISTPL4 under in vitro conditions. The growth of S. indica and Z. sp. ISTPL4 was measured in varying concentrations of arsenic and the effect of arsenic on spore size and morphology of S. indica was determined using confocal microscopy and scanning electron microscopy. The metabolomics study indicated that S. indica alone in normal growth conditions and under As stress released pentadecanoic acid, glycerol tricaprylate, L-proline and cyclo(L-prolyl-L-valine). Similarly, d-Ribose, 2-deoxy-bis(thioheptyl)-dithioacetal were secreted by a combination of S. indica and Z. sp. ISTPL4. Confocal studies revealed that spore size of S. indica decreased by 18% at 1.9 mM and by 15% when in combination with Z. sp. ISTPL4 at a 2.4 mM concentration of As. Arsenic above this concentration resulted in spore degeneration and hyphae fragmentation. Scanning electron microscopy (SEM) results indicated an increased spore size of S. indica in the presence of Z. sp. ISTPL4 (18 ± 0.75 µm) compared to S. indica alone (14 ± 0.24 µm) under normal growth conditions. Our study concluded that the suggested combination of microbial consortium can be used to increase sustainable agriculture by combating biotic as well as abiotic stress. This is because the metabolites released by the microbial combination display antifungal and antibacterial properties. The metabolites, besides evading stress, also confer other survival strategies. Therefore, the choice of consortia and combination partners is important and can help in developing strategies for coping with As stress.

1. Introduction

Various anthropogenic activities such as mining, modern agricultural practices, and industrialization have had long-term harmful impacts on the environment [1]. These factors are responsible for increasing the concentration of heavy metals in soil and water, thus leading to several environmental issues. Arsenic (As) is a highly toxic heavy metal that poses risk to millions of people worldwide [2]. Arsenic contamination in drinking water and groundwater used for irrigation is a global problem that not only affects agricultural productivity but also the ecosystem, as As uptake occurs in plant roots and is further translocated to different plant tissues, including the edible parts, and therefore enters the ecosystem through the food chain [3]. Arsenite and arsenate are the two forms of arsenic, arsenite being more toxic. Roots are the prime site of arsenic exposure; thus root proliferation and extension are affected the most. The translocation of arsenic occurs from root to shoot, and the uptake in the aerial parts affects plant growth and reproduction by inhibiting cell division [4]. Therefore, it is essential to remove these heavy metals from the contaminated soil used for growing crop plants.
Microbes including fungal and bacterial species have the potential to cope with heavy metal stress. These microbes also aid in the growth and development of plants by increasing nutrient absorption and assimilation [5]. Microbes release various molecules including siderophores, extracellular polysaccharides, ammonia, and secondary metabolites that help plants to cope with biotic and abiotic stress [6]. Secondary metabolites are chemical substances that protect plants under stress conditions. They are not directly involved in plant growth and development but indirectly boost plant growth by acting as effective defense agents against various phytopathogens. They also help in scavenging free radicals generated during oxidative stress in plants [7].
Metabolites secreted by bacteria and fungi in the rhizosphere are not directly connected with plant growth and reproduction but they participate in rhizosphere ecological interactions [8]. Lipopeptides, phytohormones, their precursors, antimicrobial peptides, siderophores, metallothioneins, and volatile organic compounds are some examples of secondary metabolites released by the microbes [9]. Secondary metabolites, such as acyl-homoserine lactone (acyl-HSL), that act as autoinducer signaling molecules and help in cell-to-cell communication and crosstalk are also secreted by some microbes. Siderophores are some other secondary metabolites released by microbes that help in iron uptake from surroundings. Siderophores-releasing microbes help in iron uptake by the plants also [9]. Other metabolites including metallothioneins are also secreted by various microbes and plants. These are the chelating molecules that help in heavy metal detoxification [10]. These metallothioneins have tiny cysteine-rich proteins which bind with heavy metals thereby helping in metal storage and detoxification. These metallothioneins are mostly released in the presence of heavy metals such as Cd2+, Hg2+, Pb2+ and Ar.
In this study, we studied various secondary metabolites released by S. indica alone and with Zhihengliuella sp. ISTPL4 under normal growth conditions and under arsenic stress. S. indica is an endophytic fungus that boosts plant growth by colonizing the roots of various plants and confers resistance against abiotic and biotic stress conditions [11,12,13]. Zhihengliuella sp. ISTPL4 is an actinobacterium, isolated from Pangong Lake, Ladakh, Jammu and Kashmir, India. The interaction between Zhihengliuella sp. ISTPL4 and S. indica has been previously reported in a systemic study [14]. The role of this microbial combination has also been deciphered in plant growth promotion. In the present study, we checked the significance of secondary metabolites secreted by a combination of S. indica and Z. sp. ISTPL4 and found out which metabolites are released in response to combined microbial treatments.

2. Materials and Methods

2.1. Microbe Culture and Conditions

The fungal disc of S. indica was inoculated into Hill and Kaefer agar plates and incubated for 14 days at 28–30 °C (with an agitation rate of 120 rpm for broth). Similarly, S. indica growth was also assessed in combination with Z. sp. ISTPL4. Bacterial culture was streaked around the periphery after five days of fungal inoculation (5 dafi) [15].

2.2. Effect of Arsenic on Fungal Growth

The arsenic tolerance capability of S. indica was checked individually as well as in combination under in vitro conditions. The concentration of arsenic used was up to 2.4 mM [16]. Dry cell weight of S. indica alone and in combination was estimated (control and treated cultures) to check the effect of arsenic on the growth of S. indica [14].

2.3. Spore Morphology

To study spore morphology SEM studies were carried out for S. indica alone and in combination with Z. sp. ISTPL4. A section of fungal discs was fixed in 2.5% glutaraldehyde (control and interaction plates) followed by incubation at room temperature (RT) for 1 h. After this, samples were centrifuged at 5000 rpm for 5 min followed by washing with 0.1 M phosphate buffer (pH 7) followed by centrifugation. The resulting pellet was dissolved in 0.1% filter sterilized silver nitrate (AgNO3) solution and then incubated for an hour at RT. Samples were gradually dehydrated in a series of ethanol from 30–90% for 15 min. The final step was repeated three times in 100% ethanol for 5 min each. Resulting samples were dehydrated, air dried and placed in aluminum double adhesive carbon conductive tape gold-coated specimens in a Quorum Q150ES coater and then observed under a scanning electron microscope (model Zeiss EVO 18; Raipur, India) [14].
Confocal microscopy was also carried out to check spore size and spore morphology of S. indica alone and in combination with Z. sp. ISTPL4 under normal growth conditions and under As stress. Spore isolation was done by adding 1 mL of a 0.02% autoclaved Tween 20 on freshly grown cultures of S. indica alone and with Z. sp. ISTPL4 (control and As-exposed plates) followed by gentle scraping and centrifugation at 5000 rpm for 10–15 min. The pellet was mixed with autoclaved distilled water, a spore count was conducted, and their concentration was maintained at 4.8 × 105 spores/mL. The resulting sample was analyzed under a Nikon confocal microscope (Model: Nikon A1) at 60× magnification by using NIS Elements software version 4.6 (Nikon, Tokyo, Japan) (Amity Institute of Microbial Technology, Amity University, Noida, India) [17].

2.4. Biotransformation of Arsenic

The arsenic oxido-reduction potential of S. indica and Z. sp. ISTPL4 was determined. For this, nutrient agar was supplemented with 500 ppm of As (V) and the fungal disc was inoculated followed by an incubation of 15 days at 28 ± 2 °C. Spot inoculation of Z. sp. ISTPL4 was conducted, and the bacterial culture was kept for incubation at 37 °C for 72 h. After fungal and bacterial growth, 100 µL AgNO3 (0.1 M) solution was flooded over the grown fungal and bacterial plates and a change in color was observed [18].

2.5. Gas Chromatography and Mass Spectroscopy Analysis (GC-MS)

GC-MS analysis was performed for the secondary metabolic profiling in S. indica alone and in combination with Z. sp. ISTPL4 under normal growth conditions and in the presence of arsenic stress. The fungal disc was inoculated in H and K broth and then kept for incubation for 2 weeks. A similar protocol was followed for the combined growth of S. indica and Z. sp. ISTPL4. The bacterial culture was inoculated in H and K broth after 5 days of fungal inoculation (5 dafi) followed by incubation (2 weeks). A 100 mL sample was taken and then centrifuged at 9000 rpm for 10 min. The supernatant was collected and mixed with an equal volume of ethyl acetate. The resulting solution was shaken for 3 h. The sample was then concentrated on a rotatory evaporator. The final volume was mixed with methanol. This concentrated sample was used for GC-MS analysis for secondary metabolite detection.
GC-MS analysis was carried out in a Perkin-Elmer GC Clarus 500 system, which included an Elite-5MS (5% diphenyl/95% dimethyl poly siloxane) fused capillary column (30 × 0.25 μm ID × 0.25 μm df) and an AOC-20i auto-sampler and Gas Chromatograph interfaced to a Mass Spectrometer (GC-MS). An electron ionization device with an ionization energy of 70 eV was used in electron impact mode for GC-MS detection. A split ratio of 10:1 was used with an injection volume of 2 μL and helium gas (99.999%) was used as the carrier gas at a steady flow rate of 1 mL/min. The temperature of the ion source was 200 °C, the injector was kept at 250 °C, and the oven was set at 110 °C (isothermal for two minutes) which was further increased by 10 °C/min to 200 °C, and 5 °C/min to 280 °C, and stopped with a 9-min isothermal at 280 °C. Mass spectra with fragments from 45 to 450 Da and a scan interval of 0.5 s were obtained at 70 eV. The GC-MS was run for 36 min, with a solvent delay of 0 to 2 min. By comparing the average peak area of each component to the total areas, the relative percentage amount was determined. The Turbo-Mass ver-5.2 software was utilized to handle mass spectra and chromatograms. Metabolite identification, retention time (R.T.) and mass to charge ratio (m/z) was analyzed as listed in the NIST library [19,20,21].

2.6. Clustered Heatmap of Metabolites

A heatmap of common metabolites secreted by the individual culture of S. indica as well as in combination with Z. sp. ISTPL4 under normal growth conditions and in the presence of As stress was prepared by versatile matrix visualization and analysis software (https://software.broadinstitute.org/morpheus/ (accessed on 1 June 2022)).

2.7. Statistical Method

The experiments were repeated five times. Statistical analysis was conducted utilizing two-way ANOVA and student’s t test (p < 0.05) using online OPSTAT software (version 6.8). All the variables were subjected to statistical analysis.

3. Results

3.1. Microbial Conditions

The growth of S. indica was checked alone and with Z. sp. ISTPL4 by measuring the hyphal radius and spore size was measured using scanning electron microscopy (Figure 1a–d). S. indica growth was assessed under varying concentrations of As and it was observed that S. indica was able to survive at 1.9 mM concentration (Figure 2). Growth of S. indica under normal conditions was (3.1 ± 0.025 cm) and it decreased up to (1.6 ± 0.01 cm) at 1.9 mM As concentration. S. indica growth was assessed in combination with Z. sp. ISTPL4. S. indica when grown in combination with Z. sp. ISTPL4 was able to grow at 2.4 mM concentration. The hyphal radius of S. indica was (2.9 ± 0.01 cm) when grown with Z. sp. ISTPL4 under normal growth conditions and it reduced (1.4 ± 0.03 cm) in the presence of As (Figure 2a–d).
The dry cell weight of S. indica alone as well as in combination with Z. sp. ISTPL4 was measured in the control as well as in the presence of As. The dry cell weight of S. indica was 69% higher than dry cell weight of S. indica under As stress. Similarly, dry cell weight of combination of S. indica and Z. sp. ISTPL4 was 51% more than the dry cell weight of the combination of S. indica and Z. sp. ISTPL4 under arsenic stress (Figure 2e).

3.2. Spore Morphology

Increased spore size of S. indica was observed in the presence of Z. sp. ISTPL4 (18 ± 0.75 µm) as compared to its individual culture (14 ± 0.24 µm) under normal growth conditions and confocal microscopy under normal growth conditions in scanning electron microscopy (Figure 1c–d). The spore size of S. indica decreased by 18% at 1.9 mM concentration and by 15% when used in combination with Z. sp. ISTPL4 at 2.4 mM concentration of As as observed under a confocal microscope. Increase in concentration beyond this resulted in spore degeneration and hyphae fragmentation (Figure 3a–d). The spore count was also decreased at higher concentration of arsenic. It was 4.59 × 105 spores/mL in S. indica under normal growth conditions and it reduced to 3.68 × 103 spores/mL at 1.9 mM concentration of arsenic. Similarly, the spore count of S. indica was slightly higher 4.65 × 105 spores/mL, when it was grown in presence of Z. sp. ISTPL4 and at 2.4 mM concentration, it decreased to 4 × 103 spores/mL.

3.3. Biotransformation of Arsenic

The biotransformation potential of S. indica and Z. sp. ISTPL4 was checked on the basis of the color change of fungal and bacterial cultures. Color change to brown in fungal cultures indicated transformation ability of As (V) (arsenate) to As (III) (arsenite). The ability of the fungal strain to bring conversion was discovered after 72 h of incubating fungal and bacterial plates. Contact of silver nitrate with As (V) (already present in media) produced a brownish precipitate, while the association with As (III) produced a pale yellow precipitate. The results of the arsenic transformation ability of S. indica indicated brown color formation which denotes that this fungus has certain genes which are involved in arsenic transformation. Z. sp. ISTPL4 revealed no change in color which indicated no conversion of arsenic to other forms (Figure 4a–d).

3.4. Production of Secondary Metabolites

Secondary metabolite production in S. indica alone as well as in combination with Z. sp. ISTPL4 was checked under normal growth conditions and under As stress (Figure 5a,b). GC-MS studies revealed the presence of 69 metabolites secreted by S. indica under normal conditions and 47 metabolites under As stress. Among these metabolites, 23 metabolites are common including 2,4-Di-tert-butylphenol having a retention time of 12.910 and molecular weight 206, 1,2-Benzenedicarboxylic acid with a retention time of 17.125 and molecular weight of 278, respectively (Table 1). 2-Ethylbutyric acid, eicosyl ester, 2-hydroxy-1(hydroxtmethyl)ethyl ester, Octocrylene 2-propenoic acid and Squalene e 2,6,10,14,18,22- Tetracosahaxaene are some of the metabolites secreted by culture of S. indica alone and under arsenic stress. A total of 67 metabolites were secreted by the combination of S. indica and Z. sp. ISTPL4 under normal conditions, and 37 metabolites were secreted under arsenic stress (Figure 6a,b). Similarly, 16 metabolites were common including Cyclo(L-prolyl-L-valine), hexahydro-3-(2-methylpropyl), Eicosane, 2,4-Di-tert-butylphenol, L-Proline and Heneicosane (Table 1). All these metabolites are involved in antibacterial, antifungal, and antioxidant activities while some of them have important roles in plant growth promotion under various environmental conditions. These metabolites are also represented in the form of venn diagram (Figure 7a,b). Figure 8 shows the clustered heatmap of the secondary metabolites. These metabolites include volatile organic compounds (VOCs), hydrocarbons, amino acids, fatty acids and vitamins. Hierarchical clustering analysis (HCA) shows the comparison of common metabolites based on the area percentage detected. A heatmap ranging from red (high) to blue (low) denoted the concentration of each metabolite detected. The numerical data of metabolites were normalized to allow for clustering and color scaling based on the concentration of compounds. In Figure 8a, compounds that appeared as red were considered highly abundant, and Figure 8b showed that an equal ratio of red and blue colored compounds appeared.

4. Discussion

Microorganisms release various secondary metabolites to cope with abiotic stress resulting in better plant growth performance, increased photosynthesis, and the production of antioxidants [21]. Besides bacteria, fungal species also confer abiotic stress tolerance in plants by helping them to adapt to a variety of conditions, such as heat, salinity, cold, drought, and toxic metals [22]. Fusarium culmorum, Azotobacter, Pseudomonas, Curvularia protuberata, Piriformospora indica, Neotyphodium lolii, and Trichoderma have all been documented to confer abiotic stress tolerance [23]. Among these, S. indica is a plant-growth-promoting root endophytic fungus. It plays an important role in defending plants from adverse biotic and abiotic factors [24,25]. The role of various secondary metabolites secreted by S. indica alone and in combination with Z. sp. ISTPL4 was studied in the present study. S. indica growth was also checked in the presence of arsenic individually and in combination with Z. sp. ISTPL4. It was reported that S. indica was able to grow up to 1.9 mM and up to 2.4 mM in combination with Z. sp. ISTPL4 in the culture conditions. Mohd et al. (2017) studied P. indica growth under arsenite (III) and arsenate (V) stress and observed a reduction in the growth of fungus at higher As concentrations [16]. The spore morphology and size of S. indica alone and in combination was also assessed under control conditions and in As stress. It was observed that the hyphae and spores were intact at 1.9 mM As concentration and hyphae started fragmenting and spores degenerated beyond 1.9 mM concentration of As in S. indica alone. Similarly, spore size and morphology of S. indica in combination with Z. sp. ISTPL4 was observed in up to 2.4 mM concentration of arsenic. The morphology of S. indica spores was also checked in the presence of Cd by Dabral et al. 2019. It was observed that spore germination inhibited beyond a 0.1 mM concentration of Cd [26].
An Increase of 69% in dry cell weight was observed in S. indica when compared with dry cell weight of S. indica under arsenic stress. Similarly, the dry cell weight of the combined culture of S. indica and Z. sp. ISTPL4 was 51% more than a combined culture of S. indica and Z. sp. ISTPL4 under arsenic stress. The spore morphology of S. indica was also checked under normal conditions and in arsenic stress by confocal microscopy. It was observed that the spore degenerated beyond a 1.9 mM concentration of arsenic and beyond 2.4 mM in the microbial combination of S. indica and Z. sp. ISTPL4. The results of the spore count of S. indica under arsenic stress was measured which indicated a reduction in spore count to 3.68 × 103 spores/mL at 1.9 mM concentration compared to the control (4.59 × 105 spores/mL). The spore count of S. indica in the presence of Z. sp. ISTPL4 was also measured, which indicated an increased spore count (4.65 × 105 spores/mL) under normal growth conditions, and it was reduced to 4 × 103 spores/mL. The spore germination and spore size of S. indica alone as well as in the presence of Z. sp. ISTPL4 was also determined under normal growth conditions which indicated an increased spore size and germination of S. indica in the presence of Z. sp. ISTPL4 than its respective control (S. indica) [14].
The arsenic biotransformation ability of S. indica and Z. sp. ISTPL4 was confirmed. The results of arsenic biotransformation in S. indica indicated the formation of a brown-colored precipitate (Figure 4), which indicated the conversion of arsenate (v) to arsenite (III). Mohd et al. (2017) also reported the bioaccumulation and biotransformation ability of S. indica under arsenic stress [16]. In the case of Z. sp. ISTPL4, there was no change in color observed but the findings of whole genome sequencing indicated the presence of arsenic-resistant genes in Z. sp. ISTPL4 [18,27].
In this study, we reported the significance of various metabolites secreted by S. indica alone and in combination with Z. sp. ISTPL4 under normal and in arsenic stress. These metabolites regulate plant growth and development under stress conditions by acting as antioxidants which scavenge free radicals generated in plants during oxidative stress [28,29]. A total of 69 metabolites were produced in S. indica under normal conditions and 47 metabolites were produced in As stress (Supplementary File S3). Among all the metabolites analyzed, 23 metabolites were common (Table 1). These metabolites include 1,2-Benzenedicarboxylic acid, 2-ethylbutyric acid, eicosyl ester, Octocrylene 2-propenoic acid, squalene 2,6,10,14,18,22-Tetracosahaxaene, phenol and, 2,4-bis(1,1-dimwthylethyl)-phosphite. The chromatogram of each metabolite has been shown in Supplementary Files S1 and S4. Similarly, 67 metabolites were secreted by a combination of S. indica and Z. sp. ISTPL4 under normal conditions and 37 metabolites were secreted by a combination of S. indica and Z. sp. ISTPL4 under arsenic stress (Supplementary File S4). Among them, 16 metabolites were common including Cyclo(L-prolyl-L-valine), hexa hydro-3-(2-methylpropyl), Eicosane, 2,4-Di-tert-butylphenol, methyl ester, Methyl stearate and L-Proline (Table 1). These metabolites have different functions such as antifungal activities, antimicrobial activities, and antioxidant activities [28,29,30]. Some of these metabolite such as glycine, Quinoline-4-carboxamide 2-phenyl-N-n.-octyl are antimicrobial and reduces stress in plants [31,32]. Other metabolites including Dodecane, 4,6-dimethyl, Tetradecane, I-Hexadecanol, Nonadecane and, Heneicosane were also identified in the individual culture of S. indica. Similarly, 5-Azacytosine, N,N,O-trimethyl, 5-Nitroso-2,4,6-triaminopyrimidine, d-Ribose, 2-deoxy-bis(thioheptyl)-dithioacetal, 5-Nitroso-2,4,6-triaminopyrimidine were secreted by combination of S. indica and Z. sp. ISTPL4. These metabolites have antimicrobial, antioxidant and nematicidal activities. I-hexadecanol is a major volatile compound produced by molds and acts as an antifeedant in different species of aphids [23,25,32,33]. Heneicosane has antimicrobial activities against Streptococcus pneumonia and Aspergillus fumigatus and Cyclo(L-propyl-L-valine) is a class of diketopiperazines (DKPs). These metabolites are mainly involved in interactions between mixed microbial communities [33,34]. The secretion of this metabolite by microbes can be a possible reason for the positive interaction of S. indica and Z. sp. ISTPL4. Other metabolites including l-(+)-Ascorbic acid 2,6-dihexadecanoate, Docosanoic acid, ethyl ester, Isopropyl palmitate, 2-Methyltetracosane, n-Hexane, 13-Docosenamide (Z) have been reported. These metabolites play a crucial role in antiallergic, antibacterial, antioxidant, termiticide and antiviral activity, antimicrobial and free radical scavenging activity [35,36]. Tetratriacontyl heptafluorobutyrate, myristic acid, glycidyl ester, tetradecanoic acid, 2-Propenoic acid, 3-(4-methoxyphenyl) are the metabolites released by S. indica in the presence of As. These metabolites have antifungal and antimicrobial activity [6,34,37]. Metabolites including 2,3-dihydroxypropyl ester Stearin, Eicosane, 3-Indol-1-yl-propionic acid, methyl ester and, Glycerol tricaprylate, have antimicrobial, antifungal, probiotics and antioxidant activities [38,39,40]. L-Proline, glycine, squalene, heptadecane, 7,9 di-tert butyl-1-oxaspiro(4,5) deca-a-6,9-diene-2,8-dione, Dodecane,4,6-dimethyl, Tridecanoic acid, 12-methyl-, methyl ester, 2-methyl tetracosane and quercetin play an essential role in plant growth and development under abiotic stress [41,42,43,44,45]. These metabolites protect plants under stress by acting as antioxidants, promoting signaling cascade in plants for enhancing plant growth and scavenging free radicals generated during oxidative stress in plants. Quercetin is a polyphenolic compound with antioxidant properties secreted by microbial combinations.
The study suggests that an active efflux system operates in the removal of arsenic by S. indica and Z. sp. ISTPL4. S. indica and Z. sp. ISTPL4 uptakes arsenate through phosphate transporters (Ars C) and converts it into arsenite by arsenate reductase. The converted form of arsenite (III) is then shunted out. The presence of the ArsC gene is also reported in Z. sp. ISTPL4 which also confers arsenic tolerance ability of this actinobacterium. This combination of microbes can be used to mitigate the toxic effects of arsenic in the contaminated environments and increase sustainable agriculture in the soils that are contaminated (Figure 9).

5. Conclusions

Our study concluded the significance of various metabolites secreted by S. indica alone and in combination with Z. sp. ISTPL4 under normal environmental conditions and in the presence of arsenic stress. The secretion of Cyclo(L-propyl-L-valine) by both S. indica and Z. sp. ISTPL4 indicated the possible reason for their interaction. Also, the arsenic tolerance ability of S. indica was checked individually and in combination with Z. sp. ISTPL4 in this study. Results of the biotransformation experiment also indicated the arsenic tolerance ability of S. indica and Z. sp. ISTPL4. However, these microbes can be used to mitigate arsenic stress. The presence of various metabolites also indicated the capability of S. indica and Z. sp. ISTPL4 in plant growth and stress alleviation under various biotic and abiotic factors. Our data are largely confirmed by other scientific literature, which has shown that these microbial strains can efficiently remove arsenic from contaminated environments.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/microorganisms12020405/s1, Supplementary File S1: Mass fragmentation pattern and structural elucidations of common metabolites secreted by Serendipita indica under normal growth conditions and in presence of arsenic stress; Supplementary File S2: Mass fragmentation patterns and structural elucidations of common secondary metabolites secreted by Serendipita indica and Zhihengliuella sp. ISTPL4 under normal growth conditions and in the presence of arsenic stress; Supplementary File S3: Secondary metabolites production by Serendipita indica and Zhihengliuella sp. ISTPL4 under normal growth conditions and in presence of As stress; Supplementary file S4: Secondary metabolites production by Serendipita indica and Zhihengliuella sp. ISTPL4 under normal growth conditions and in presence of As stress. Refs. [40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113,114,115,116,117,118,119,120,121,122,123,124,125,126,127,128,129,130,131,132,133,134,135,136,137,138,139,140,141,142,143,144,145,146,147,148,149,150,151,152,153,154] can be found in Supplementary Materials.

Author Contributions

Conceptualization, A.M. and L.D.; methodology, N.S.; software, M.K.; validation, A.M.; investigation, N.C.J.; resources, N.C.J.; data curation, A.M. and L.D.; writing—original draft preparation, N.S.; writing—review and editing, N.S.; supervision, N.C.J.; project administration, N.C.J.; funding acquisition, N.C.J. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

Data are contained within the article.

Acknowledgments

All the authors are thankful to the Amity Institute of Microbial Technology, Amity University, Noida for providing all the facilities and DST-FIST for the Confocal facility. Laurent Dufossé is deeply thankful to the Conseil Régional de La Réunion and the Conseil Régional de Bretagne for their continuous support of microbial biotechnology activities.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Zaman, N.R.; Chowdhury, U.F.; Reza, R.N.; Chowdhury, F.T.; Sarker, M.; Hossain, M.M.; Akbor, M.A.; Amin, A.; Islam, M.R.; Khan, H. Plant Growth Promoting Endophyte Burkholderia Contaminans NZ Antagonizes Phytopathogen Macrophomina Phaseolina through Melanin Synthesis and Pyrrolnitrin Inhibition. PLoS ONE 2021, 16, e0257863. [Google Scholar] [CrossRef] [PubMed]
  2. Genchi, G.; Lauria, G.; Catalano, A.; Carocci, A.; Sinicropi, M.S. Arsenic: A Review on a Great Health Issue Worldwide. Appl. Sci. 2022, 12, 6184. [Google Scholar] [CrossRef]
  3. Bianucci, E.; Peralta, J.M.; Furlan, A.; Hernández, L.E. Arsenic in Drinking Water and Food; Springer: Berlin/Heidelberg, Germany, 2020. [Google Scholar] [CrossRef]
  4. Chandrakar, V.; Pandey, N.; Keshavkant, S. Plant Responses to Arsenic Toxicity: Morphology and Physiology. In Mechanisms of Arsenic Toxicity and Tolerance in Plants; Springer: Singapore, 2018. [Google Scholar]
  5. Pérez-Montaño, F.; Alías-Villegas, C.; Bellogín, R.A.; Del Cerro, P.; Espuny, M.R.; Jiménez-Guerrero, I.; López-Baena, F.J.; Ollero, F.J.; Cubo, T. Plant Growth Promotion in Cereal and Leguminous Agricultural Important Plants: From Microorganism Capacities to Crop Production. Microbiol. Res. 2014, 169, 325–336. [Google Scholar] [CrossRef] [PubMed]
  6. Mitra, D.; Mondal, R.; Khoshru, B.; Senapati, A.; Radha, T.K.; Mahakur, B.; Uniyal, N.; Myo, E.M.; Boutaj, H.; Sierra, B.E.G.; et al. Actinobacteria-Enhanced Plant Growth, Nutrient Acquisition, and Crop Protection: Advances in Soil, Plant, and Microbial Multifactorial Interactions. Pedosphere 2022, 32, 149–170. [Google Scholar] [CrossRef]
  7. Koza, N.A.; Adedayo, A.A.; Babalola, O.O.; Kappo, A.P. Microorganisms in Plant Growth and Development: Roles in Abiotic Stress Tolerance and Secondary Metabolites Secretion. Microorganisms 2022, 10, 1528. [Google Scholar] [CrossRef]
  8. Pang, Z.; Chen, J.; Wang, T.; Gao, C.; Li, Z.; Guo, L.; Xu, J.; Cheng, Y. Linking Plant Secondary Metabolites and Plant Microbiomes: A Review. Front. Plant Sci. 2021, 12, 621276. [Google Scholar] [CrossRef]
  9. Barra Caracciolo, A.; Terenzi, V. Rhizosphere Microbial Communities and Heavy Metals. Microorganisms 2021, 9, 1462. [Google Scholar] [CrossRef]
  10. Raychaudhuri, S.S.; Pramanick, P.; Talukder, P.; Basak, A. Polyamines, Metallothioneins, and Phytochelatins—Natural Defense of Plants to Mitigate Heavy Metals. Stud. Nat. Prod. Chem. 2021, 69, 227–261. [Google Scholar]
  11. Varma, A.; Sowjanya Sree, K.; Arora, M.; Bajaj, R.; Prasad, R.; Kharkwal, A.C. Functions of Novel Symbiotic Fungus—Piriformospora indica. Proc. Indian Natl. Sci. Acad. 2014, 80, 429–441. [Google Scholar] [CrossRef]
  12. Jangir, P.; Shekhawat, P.K.; Bishnoi, A.; Ram, H.; Soni, P. Role of Serendipita indica in Enhancing Drought Tolerance in Crops. Physiol. Mol. Plant Pathol. 2021, 116, 101691. [Google Scholar] [CrossRef]
  13. Yang, G.; Ahmad, F.; Zhou, Q.; Guo, M.; Liang, S.; Gaal, H.A.; Mo, J. Investigation of Physicochemical Indices and Microbial Communities in Termite Fungus-Combs. Front. Microbiol. 2021, 11, 581219. [Google Scholar] [CrossRef] [PubMed]
  14. Sharma, N.; Dabral, S.; Tyagi, J.; Yadav, G.; Aggarwal, H.; Joshi, N.C.; Varma, A.; Koul, M.; Choudhary, D.K.; Mishra, A. Interaction Studies of Serendipita indica and Zhihengliuella sp. ISTPL4 and Their Synergistic Role in Growth Promotion in Rice. Front. Plant Sci. 2023, 14, 1155715. [Google Scholar] [CrossRef] [PubMed]
  15. Hill, T.W.; Kafer, E. Improved Protocols for Aspergillus minimal Medium: Trace Element and Minimal Medium Salt Stock Solutions. Fungal Genet. Rep. 2001, 48, 20–21. [Google Scholar] [CrossRef]
  16. Mohd, S.; Shukla, J.; Kushwaha, A.S.; Mandrah, K.; Shankar, J.; Arjaria, N.; Saxena, P.N.; Narayan, R.; Roy, S.K.; Kumar, M. Endophytic Fungi Piriformospora indica Mediated Protection of Host from Arsenic Toxicity. Front. Microbiol. 2017, 8, 754. [Google Scholar] [CrossRef]
  17. Dabral, S.; Saxena, S.C.; Choudhary, D.K.; Bandyopadhyay, P.; Sahoo, R.K.; Tuteja, N.; Nath, M. Synergistic Inoculation of Azotobacter Vinelandii and Serendipita indica Augmented Rice Growth. Symbiosis 2020, 81, 139–148. [Google Scholar] [CrossRef]
  18. Bhati, R.; Sreedharan, S.M.; Rizvi, A.; Khan, M.S.; Singh, R. An Insight into Efflux-Mediated Arsenic Resistance and Biotransformation Potential of Enterobacter cloacae RSC3 from Arsenic Polluted Area. Indian J. Microbiol. 2022, 62, 456–467. [Google Scholar] [CrossRef]
  19. Gengmao, Z.; Quanmei, S.; Yu, H.; Shihui, L.; Changhai, W. The Physiological and Biochemical Responses of a Medicinal Plant (Salvia miltiorrhiza L.) to Stress Caused by Various Concentrations of NaCl. PLoS ONE 2014, 9, e89624. [Google Scholar] [CrossRef] [PubMed]
  20. Tripathi, A.; Singh, Y.; Verma, D.K.; Ranjan, M.R.; Srivastava, S.K. Bioremediation of Hazardous Azo Dye Methyl Red by a Newly Isolated Bacillus megaterium ITBHU01: Process Improvement through ANN-GA Based Synergistic Approach. Indian J. Biochem. Biophys. 2016, 53, 112–125. [Google Scholar]
  21. Anantha, P.S.; Deventhiran, M.; Saravanan, P.; Anand, D.; Rajarajan, S. A Comparative GC-MS Analysis of Bacterial Secondary Metabolites of Pseudomonas Species. Pharma Innov. 2016, 5, 84–89. [Google Scholar]
  22. Poveda, J.; Baptista, P.; Sacristán, S.; Velasco, P. Editorial: Beneficial Effects of Fungal Endophytes in Major Agricultural Crops. Front. Plant Sci. 2022, 13, 1061112. [Google Scholar] [CrossRef]
  23. Okon, O.; Matrood, A.; Okon, J. Na+ Exclusion and Na+/K+ Ratio Adjustment by Mycorrhiza Enhances Macro/Micro Nutrients Uptake in Two Members of Cucurbitaceae Family under Salt Stress. Int. J. Bot. Stud. 2020, 5, 108–114. [Google Scholar]
  24. Fa, A.N. Endophytic Fungi for Sustainable Agriculture. Microb. Biosyst. 2019, 4, 31–44. [Google Scholar] [CrossRef]
  25. Rabiey, M.; Ullah, I.; Shaw, L.J.; Shaw, M.W. Potential Ecological Effects of Piriformospora indica, a Possible Biocontrol Agent, in UK Agricultural Systems. Biol. Control 2017, 104, 1–9. [Google Scholar] [CrossRef]
  26. Dabral, S.; Yashaswee; Varma, A.; Choudhary, D.K.; Bahuguna, R.N.; Nath, M. Biopriming with Piriformospora indica Ameliorates Cadmium Stress in Rice by Lowering Oxidative Stress and Cell Death in Root Cells. Ecotoxicol. Environ. Saf. 2019, 186, 109741. [Google Scholar] [CrossRef] [PubMed]
  27. Mishra, A.; Jha, G.; Thakur, I.S. Draft Genome Sequence of Zhihengliuella sp. Strain ISTPL4, a Psychrotolerant and Halotolerant Bacterium Isolated from Pangong Lake, India. Genome Announc. 2018, 6, e01533-17. [Google Scholar] [CrossRef] [PubMed]
  28. Bernhard, A.E.; Sheffer, R.; Giblin, A.E.; Marton, J.M.; Roberts, B.J. Population Dynamics and Community Composition of Ammonia Oxidizers in Salt Marshes after the Deepwater Horizon Oil Spill. Front. Microbiol. 2016, 7, 854. [Google Scholar] [CrossRef]
  29. Vanitha, V.; Vijayakumar, S.; Nilavukkarasi, M.; Punitha, V.; Vidhya, E.; Praseetha, P. Heneicosane—A Novel Microbicidal Bioactive Alkane Identified from Plumbago Zeylanica L. Ind. Crops Prod. 2020, 154, 112748. [Google Scholar] [CrossRef]
  30. Wani, S.H.; Kumar, V.; Shriram, V.; Sah, S.K. Phytohormones and Their Metabolic Engineering for Abiotic Stress Tolerance in Crop Plants. Crop J. 2016, 4, 162–176. [Google Scholar] [CrossRef]
  31. Singh, R.; Kumar, M.; Mittal, A.; Mehta, P.K. Microbial Metabolites in Nutrition, Healthcare and Agriculture. 3 Biotech 2017, 7, 15. [Google Scholar] [CrossRef]
  32. Gadhi, A.A.A.; El-Sherbiny, M.M.O.; Al-Sofyani, A.M.A.; Ba-Akdah, M.A.; Satheesh, S. Antibiofilm Activities of Extracts of the Macroalga Halimeda sp. from the Red Sea. J. Mar. Sci. Technol. 2018, 26, 838–846. [Google Scholar] [CrossRef]
  33. Khattab, A.I.; Babiker, E.H.; Saeed, H.A. Streptomyces: Isolation, Optimization of Culture Conditions and Extraction of Secondary Metabolites. Int. Curr. Pharm. J. 2016, 5, 27–32. [Google Scholar] [CrossRef]
  34. Shaaban, M.T.; Ghaly, M.F.; Fahmi, S.M. Antibacterial Activities of Hexadecanoic Acid Methyl Ester and Green-Synthesized Silver Nanoparticles against Multidrug-Resistant Bacteria. J. Basic Microbiol. 2021, 61, 557–568. [Google Scholar] [CrossRef]
  35. Ferdosi, M.F.H.; Javaid, A.; Khan, I.H. Phytochemical Profile of N-Hexane Flower Extract of Cassia fistula L. Bangladesh J. Bot. 2022, 51, 393–399. [Google Scholar] [CrossRef]
  36. Chenniappan, J.; Sankaranarayanan, A.; Arjunan, S. Evaluation of Antimicrobial Activity of Cissus quadrangularis L. Stem Extracts against Avian Pathogens and Determination of Its Bioactive Constituents Using GC-MS. J. Sci. Res. 2020, 64, 90–96. [Google Scholar] [CrossRef]
  37. Chandrasekaran, M.; Senthilkumar, A.; Venkatesalu, V. Antibacterial and Antifungal Efficacy of Fatty Acid Methyl Esters from the Leaves of Sesuvium portulacastrum L. Eur. Rev. Med. Pharmacol. Sci. 2011, 15, 775–780. [Google Scholar]
  38. Naim, M.J.; Alam, O.; Alam, J.; Bano, F.; Alam, P.; Shrivastava, N. Recent Review on Indole: A privileged scaffold structure. Int. J. Pharma Sci. Res. 2016, 7, 51–62. [Google Scholar]
  39. Chen, S.; Liu, J.; Gong, H.; Yang, D. Identification and Antibacterial Activity of Secondary Metabolites from Taxus Endophytic Fungus. Chin. J. Biotechnol. 2009, 25, 368–374. [Google Scholar] [PubMed]
  40. Kumari, N.; Menghani, E.; Mithal, R. GCMS Analysis of Compounds Extracted from Actinomycetes AIA6 Isolates and Study of Its Antimicrobial Efficacy. Indian J. Chem. Technol. 2019, 26, 362–370. [Google Scholar]
  41. Ramya, B.; Malarvili, T.; Velavan, S. GC-MS Analysis of Bioactive Compounds in Bryonopsis Laciniosa Fruit Extract. Int. J. Pharm. Sci. Res. 2015, 6, 3375–3379. [Google Scholar]
  42. Mooney, E.C.; Holden, S.E.; Xia, X.J.; Li, Y.; Jiang, M.; Banson, C.N.; Zhu, B.; Sahingur, S.E. Quercetin Preserves Oral Cavity Health by Mitigating Inflammation and Microbial Dysbiosis. Front. Immunol. 2021, 12, 774273. [Google Scholar] [CrossRef] [PubMed]
  43. Babar, A.G. Antifungal Activity and Investigation of Bioactive Compounds of Marine Intertidal Bivalve Gafrarium Divaricatum from West Coast of India. Int. J. Pure Appl. Biosci. 2016, 4, 211–217. [Google Scholar] [CrossRef]
  44. Nakkeeran, S.; Priyanka, R.; Rajamanickam, S.; Sivakumar, U. Bacillus amyloliquefaciens Alters the Diversity of Volatile and Non-Volatile Metabolites and Induces the Expression of Defence Genes for the Management of Botrytis Leaf Blight of Lilium under Protected Conditions. J. Plant Pathol. 2020, 102, 1179–1189. [Google Scholar] [CrossRef]
  45. Younis, A.A.; Saleh, H.A. Phytochemical Screening and Assessment of Antioxidant and Antimicrobial Potentialities of Two Egyptian Medicinal Plants. Egypt. J. Pure Appl. Sci. 2021, 59, 49–57. [Google Scholar] [CrossRef]
  46. Ahmad Mustafa, F.N. Green Synthesis of Isopropyl Palmitate Using Immobilized Candida Antarctica Lipase: Process Optimization Using Response Surface Methodology. Clean. Eng. Technol. 2022, 8, 100516. [Google Scholar] [CrossRef]
  47. Kumari, N.; Menghani, E.; Mithal, R. Bioactive Compounds Characterization and Antibacterial Potentials of Actinomycetes Isolated from Rhizospheric Soil. J. Sci. Ind. Res. 2019, 78, 793–798. [Google Scholar]
  48. Parthasarathy, R. Ethnic Quotas as Term-Limits: Caste and Distributive Politics in South India. Comp. Political Stud. 2017, 50, 1735–1767. [Google Scholar] [CrossRef]
  49. Arya, A.; Kumar, S.; Kain, D.; Ahanger, A.M.; Suryavanshi, A.; Vandana. Unfolding the Chemical Composition, Antioxidant and Antibacterial Activities of Drymaria cordata (Linn.) Willd. against Chloramphenicol-Resistant Bacillus subtilis and β-Lactams-Resistant Pseudomonas aeruginosa. Vegetos 2023, 1–10. [Google Scholar] [CrossRef]
  50. Babatunde, D.E.; Otusemade, G.O.; Efeovbokhan, V.E.; Ojewumi, M.E.; Bolade, O.P.; Owoeye, T.F. Chemical Composition of Steam and Solvent Crude Oil Extracts from Azadirachta indica Leaves. Chem. Data Collect. 2019, 20, 100208. [Google Scholar] [CrossRef]
  51. Kalaba, M.H.; Sultan, M.H.; Elbahnasawy, M.A.; El-Didamony, S.E.; Bakary, N.M.E.; Sharaf, M.H. First Report on Isolation of Mucor Bainieri from Honeybees, Apis mellifera: Characterization and Biological Activities. Biotechnol. Rep. 2022, 36, e00770. [Google Scholar] [CrossRef] [PubMed]
  52. Selvamani, K.; Tadigiri, S.; Das, D. Isolation and Characterization of Chemical Constituents from B. amyloliquefaciens and Their Nematicidal Activity. J. Entomol. Zool. Stud. 2020, 8, 2062–2066. [Google Scholar]
  53. Zhu, F.; Zhu, C.; Doyle, E.; Gao, J. Fate of Di (2-Ethylhexyl) Phthalate in Different Soils and Associated Bacterial Community Changes. Sci. Total Environ. 2018, 637, 460–469. [Google Scholar] [CrossRef]
  54. Saboon; Bibi, Y.; Ayoubi, S.A.; Afzal, T.; Gilani, S.; Malik, K.; Qayyum, A.; Hussain, M.; Kumar, S. Antioxidant-Activity-Guided Purification and Separation of Octocrylene from Saussurea heteromalla. Separations 2023, 10, 107. [Google Scholar] [CrossRef]
  55. Stevenson, J.; Luu, W.; Kristiana, I.; Brown, A.J. Squalene Mono-Oxygenase, a Key Enzyme in Cholesterol Synthesis, Is Stabilized by Unsaturated Fatty Acids. Biochem. J. 2014, 461, 435–442. [Google Scholar] [CrossRef] [PubMed]
  56. Eramma, N.; Patil, S.J. Exploration of the Biomolecules in roots of Flacourtia indica (Burm. F) Merr. Methanol Extract by Chromatography Approach. Lett. Appl. NanoBioSci. 2023, 12, 166–177. [Google Scholar]
  57. Tyagi, S.; Singh, R.K.; Tiwari, S.P. Anti-Enterococcal and Anti-Oxidative Potential of a Thermophilic Cyanobacterium, Leptolyngbya sp. HNBGU 003. Saudi J. Biol. Sci. 2021, 28, 4022–4028. [Google Scholar] [CrossRef]
  58. Saleh, A.E.; Ul-Hassan, Z.; Zeidan, R.; Al-Shamary, N.; Al-Yafei, T.; Alnaimi, H.; Higazy, N.S.; Migheli, Q.; Jaoua, S. Biocontrol Activity of Bacillus megaterium BM344-1 against Toxigenic Fungi. ACS Omega 2021, 6, 10984–10990. [Google Scholar] [CrossRef]
  59. Guo, C.; Chen, Y.; Wu, D.; Du, Y.; Wang, M.; Liu, C.; Chu, J.; Yao, X. Transcriptome Analysis Reveals an Essential Role of Exogenous Brassinolide on the Alkaloid Biosynthesis Pathway in Pinellia Ternata. Int. J. Mol. Sci. 2022, 23, 10898. [Google Scholar] [CrossRef] [PubMed]
  60. Chakraborty, B.; Suresh, R.; Almansour, A.I.; Gunasekaran, P.; Nayaka, S. Saudi Journal of Biological Sciences Bioprospection and Secondary Metabolites Profiling of Marine Streptomyces levis Strain KS46. Saudi J. Biol. Sci. 2022, 29, 667–679. [Google Scholar] [CrossRef]
  61. Uyan, A.; Turan, C.; Erdogan-Eliuz, E.A.; Sangun, M.K. Antimicrobial Properties of Bioactive Compounds Isolated from Epidermal Mucus in Two Ray Species (Dasyatis marmorata and Gymnura altavela). Trop. J. Pharm. Res. 2020, 19, 2115–2121. [Google Scholar] [CrossRef]
  62. Siddharthan, N.; Balagurunathan, R.; Venkatesan, S.; Hemalatha, N. Bio-Efficacy of Geobacillus thermodenitrificans PS41 against Larvicidal, Fungicidal, and Plant Growth–Promoting Activities. Environ. Sci. Pollut. Res. 2022, 30, 42596–42607. [Google Scholar] [CrossRef]
  63. Kanbak, S.A.; Koksal, M.; Sahin, F.; Erol, D.D. Synthesis of New 4(1H)-Pyridinone Derivatives and Their Antibacterial Activity. Rev. Chim. 2009, 60, 888–892. [Google Scholar]
  64. Łukowska-Chojnacka, E.; Kowalkowska, A.; Gizińska, M.; Koronkiewicz, M.; Staniszewska, M. Synthesis of Tetrazole Derivatives Bearing Pyrrolidine Scaffold and Evaluation of Their Antifungal Activity against Candida albicans. Eur. J. Med. Chem. 2019, 164, 106–120. [Google Scholar] [CrossRef]
  65. Dutta, J.; Thakur, D. Evaluation of Antagonistic and Plant Growth Promoting Potential of Streptomyces sp. TT3 Isolated from Tea (Camellia Sinensis) Rhizosphere Soil. Curr. Microbiol. 2020, 77, 1829–1838. [Google Scholar] [CrossRef]
  66. Sakthiselvan, P.; Madhumathi, R.; Meenambiga, S.S. Moronic Acid: An Antiviral for Herpes Simplex Virus. In A Centum of Valuable Plant Bioactives; Academic Press: Berlin/Heidelberg, Germany, 2021; pp. 143–158. [Google Scholar] [CrossRef]
  67. Díaz-Pérez, A.L.; Díaz-Pérez, C.; Campos-García, J. Bacterial L-Leucine Catabolism as a Source of Secondary Metabolites. Rev. Environ. Sci. Bio/Technol. 2016, 15, 1–29. [Google Scholar] [CrossRef]
  68. Jung, H.; Hilger, D.; Raba1, M. The Na+/L-Proline Transporter PutP. Front. Biosci. 2012, 17, 745–759. [Google Scholar] [CrossRef] [PubMed]
  69. Shwaish, T.; Al-Imarah, F.J.M.; Jasim, F.A. Wound Healing Capacity, Antibacterial Activity, and GC-MS Analysis of Bienertia sinuspersici Leaves Extract. J. Phys. Conf. Ser. 2019, 1294, 062056. [Google Scholar] [CrossRef]
  70. Rhetso, T.; Shubharani, R.; Roopa, M.S.; Sivaram, V. Chemical Constituents, Antioxidant, and Antimicrobial Activity of Allium chinense G. Don. Future J. Pharm. Sci. 2020, 6, 102. [Google Scholar] [CrossRef]
  71. Touria Ould Bellahcen, M.C. Chemical Composition and Antibacterial Activity of the Essential Oil of Spirulina platensis from Morocco. J. Essent. Oil Bear. Plants 2019, 22, 1265–1276. [Google Scholar] [CrossRef]
  72. Singh, P.; Singh, J.; Ray, S.; Vaishnav, A.; Jha, P.; Singh, R.K.; Singh, H. Microbial Volatiles (MVOCs) Induce Tomato Plant Growth and Disease Resistance Against Wilt Pathogen Fusarium oxysporum f.sp. lycopersici. J. Plant Growth Regul. 2023, 1–14. [Google Scholar] [CrossRef]
  73. Ladkau, N.; Assmann, M.; Schrewe, M.; Julsing, M.K.; Schmid, A.; Bühler, B. Efficient Production of the Nylon 12 Monomer ω-Aminododecanoic Acid Methyl Ester from Renewable Dodecanoic Acid Methyl Ester with Engineered Escherichia coli. Metab. Eng. 2016, 36, 1–9. [Google Scholar] [CrossRef]
  74. Ashraf, M.F.M.R.; Foolad, M.R. Roles of Glycine Betaine and Proline in Improving Plant Abiotic Stress Resistance. Environ. Exp. Bot. 2007, 59(2), 206–216. [Google Scholar] [CrossRef]
  75. He, K.; Zhang, T.; Zhang, S.; Sun, Z.; Zhang, Y.; Yuan, Y.; Jia, X. Tunable Functionalization of Saturated C–C and C–H Bonds of N,N′-Diarylpiperazines Enabled by tert-Butyl Nitrite (TBN) and NaNO2 Systems. Org. Lett. 2019, 21, 5030–5034. [Google Scholar] [CrossRef]
  76. Vorobjeva, L.I.; Khodjaev, E.Y.; Vorobjeva, N.V. Propionic Acid Bacteria as Probiotics. Microb. Ecol. Health Dis. 2008, 20, 109–112. [Google Scholar] [CrossRef]
  77. Rathod, S.V.; Shinde, K.W.; Kharkar, P.S.; Shah, C.P.; Aruna, K.; Raut, D.A. Synthesis, Molecular Docking and Biological Evaluation of New Quinoline Analogues as Potent Anti-Breast Cancer and Antibacterial Agents. Indian J. Chem. Sect. B Org. Med. Chem. 2021, 60B, 1215–1222. [Google Scholar] [CrossRef]
  78. Monjil, M.S.; Takemoto, D.; Kawakita, K. Defense Induced by a Bis-Aryl Methanone Compound Leads to Resistance in Potato against Phytophthora infestans. J. Gen. Plant Pathol. 2014, 80, 38–49. [Google Scholar] [CrossRef]
  79. Singh, J.; Sharma, S.; Kaur, A.; Vikal, Y.; Cheema, A.K.; Bains, B.K.; Kaur, N.; Gill, G.K.; Malhotra, P.K.; Kumar, A.; et al. Marker-Assisted Pyramiding of Lycopene-ε-Cyclase, β-Carotene Hydroxylase1 and Opaque2 Genes for Development of Biofortified Maize Hybrids. Sci. Rep. 2021, 11, 12642. [Google Scholar] [CrossRef] [PubMed]
  80. Daood, U.; Matinlinna, J.P.; Pichika, M.R.; Mak, K.K.; Nagendrababu, V.; Fawzy, A.S. A Quaternary Ammonium Silane Antimicrobial Triggers Bacterial Membrane and Biofilm Destruction. Sci. Rep. 2020, 10, 10970. [Google Scholar] [CrossRef] [PubMed]
  81. Das, P.; Devi, N.; Gaur, N.; Goswami, S.; Dutta, D.; Dubey, R.; Puzari, A. Acrylonitrile Adducts: Design, Synthesis and Biological Evaluation as Antimicrobial, Haemolytic and Thrombolytic Agent. Sci. Rep. 2023, 13, 6209. [Google Scholar] [CrossRef] [PubMed]
  82. Yadav, B.; Jogawat, A.; Rahman, M.S.; Narayan, O.P. Secondary Metabolites in the Drought Stress Tolerance of Crop Plants: A Review. Gene Rep. 2021, 23, 101040. [Google Scholar] [CrossRef]
  83. Harikrishnan, S.; Parivallal, M.; Alsalhi, M.S.; Sudarshan, S.; Jayaraman, N.; Devanesan, S.; Rajasekar, A.; Jayalakshmi, S. Characterization of Active Lead Molecules from Lissocarinus orbicularis with Potential Antimicrobial Resistance Inhibition Properties. J. Infect. Public Health 2021, 14, 1903–1910. [Google Scholar] [CrossRef] [PubMed]
  84. Kumaresan, S.; Senthilkumar, V.; Stephen, A.; Balakumar, B.S. GC-MS analysis and pass-assisted prediction of biological activity spectra of extract of Phomopsis sp. isolated from Andrographis paniculata. World J. Pharm. Res. 2015, 4, 1035–1053. [Google Scholar]
  85. Trivedi, D.K.; Sinclair, E.; Xu, Y.; Sarkar, D.; Walton-Doyle, C.; Liscio, C.; Banks, P.; Milne, J.; Silverdale, M.; Kunath, T.; et al. Discovery of Volatile Biomarkers of Parkinson’s Disease from Sebum. ACS Cent. Sci. 2019, 5, 599–606. [Google Scholar] [CrossRef]
  86. Varsha, K.K.; Devendra, L.; Shilpa, G.; Priya, S.; Pandey, A.; Nampoothiri, K.M. 2,4-Di-tert-butyl Phenol as the Antifungal, Antioxidant Bioactive Purified from a Newly Isolated Lactococcus sp. Int. J. Food Microbiol. 2015, 211, 44–50. [Google Scholar] [CrossRef]
  87. Abdullah, R. Insecticidal Activity of Secondary Metabolites of Locally Isolated Fungal Strains against Some Cotton Insect Pests. J. Plant Prot. Pathol. 2019, 10, 647–653. [Google Scholar] [CrossRef]
  88. Rani, A.; Saini, K.C.; Bast, F.; Mehariya, S.; Bhatia, S.K.; Lavecchia, R.; Zuorro, A. Microorganisms: A Potential Source of Bioactive Molecules for Antioxidant Applications. Molecules 2021, 26, 1142. [Google Scholar] [CrossRef]
  89. Sharma, S.; Chandra, D.; Sharma, A.K. Rhizosphere Plant–Microbe Interactions Under Abiotic Stress. In Rhizosphere Biology: Interactions between Microbes and Plants; Springer: Singapore, 2021; pp. 195–216. [Google Scholar] [CrossRef]
  90. Javed, S.; Javaid, A.; Al-Taie, A.H.; Zahid, M. Identification of Antimicrobial Compounds from n-Hexane Stem Extract of Kochia indica by GC-MS Analysis. Mycopath 2018, 16, 51–55. [Google Scholar]
  91. Ahmad, R.; Ahmad, T.; Hussain, B. Proceedings of International Conference on Recent Advances in Space Technologies (IEEE Cat. No.03EX743); IEEE: New York, NY, USA, 2011; ISBN 9788195663415. [Google Scholar]
  92. Rachmawaty; Mu’Nisa, A.; Hasri; Pagarra, H.; Hartati; Qureshi, M.Z. Active Compounds Extraction of Cocoa Pod Husk (Thebroma cacao L.) and Potential as Fungicides. J. Phys. Conf. Ser. 2018, 1028, 012013. [Google Scholar] [CrossRef]
  93. Duraisamy, M.; Raja, S. Analysis of Bioactive Compounds by Gas Chromatography-Mass Spectrum and Anti-Bacterial Activity of Zonaria crenata. Aegaeum J. 2020, 8, 829–844. [Google Scholar] [CrossRef]
  94. Younus, I.; Khan, S.J.; Maqbool, S.; Begum, Z. Anti-Fungal Therapy via Incorporation of Nanostructures: A Systematic Review for New Dimensions. Phys. Scr. 2022, 97, 012001. [Google Scholar] [CrossRef]
  95. Ser, H.L.; Palanisamy, U.D.; Yin, W.F.; Abd Malek, S.N.; Chan, K.G.; Goh, B.H.; Lee, L.H. Presence of Antioxidative Agent, Pyrrolo[1,2-a]pyrazine-1,4-dione, Hexahydro- in Newly Isolated Streptomyces mangrovisoli sp. nov. Front. Microbiol. 2015, 6, 854. [Google Scholar] [CrossRef] [PubMed]
  96. Komansilan, A.; Abadi, A.L.; Yanuwiadi, B.; Kaligis, D.A. Isolation and Identification of Biolarvicide from Soursop (Annona muricata Linn) Seeds to Mosquito (Aedes aegypti) Larvae. Int. J. Eng. Technol. 2012, 12, 28–32. [Google Scholar]
  97. Momodu, I.B.; Okungbowa, E.S.; Agoreyo, B.O.; Maliki, M.M. Gas Chromatography—Mass Spectrometry Identification of Bioactive Compounds in Methanol and Aqueous Seed Extracts of Azanza garckeana Fruits. Niger. J. Biotechnol. 2022, 38, 25–38. [Google Scholar] [CrossRef]
  98. Ansari, M.W.; Gill, S.S.; Tuteja, N. Piriformospora indica a Powerful Tool for Crop Improvement. Proc. Indian Natl. Sci. Acad. 2014, 80, 317–324. [Google Scholar] [CrossRef]
  99. Sahu, P.K.; Jayalakshmi, K.; Tilgam, J.; Gupta, A.; Nagaraju, Y.; Kumar, A.; Rajput, V.D.; Vikram, M.; Rajawat, S. ROS Generated from Biotic Stress: Effects on Plants and Alleviation by Endophytic Microbes. Front. Plant Sci. 2022, 13, 1042936. [Google Scholar] [CrossRef] [PubMed]
  100. Rani, S.V.G.; Murugaiah, K. GC-MS Determination of Bioactive Compounds in Azima tetracantha Leaves. World J. Pharm. Res. 2015, 4, 2225–2231. [Google Scholar]
  101. Suharti, W.S.; Tini, E.W.; Istiqomah, D. Antimicrobial Activity of Kaempferia galanga against Plant Pathogen on Rice. Biodiversitas 2023, 24, 1320–1326. [Google Scholar]
  102. Saravanan, R.; Pemiah, B.; Narayanan, M.; Ramalingam, S. In Vitro Cytotoxic and Gas Chromatography-Mass Spectrometry Studies on Orthosiphon stamineus Benth. (Leaf) against MCF–7 Cell Lines. Asian J. Pharm. Clin. Res. 2017, 10, 129–135. [Google Scholar] [CrossRef]
  103. Okoro, E.E.; Osoniyi, O.R.; Jabeen, A.; Shams, S.; Choudhary, M.I.; Onajobi, F.D. Anti-Proliferative and Immunomodulatory Activities of Fractions from Methanol Root Extract of Abrus precatorius L. Clin. Phytosci. 2019, 5, 45. [Google Scholar] [CrossRef]
  104. Adnan, M.; Nazim Uddin Chy, M.; Mostafa Kamal, A.T.M.; Azad, M.O.K.; Paul, A.; Uddin, S.B.; Barlow, J.W.; Faruque, M.O.; Park, C.H.; Cho, D.H. Investigation of the Biological Activities and Characterization of Bioactive Constituents of Ophiorrhiza rugosa var. prostrata (D.Don) & Mondal Leaves through in Vivo, in Vitro, and in Silico Approaches. Molecules 2019, 24, 1367. [Google Scholar] [CrossRef]
  105. Ponnamma, S.U.; Manjunath, K. GC-MS Analysis of Phytocomponents in the Methanolic Extract of Justicia wynaadensis (NEES) T. Anders. Int. J. Pharma Bio Sci. 2012, 3, 570–576. [Google Scholar]
  106. Chrząszcz, M.; Miazga-Karska, M.; Klimek, K.; Dybowski, M.P.; Typek, R.; Tchórzewska, D.; Dos Santos Szewczyk, K. The Anti-Acne Potential and Chemical Composition of Knautia drymeia Heuff. and Knautia macedonica Griseb Extracts. Int. J. Mol. Sci. 2023, 24, 9188. [Google Scholar] [CrossRef]
  107. Kandasamy, S.; Sahu, S.K.; Kandasamy, K. In Silico Studies on Fungal Metabolite against Skin Cancer Protein (4,5-Diarylisoxazole HSP90 Chaperone). Int. Sch. Res. Not. 2012, 2012, 626214. [Google Scholar] [CrossRef]
  108. Oviya, R.; Thiruvudainambi, S.; Ramamoorthy, V.; Vendan, R.T.; Vellaikumar, S. Gas Chromatography Mass Spectrometry (GCMS) Analysis of the Antagonistic Potential of Trichoderma hamatum against Fusarium oxysporum f. sp. cepae Causing Basal Rot Disease of Onion. J. Biol. Control 2022, 36, 17–30. [Google Scholar] [CrossRef]
  109. Sen, S.; Dehingia, M.; Talukdar, N.C.; Khan, M. Chemometric Analysis Reveals Links in the Formation of Fragrant Bio-Molecules during Agarwood (Aquilaria malaccensis) and Fungal Interactions. Sci. Rep. 2017, 7, 44406. [Google Scholar] [CrossRef] [PubMed]
  110. Ain, Q.U.; Asad, S.; Jamal, A.; Arif, M.; Mahmood-Ul-hassan, M. Phytochemical Analysis and Antifungal Activity of Gymnosperm against Fusarium Wilt of Banana. Appl. Ecol. Environ. Res. 2021, 19, 2477–2493. [Google Scholar] [CrossRef]
  111. O’Leary, J.; Hiscox, J.; Eastwood, D.C.; Savoury, M.; Langley, A.; McDowell, S.W.; Rogers, H.J.; Boddy, L.; Müller, C.T. The Whiff of Decay: Linking Volatile Production and Extracellular Enzymes to Outcomes of Fungal Interactions at Different Temperatures. Fungal Ecol. 2019, 39, 336–348. [Google Scholar] [CrossRef]
  112. Abu Zeid, I.M.; Al-Thobaiti, S.A.; EL Hag, G.A.; Alghamdi, S.A.; Umar, A.; Abdalla Ahmed Hamdi, O. Phytochemical and GC-MS Analysis of Bioactive Compounds from Balanites aegyptiaca. Acta Sci. Pharm. Sci. 2019, 3, 129–134. [Google Scholar] [CrossRef]
  113. Jiménez-Teja, D.; Daoubi, M.; Collado, I.G.; Hernández-Galán, R. Lipase-Catalyzed Resolution of 5-Acetoxy-1,2-dihydroxy-1,2,3,4-tetrahydronaphthalene. Application to the Synthesis of (+)-(3R,4S)-cis-4-Hydroxy-6-deoxyscytalone, a Metabolite Isolated from Colletotrichum acutatum. Tetrahedron 2009, 65, 3392–3396. [Google Scholar] [CrossRef]
  114. Zhang, Y.; Berman, A.; Shani, E. Plant Hormone Transport and Localization: Signaling Molecules on the Move. Annu. Rev. Plant Biol. 2023, 74, 453–479. [Google Scholar] [CrossRef]
  115. Yang, H.; Luo, P. Changes in Photosynthesis Could Provide Important Insight into the Interaction between Wheat and Fungal Pathogens. Int. J. Mol. Sci. 2021, 22, 8865. [Google Scholar] [CrossRef]
  116. Sebastian, J.; Hegde, K.; Kumar, P.; Rouissi, T.; Brar, S.K. Bioproduction of Fumaric Acid: An Insight into Microbial Strain Improvement Strategies. Crit. Rev. Biotechnol. 2019, 39, 817–834. [Google Scholar] [CrossRef]
  117. Vijay, K.; Hassan, S.; Govarthanan, M.; Kavitha, T. Biosurfactant Lipopeptides and Polyketide Biosynthetic Gene in Rhizobacterium Achromobacter kerstersii to Induce Systemic Resistance in Tomatoes. Rhizosphere 2022, 23, 100558. [Google Scholar] [CrossRef]
  118. Palani, V.; Shanmugasundaram, M.; Maluventhen, V.; Chinnaraj, S.; Liu, W.; Balasubramanian, B.; Arumugam, M. Phytoconstituents and Their Potential Antimicrobial, Antioxidant and Mosquito Larvicidal Activities of Goniothalamus wightii Hook. F. & Thomson. Arab. J. Sci. Eng. 2020, 45, 4541–4555. [Google Scholar] [CrossRef]
  119. Ratheesh, M.; Sunil, S.; Sheethal, S.; Jose, S.P.; Sandya, S.; Ghosh, O.S.N.; Rajan, S.; Jagmag, T.; Tilwani, J. Anti-Inflammatory and Anti-COVID-19 Effect of a Novel Polyherbal Formulation (Imusil) via Modulating Oxidative Stress, Inflammatory Mediators and Cytokine Storm. Inflammopharmacology 2022, 30, 173–184. [Google Scholar] [CrossRef]
  120. Aziz, S.D.A.; Jafarah, N.F.; Yusof, Z.N.B. Phytol-Containing Seaweed Extracts as Control for Ganoderma boninense. J. Oil Palm Res. 2019, 31, 238–247. [Google Scholar] [CrossRef]
  121. Park, H.B.; Lee, B.; Kloepper, J.W.; Ryu, C.M. One Shot-Two Pathogens Blocked: Exposure of Arabidopsis to Hexadecane, a Long Chain Volatile Organic Compound, Confers Induced Resistance against Both Pectobacterium carotovorum and Pseudomonas syringae. Plant Signal. Behav. 2013, 8, e24619. [Google Scholar] [CrossRef]
  122. Parmagnani, A.S.; Kanchiswamy, C.N.; Paponov, I.A.; Bossi, S.; Malnoy, M.; Maffei, M.E. Bacterial Volatiles (MVOC) Emitted by the Phytopathogen Erwinia amylovora Promote Arabidopsis thaliana Growth and Oxidative Stress. Antioxidants 2023, 12, 600. [Google Scholar] [CrossRef]
  123. Majrashi, T.A.; Sabt, A.; Abd El Salam, H.A.; Al-Ansary, G.H.; Hamissa, M.F.; Eldehna, W.M. An Updated Review of Fatty Acid Residue-Tethered Heterocyclic Compounds: Synthetic Strategies and Biological Significance. RSC Adv. 2023, 13, 13655–13682. [Google Scholar] [CrossRef]
  124. Zheng, L.; Yan, X.; Xu, J.; Chen, H.; Lin, W. Hymeniacidon Perleve Associated Bioactive Bacterium Pseudomonas sp. NJ6-3-1. Appl. Biochem. Microbiol. 2005, 41, 29–33. [Google Scholar] [CrossRef]
  125. Taghavi, N. Enhancement in Biodegradation of Thermoplastics Using UV-Pretreatment and Biosurfactant. Ph.D. Thesis, The University of Auckland, Auckland, New Zealand, 2021. [Google Scholar]
  126. Sehim, A.E.; Amin, B.H.; Yosri, M.; Salama, H.M.; Alkhalifah, D.H.; Alwaili, M.A.; Elghaffar, R.Y.A. GC-MS Analysis, Antibacterial, and Anticancer Activities of Hibiscus sabdariffa L. Methanolic Extract: In Vitro and In Silico Studies. Microorganisms 2023, 11, 1601. [Google Scholar] [CrossRef]
  127. Zhang, X.; Li, Q.; Xu, W.; Zhao, H.; Guo, F.; Wang, P.; Wang, Y.; Ni, D.; Wang, M.; Wei, C. Identification of MTP Gene Family in Tea Plant (Camellia sinensis L.) and Characterization of CsMTP8.2 in Manganese Toxicity. Ecotoxicol. Environ. Saf. 2020, 202, 110904. [Google Scholar] [CrossRef]
  128. Adesanwo, J.K.; Ajayi, I.S.; Ajayi, O.S.; Igbeneghu, O.A.; McDonald, A.G. Identification of Chemical Constituents and Evaluation of the Antibacterial Activity of Methanol Extract and Fractions of the Leaf of Melanthera scandens (Schum. et Thonn.) Roberty. J. Explor. Res. Pharmacol. 2019, 4, 31–40. [Google Scholar] [CrossRef]
  129. Hawar, S.N.; Taha, Z.K.; Hamied, A.S.; Al-Shmgani, H.S.; Sulaiman, G.M.; Elsilk, S.E. Antifungal Activity of Bioactive Compounds Produced by the Endophytic Fungus Paecilomyces sp. (JN227071.1) against Rhizoctonia solani. Int. J. Biomater. 2023, 2023, 2411555. [Google Scholar] [CrossRef]
  130. Idris, N. Potential of Hexadecanoic Acid as Antimicrobials in Bacteria and Fungi That Cause Decay in Mustard Greens Brassica juncea L. Int. J. Appl. Biol. 2022, 6, 36–42. [Google Scholar]
  131. Phukan, H.; Brahma, R.; Mitra, P.K. An Endophytic Fungus Associated with Kayea assamica (King & Prain): A Study on Its Molecular Phylogenetics and Natural Products. S. Afr. J. Bot. 2020, 134, 314–321. [Google Scholar] [CrossRef]
  132. Jiao, S.; Chen, W.; Wang, E.; Wang, J.; Liu, Z.; Li, Y.; Wei, G. Microbial Succession in Response to Pollutants in Batch-Enrichment Culture. Sci. Rep. 2016, 6, 21791. [Google Scholar] [CrossRef]
  133. Boadu, A.; Karpoormath, R.; Nlooto, M. Spondias Mombin: Biosafety and GC–MS Analysis of Anti-Viral Compounds from Crude Leaf Extracts. Adv. Tradit. Med. 2023, 1–24. [Google Scholar] [CrossRef]
  134. Firdaus, M.; Kartikaningsih, H.; Sulifah, U. Sargassum spp Extract Inhibits the Growth of Foodborne Illness Bacteria. AIP Conf. Proc. 2019, 2202, 020083. [Google Scholar] [CrossRef]
  135. Williams, A.; Langridge, H.; Straathof, A.L.; Muhamadali, H.; Hollywood, K.A.; Goodacre, R.; de Vries, F.T. Root Functional Traits Explain Root Exudation Rate and Composition across a Range of Grassland Species. J. Ecol. 2022, 110, 21–33. [Google Scholar] [CrossRef]
  136. Shahbaz, E.; Ali, M.; Shafiq, M.; Atiq, M.; Hussain, M.; Balal, R.M.; Sarkhosh, A.; Alferez, F.; Sadiq, S.; Shahid, M.A. Citrus Canker Pathogen, Its Mechanism of Infection, Eradication, and Impacts. Plants 2023, 12, 123. [Google Scholar] [CrossRef]
  137. Chuah, X.; Okechukwu, P.; Amini, F.; Teo, S. Eicosane, Pentadecane and Palmitic Acid: The Effects in In Vitro Wound Healing Studies. Asian Pac. J. Trop. Biomed. 2018, 8, 490–499. [Google Scholar] [CrossRef]
  138. Ghorbani, A.; Tafteh, M.; Roudbari, N.; Pishkar, L.; Zhang, W.; Wu, C. Piriformospora indica Augments Arsenic Tolerance in Rice (Oryza sativa) by Immobilizing Arsenic in Roots and Improving Iron Translocation to Shoots. Ecotoxicol. Environ. Saf. 2021, 209, 111793. [Google Scholar] [CrossRef]
  139. Laport, M.; Santos, O.; Muricy, G. Marine Sponges: Potential Sources of New Antimicrobial Drugs. Curr. Pharm. Biotechnol. 2009, 10, 86–105. [Google Scholar] [CrossRef]
  140. Dimmock, J.; Turner, W.; Baker, H. Antimicrobial Evaluation of Diastereoisomeric 2-Dimethylaminomethyl-6-phenylcyclohexanols and Related Esters. J. Pharm. Sci. Res. 1975, 64, 995–997. [Google Scholar] [CrossRef]
  141. Hostettmann–Kaldas, M.; Nakanishi, K. Moronic Acid, a Simple Triterpenoid Keto Acid with Antimicrobial Activity Isolated from Ozoroa mucronata. Planta Medica 1979, 37, 358–360. [Google Scholar] [CrossRef]
  142. Huang, Y.; Sun, C.; Guan, X.; Lian, S.; Li, B.; Wang, C. Butylated Hydroxytoluene Induced Resistance Against Botryosphaeria dothidea in Apple Fruit. Front. Microbiol. 2021, 11, 599062. [Google Scholar] [CrossRef]
  143. Qian, F.; Huang, X.; Su, X.; Bao, Y. Responses of Microbial Communities and Metabolic Profiles to the Rhizosphere of Tamarix ramosissima in Soils Contaminated by Multiple Heavy Metals. J. Hazard. Mater. 2022, 438, 129469. [Google Scholar] [CrossRef]
  144. Fathi, M.; Ghane, M.; Pishkar, L. Phytochemical Composition, Antibacterial, and Antibiofilm Activity of Malva sylvestris Against Human Pathogenic Bacteria. Jundishapur J. Nat. Pharm. Prod. 2022, 17, e114164. [Google Scholar] [CrossRef]
  145. Nautiyal, V.; Pradhan, S.; Dubey, R.C. In Silico Molecular Docking Analysis and ADME Prediction of Cow Urine Derived 1-Heneicosanol against Some Bacterial Proteins. Vegetos 2023, 38, 1–7. [Google Scholar] [CrossRef]
  146. Salim, S.A. Identification of Active Pharmaceutical Ingredients in Thevetia neriifolia Juss Leaf Callus Using Analysis of GC-MS. Indian J. Public Health Res. Dev. 2018, 9, 1019–1023. [Google Scholar]
  147. Li, J.; Wang, Y.; Zheng, L.; Li, Y.; Zhou, X.; Li, J.; Gu, D.; Xu, E.; Lu, Y.; Chen, X.; et al. The Intracellular Transporter AtNRAMP6 Is Involved in Fe Homeostasis in Arabidopsis. Front. Plant Sci. 2019, 10, 1124. [Google Scholar] [CrossRef]
  148. Angeli, A.; Petrou, A.; Kartsev, V.; Lichitsky, B.; Komogortsev, A.; Capasso, C.; Geronikaki, A.; Supuran, C.T. Synthesis, Biological and In Silico Studies of Griseofulvin and Usnic Acid Sulfonamide Derivatives as Fungal, Bacterial and Human Carbonic Anhydrase Inhibitors. Int. J. Mol. Sci. 2023, 24, 2802. [Google Scholar] [CrossRef]
  149. Xuan, T.D.; Roni, Y.; Andriana, Y.; Khanh, T.D.; Anh, T.T.T.; Kakar, K.; Haqani, M.I. Chemical Profile, Antioxidant Activities and Allelopathic Potential of Liquid Waste from Germinated Brown Rice. Allelopath. J. 2018, 45, 89–100. [Google Scholar] [CrossRef]
  150. Ahmad, K.S. Environmental Contaminant 2-Chloro-N-(2,6-diethylphenyl)-N-(methoxymethyl)acetamide Remediation via Xanthomonas axonopodis and Aspergillus niger. Environ. Res. 2020, 182, 109117. [Google Scholar] [CrossRef]
  151. Vázquez-Fuentes, S.; Pelagio-Flores, R.; López-Bucio, J.; Torres-Gavilán, A.; Campos-García, J.; de la Cruz, H.R.; López-Bucio, J.S. N-Vanillyl-Octanamide Represses Growth of Fungal Phytopathogens In Vitro and Confers Postharvest Protection in Tomato and Avocado Fruits against Fungal-Induced Decay. Protoplasma 2021, 258, 729–741. [Google Scholar] [CrossRef]
  152. Minerdi, D.; Maggini, V.; Fani, R. Volatile Organic Compounds: From Figurants to Leading Actors in Fungal Symbiosis. FEMS Microbiol. Ecol. 2021, 97, fiab067. [Google Scholar] [CrossRef]
  153. Kawle, P.R. Synthesis and Antituberculosis Action of Symmetric Acridin-9-yl-bisbenzothiazol-2-yl-amines. Indian J. Chem. IJC 2023, 62, 691–695. [Google Scholar] [CrossRef]
  154. Brodzka, A.; Kowalczyk, P.; Trzepizur, D.; Koszelewski, D.; Kramkowski, K.; Szymczak, M.; Wypych, A.; Lizut, R.; Ostaszewski, R. The Synthesis and Evaluation of Diethyl Benzylphosphonates as Potential Antimicrobial Agents. Molecules 2022, 27, 6865. [Google Scholar] [CrossRef]
Microorganisms 12 00405 g001
Figure 1. Growth of (a) Serendipita indica (Fungus) alone (b) in the presence of Zhihengliuella sp. ISTPL4 (Bacteria) on a Hill and Kaefer agar plate (c) morphology of S. indica spores visualized using scanning electron microscopy (SEM) at Magnification: 2910×; voltage: 10 Kv; scale: 10 µm. (d) Spore morphology of S. indica in presence of Z. sp. ISTPL4 at Magnification: 2000×; voltage: 10 Kv; scale: 10 µm.
Figure 1. Growth of (a) Serendipita indica (Fungus) alone (b) in the presence of Zhihengliuella sp. ISTPL4 (Bacteria) on a Hill and Kaefer agar plate (c) morphology of S. indica spores visualized using scanning electron microscopy (SEM) at Magnification: 2910×; voltage: 10 Kv; scale: 10 µm. (d) Spore morphology of S. indica in presence of Z. sp. ISTPL4 at Magnification: 2000×; voltage: 10 Kv; scale: 10 µm.
Microorganisms 12 00405 g001
Microorganisms 12 00405 g002
Figure 2. Growth of S. indica alone (a) under normal growth condition (2.9 ± 0.01 cm) (b) in As stress (1.6 ± 0.01 cm; 1.9 mM) (c) in presence of Z. sp. ISTPL4 under normal growth condition (2.5 ± 0.05 cm), (d) in presence of As stress (1.4 ± 0.03 cm; 2.4 mM) and (e) shows the difference in dry weight of S. indica alone, in the presence of arsenic stress, in combination with Z. sp. ISTPL4 and under arsenic stress after microbial inoculation. According to the student’s t-test, asterisks showed significant differences: ‘*’: p ≤ 0.05; ‘**’: p ≤ 0.01).
Figure 2. Growth of S. indica alone (a) under normal growth condition (2.9 ± 0.01 cm) (b) in As stress (1.6 ± 0.01 cm; 1.9 mM) (c) in presence of Z. sp. ISTPL4 under normal growth condition (2.5 ± 0.05 cm), (d) in presence of As stress (1.4 ± 0.03 cm; 2.4 mM) and (e) shows the difference in dry weight of S. indica alone, in the presence of arsenic stress, in combination with Z. sp. ISTPL4 and under arsenic stress after microbial inoculation. According to the student’s t-test, asterisks showed significant differences: ‘*’: p ≤ 0.05; ‘**’: p ≤ 0.01).
Microorganisms 12 00405 g002
Microorganisms 12 00405 g003
Figure 3. Confocal microscopy analysis shows the spore morphology and spore size of (a) S. indica alone (b) under arsenic stress (1.9 mM) (c) in combination with Z. sp. ISTPL4 and, (d) in combination with Z. sp. ISTPL4 under arsenic stress (2.4 mM).
Figure 3. Confocal microscopy analysis shows the spore morphology and spore size of (a) S. indica alone (b) under arsenic stress (1.9 mM) (c) in combination with Z. sp. ISTPL4 and, (d) in combination with Z. sp. ISTPL4 under arsenic stress (2.4 mM).
Microorganisms 12 00405 g003
Microorganisms 12 00405 g004
Figure 4. Screening of arsenate transformation ability of S. indica and Z. sp. ISTPL4: Change in color from white to yellow indicates the reduction of arsenate to arsenite (a) S. indica (control): Arsenate plate without silver nitrate (b) S. indica (Test): Arsenate plate with silver nitrate (c) Z. sp. ISTPL4 (control): Arsenate plate without silver nitrate (d) Z. sp. ISTPL4 (test): Arsenate plate with silver nitrate.
Figure 4. Screening of arsenate transformation ability of S. indica and Z. sp. ISTPL4: Change in color from white to yellow indicates the reduction of arsenate to arsenite (a) S. indica (control): Arsenate plate without silver nitrate (b) S. indica (Test): Arsenate plate with silver nitrate (c) Z. sp. ISTPL4 (control): Arsenate plate without silver nitrate (d) Z. sp. ISTPL4 (test): Arsenate plate with silver nitrate.
Microorganisms 12 00405 g004
Microorganisms 12 00405 g005
Figure 5. GC-MS chromatogram of secondary metabolites secreted by (a) S. indica under normal growth conditions and, (b) in the presence of arsenic.
Figure 5. GC-MS chromatogram of secondary metabolites secreted by (a) S. indica under normal growth conditions and, (b) in the presence of arsenic.
Microorganisms 12 00405 g005
Microorganisms 12 00405 g006
Figure 6. GC-MS chromatogram of secondary metabolites secreted by (a) a combination of S. indica and Z. sp. ISTPL4 under normal growth conditions and, (b) in the presence of arsenic.
Figure 6. GC-MS chromatogram of secondary metabolites secreted by (a) a combination of S. indica and Z. sp. ISTPL4 under normal growth conditions and, (b) in the presence of arsenic.
Microorganisms 12 00405 g006
Microorganisms 12 00405 g007
Figure 7. (a) Venn diagram representing different and common metabolites released by S. indica under normal growth conditions and in the presence of arsenic with common metabolites mentioned in box. (b) Venn diagram representing different and common metabolites released by combination of S. indica and Z. sp. ISTPL4 under normal growth conditions and in the presence of arsenic with common metabolites mentioned in box.
Figure 7. (a) Venn diagram representing different and common metabolites released by S. indica under normal growth conditions and in the presence of arsenic with common metabolites mentioned in box. (b) Venn diagram representing different and common metabolites released by combination of S. indica and Z. sp. ISTPL4 under normal growth conditions and in the presence of arsenic with common metabolites mentioned in box.
Microorganisms 12 00405 g007
Microorganisms 12 00405 g008
Figure 8. Gas chromatography-mass spectrometry (GC-MS) spectrum comparison (a) clustered heatmap of common metabolites secreted by S. indica alone under normal growth conditions and in presence of As stress (b) heatmap showing common metabolites secreted by combination of S. indica and Z. sp. ISTPL4 under normal growth conditions and in presence of As stress; heatmap ranging from red to blue shows high to low abundance of metabolites detected.
Figure 8. Gas chromatography-mass spectrometry (GC-MS) spectrum comparison (a) clustered heatmap of common metabolites secreted by S. indica alone under normal growth conditions and in presence of As stress (b) heatmap showing common metabolites secreted by combination of S. indica and Z. sp. ISTPL4 under normal growth conditions and in presence of As stress; heatmap ranging from red to blue shows high to low abundance of metabolites detected.
Microorganisms 12 00405 g008
Microorganisms 12 00405 g009
Figure 9. Schematic representation of arsenic uptake and efflux by S. indica and Z. sp. ISTPL4.
Figure 9. Schematic representation of arsenic uptake and efflux by S. indica and Z. sp. ISTPL4.
Microorganisms 12 00405 g009
Table 1. List of common metabolites secreted by S. indica alone and in combination with Z. sp. ISTPL4 under normal growth conditions and in presence of As stress.
Table 1. List of common metabolites secreted by S. indica alone and in combination with Z. sp. ISTPL4 under normal growth conditions and in presence of As stress.
S. No.Metabolites
(S. indica/S. indica; As)		Metabolites
(S. indica + Z. sp. ISTPL4/S. indica + Z. sp. ISTPL4; As)
12,4-Di-tert-butyl-phenol) phosphate2,4-Di-tert-butyl-phenol) phosphate
2Cyclo(L-prolyl-L-valine)Cyclo(L-prolyl-L-valine)
31,2-Benzenedicarboxylic acid, bis (2-methyl propyl) ester1,2-Benzenedicarboxylic acid, bis (2-methyl propyl) ester
47,9-Di-tert-butyl-1-oxaspiro (4,5) deca-a-6,9-diene-2,8-dione7,9-Di-tert-butyl-1-oxaspiro (4,5) deca-a-6,9-diene-2,8-dione
5Hexadecenoic acid, methyl esterHexadecenoic acid, methyl ester
6Pyrrole[1,2-a]pyrazine-1,4-dione, hexahyd dro-3-(2-methyl propyl)octadecanoic acid, 3-oxo-, ethyl ester
71,2-Benzenedicarboxylic acid, butyl octyl esterOlean-18-ene
8Methyl stearateL-Proline
92-Ethylbutyric acid, eicosyl esterGlycerol 1-palmitate
102-(4-Hydroxy-4-methyl-tetrahydro-pyran-3-ylamino)-3-(1H-indol-2-yl)-propionic acidHexadecanoic acid, 2-hydroxy-1-(hydroxymethyl)ethyl ester
11LycopeneOctadecanoic acid, 2,3-dihydroxypropy ester
12Hexadecanoic acid, 2-hydroxy-1-(hydro oxymethyl) ethyl esterMethyl stearate
13Bis(2-ethylhexyl) phthalatePyrrolo[1,2-a]pyrazine-1,4-dione, hexa hydro-3-(2-methylpropyl)-
14Octocrylene 2-Propenoic acid,Tetradecane
15Octadecanoic acid, 2,3-dihydroxypropyl esterEicosane
16Squalene e 2,6,10,14,18,22-Tetracosahexaene,Heneicosane
17Phenol, 2,4-bis (1,1-dimethyl ethyl)-, phosphite
18Tris (2,4-di-tert-butyl phenyl) phosphate
19Octahydro-2H-pyrido(1,2-a)pyrimidin-2-one
20Olean-18-ene
21l-Leucine
22L-Proline
23Ergotaman-3′,6′,18-trione
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Sharma, N.; Koul, M.; Joshi, N.C.; Dufossé, L.; Mishra, A. Fungal-Bacterial Combinations in Plant Health under Stress: Physiological and Biochemical Characteristics of the Filamentous Fungus Serendipita indica and the Actinobacterium Zhihengliuella sp. ISTPL4 under In Vitro Arsenic Stress. Microorganisms 2024, 12, 405. https://doi.org/10.3390/microorganisms12020405

AMA Style

Sharma N, Koul M, Joshi NC, Dufossé L, Mishra A. Fungal-Bacterial Combinations in Plant Health under Stress: Physiological and Biochemical Characteristics of the Filamentous Fungus Serendipita indica and the Actinobacterium Zhihengliuella sp. ISTPL4 under In Vitro Arsenic Stress. Microorganisms. 2024; 12(2):405. https://doi.org/10.3390/microorganisms12020405

Chicago/Turabian Style

Sharma, Neha, Monika Koul, Naveen Chandra Joshi, Laurent Dufossé, and Arti Mishra. 2024. "Fungal-Bacterial Combinations in Plant Health under Stress: Physiological and Biochemical Characteristics of the Filamentous Fungus Serendipita indica and the Actinobacterium Zhihengliuella sp. ISTPL4 under In Vitro Arsenic Stress" Microorganisms 12, no. 2: 405. https://doi.org/10.3390/microorganisms12020405

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop