Skip to main content
Download PDF

Isolation and identification of antifungal, antibacterial and nematocide agents from marine bacillus gottheilii MSB1

BMC Biotechnology volume 24, Article number: 92 (2024) Cite this article

Abstract

Pathogenic fungi employ numerous strategies to colonize plants, infect them, reduce crop yield and quality, and cause significant losses in agricultural production. The increasing use of chemical pesticides has led to various ecological and environmental issues, including the emergence of resistant weeds, soil compaction, and water pollution, all negatively impacting agricultural sustainability. Additionally, the extensive development of synthetic fungicides has adverse effects on animal and human health, prompting the exploration of alternative approaches and green strategies for phytopathogen control. Microorganisms living in sponges represent a promising source of novel bioactive secondary metabolites, potentially useful in developing new nematicidal and antimicrobial agents. This study focuses on extracting bioactive compounds from endosymbiotic bacteria associated with the marine sponge Hyrtios erect sp. (collected from NIOF Station, Hurghada, Red Sea, Egypt) using various organic solvents. Bacillus sp. was isolated and identified through 16 S rRNA gene sequencing. The biocidal activity of Bacillus gotheilii MSB1 extracts was screened against plant pathogenic bacteria, fungi, and nematodes. The n-butanol extract showed significant potential as a biological fungicide against Alternaria alternata and Fusarium oxysporum. Both n-hexane and ethyl acetate extracts exhibited negative impacts against the plant pathogenic bacteria Erwinia carotovora and Ralstonia solanacearum, whereas the n-butanol extract had a positive effect. Regarding nematicidal activity, ethyl acetate and n-butanol extracts demonstrated in-vitro activity against the root-knot nematode Meloidogyne incognita, which causes serious vegetable crop diseases, but the n-hexane extract showed no positive effects. The findings suggest that bioactive compounds from endosymbiotic bacteria associated with marine sponges, particularly B. gotheilii MSB1, hold significant potential as alternative biological control agents against plant pathogens. The n-butanol extract, in particular, displayed promising biocidal activities against various plant pathogenic fungi, bacteria, and nematodes. These results support further exploration and development of such bioactive compounds as sustainable, environmentally friendly alternatives to synthetic pesticides and fungicides in agricultural practices.

Peer Review reports

Introduction

Worldwide, approximately 40% of agricultural output is lost due to plant diseases, weeds, and pests. In the absence of pesticides, these crop losses would rise considerably. Furthermore, these crop-protection agents not only prevent pest damage but also play a key role in boosting yields [1].

Pesticides are toxic chemical compounds, combinations of substances, or biological agents that are deliberately introduced into the environment to manage, prevent, and eliminate populations of various plant-pathogenic organisms. These agents function by luring and then controlling pests. Over time, pests can evolve resistance to pesticides, generating different substances, including toxins that are detrimental to both plants and humans. The hazards linked to pesticide usage now outweigh their advantages. Moreover, pesticides have profound effects on non-target species, disrupting animal and plant biodiversity and impacting both aquatic and terrestrial food webs and ecosystems [2,3,4]. The unchecked application of pesticides has resulted in a decline of numerous terrestrial and aquatic animal and plant species [5]. This situation has underscored the significance of biologically active secondary metabolites in agricultural use, spurring the creation of new types of pesticides [6,7,8,9].

The marine environment has emerged as an exceptionally abundant source of powerful chemicals, with a multitude of species adapted to thrive in extreme conditions [10,11,12,13,14]. Marine organisms are particularly noteworthy for their capacity to produce bioactive compounds that exhibit significant antimicrobial, anticancer, anti-inflammatory, analgesic, immunomodulatory, antiallergy and antiviral properties [10, 15, 16].

Recent research underscores the significant potential of marine sponges as a source of bioactive compounds. Anteneh et al. [17]. discovered that marine sponges from South Australia host diverse bacteria capable of producing bioactive metabolites, with 70 out of 169 tested bacterial isolates showing antimicrobial activity against human pathogens such as Staphylococcus aureus and fungi. Notably, a novel compound from Streptomyces sp. was identified, highlighting these sponges’ potential as a source of new antibiotics. Similarly, Campana et al. [18]. revealed that sponges possess diverse microbial communities that play a critical role in the cycling of dissolved organic matter (DOM) in marine ecosystems. Using DNA-stable isotope probing and 16 S rRNA amplicon sequencing, they noted active DOM uptake by specific bacterial taxa, with PAUC34f, Poribacteria, and Chloroflexi identified as key players in organic matter degradation, while Nitrospirae may engage in mixotrophic metabolism.

Further, Sarjito et al. [19]. demonstrated the use of sponge-associated bacteria like Bacillus spp. to control vibriosis in shrimp, with chitosan encapsulation improving bacterial viability and shelf life. Bacillus altitudinis PH.1 encapsulated in chitosan showed high viability after 14 days at -20 °C and a strong anti-vibrio activity, suggesting chitosan as a promising preservation method. Wibowo et al. [20]. highlighted marine bacteria as a rich source of novel bioactive compounds against drug-resistant pathogens. Research between January 2016 and December 2021 focused on secondary metabolites, with Streptomyces and other Actinobacteria revealing compounds effective against MRSA, VRE, MDR-TB, and amphotericin B-resistant Candida albicans, indicating their potential in new drug development.

Additionally, Bibi et al. [21] noted sponges as rich sources of bioactive natural products synthesized by symbiotic bacteria, with approximately 5,300 natural compounds identified to date. These products are often produced due to environmental competition for space and nutrients. The review emphasizes sponge-microbe interactions, highlighting the significant industrial and pharmaceutical potential of sponge-associated bacteria. Hentschel et al. [22]. highlighted the diverse microbial communities within marine sponges, comprising close to 30 bacterial phyla and several archaeal lineages, which can constitute up to 35% of sponge biomass. The sequencing of the Amphimedon queenslandica genome has provided insights into animal evolution and sponge-symbiont interactions, reinforcing the importance of marine sponges in studying host-microbe relationships.

Sponges are known to produce a wide array of chemically diverse bioactive substances, such as sterols, terpenes, nucleosides, cyclic peptides, and alkaloids [10, 23]. Although sponges themselves synthesize many of these valuable compounds, their microbial symbionts also play a crucial role in their production [24]. A significant part of the biomass of many marine sponges is composed of dense and genetically diverse microbial communities [24, 25], which include bacteria, archaea, fungi, and microalgae [26,27,28].

Studies have shown that Bacillus species dominate the microbial communities within marine sponges [29,30,31,32]. These bacteria are particularly noted for producing a variety of antimicrobial peptides with diverse chemical structures, making them central to bacteriocin research. Bacillus strains exhibit the broadest array of agriculturally beneficial compounds with significant potential [33, 34]. They are also renowned for producing various antifungal compounds that control or suppress fungal pathogens [35,36,37]. Recently, volatile organic compounds (VOCs) synthesized by Bacillus species have been explored as a novel approach to managing plant fungal diseases [38,39,40,41,42,43,44]. These VOCs can diffuse between soil particles and spread extensively from their application sites, exerting inhibitory effects without direct contact between the VOC-producing microorganisms and target pathogens [45, 46]. Their potent antifungal properties, coupled with their safety for the environment and human health, make VOCs a promising and sustainable alternative to traditional fungicides for future plant pathogen control [47,48,49].

Alternaria alternata is a fungal pathogen responsible for early blight disease in tomatoes, potatoes, tobacco, and various other vegetables and crops, resulting in substantial agricultural losses [50, 51]. For instance, potatoes, one of the most crucial crops globally, can experience up to 80% annual yield reductions due to early blight in specific regions [38, 39]. At present, chemical fungicides are the most effective means to manage early blight. However, excessive and improper use of these fungicides has led to the development of resistant pathogens, threatening both food safety and human health [52, 53]. Fusarium species are another group of phytopathogens that impact numerous economically significant crops. Among them, Fusarium oxysporum is particularly widespread, with over 120 reported formae speciales [54]. To combat these diseases, a variety of agronomic practices have been devised, including biological control, cultural practices, and chemical interventions.

In this study, we isolated, purified, and characterized several active ingredients produced by marine bacteria, aiming to explore their potential as alternatives to chemical pesticides. The effectiveness of these isolated compounds was evaluated against two pathogenic fungi; Alternaria alternata and Fusarium oxysporum, as well as the root-knot nematode Meloidogyne incognita.

Materials and methods

All chemicals and microbial media used in this study were sourced from Becton Dickinson (Sparks, MD, USA) and Loba Chemie PVT. LTD (Mumbai, India), with additional chemicals purchased from Sigma-Aldrich (St. Louis, MO, USA).

Sponge collection, identification and storage

A marine sponge sample was collected from the Red Sea near Hurghada, Egypt, at a depth of 2 m, close to the National Institute of Oceanography and Fisheries Station (coordinates: N 27 17 07.45, E 33 46 26.50). The sponge was identified as Hyrtios erecta (Order Dictyoceratida, Family Thorectidae) thanks to Prof. Rob. W. M. van Soest from the Department of Marine Zoology at the Netherlands Centre for Biodiversity [55, 56]. To cleanse the specimens of loosely attached bacteria, they were initially rinsed with sterilized artificial seawater (ASW) [57] and then underwent surface sterilization using 70% alcohol. Following sterilization, the sponge samples were rapidly placed on dry ice, frozen, and subsequently stored at -20 °C.

Preparation of the bacterial culture media

Marine Nutrient Agar (MNA) was employed as a general nutrient-rich medium to culture various heterotrophic marine bacteria. These bacteria were subsequently subcultured on ISP Agar medium following established protocols [58, 59]. Each medium was supplemented with NaCl at a concentration of 2% (w/v). To inhibit fungal growth, nystatin was added at a concentration of 25 µg/ml, as described by Webster et al. [60]. The plates were then filled, inverted, and stored at 4 °C until further use.

Isolation and purification of the suspected bacterial strain(s)

A fresh sponge sample, approximately 1 cm³ in size, was thoroughly milled in a sterile mortar with 10 ml of sterile artificial seawater (ASW) for two to three minutes. The resultant homogenate was transferred into a sterile 15 ml test tube, creating a 10 − 1 dilution. A 100 µL aliquot from each dilution series was spread onto various isolation media using a 10-fold dilution approach. The plates were then aerobically incubated for 1–2 weeks at 30 °C. Unique colony morphotypes were repeatedly selected and sub-cultured to achieve pure cultures, identified by their colony homogeneity.

The purified isolates were subsequently inoculated into ISP Medium 2 (ISP2). The liquid cultures were incubated at 37 °C in a shaking incubator set at 160 rpm for 48–72 h. Following the incubation period, cells were harvested by centrifugation at 6000 × g for 15 min.

Morphological and molecular identification of selected bacterial strain using 16 S rRNA gene

The Bacillus sp. isolate underwent further identification through 16S rRNA gene sequence analysis, following a series of morphological, microscopic, and biochemical characterizations. The polymerase chain reaction (PCR) amplification of the 16S rRNA gene was performed using specific primers: 27f (5’-AGAGTTTGATCCTGGCTCAG-3’) and 1492r (5’-GGTTACCTTGTTACGACTT-3’) [61]. The entire genome was amplified using a PCR system cycler from Creacon (Holland, Inc.).

Extraction of bioactive secondary metabolites

Under optimal conditions, B. gottheilii MSB1 was cultured in liquid ISP2 media at 28 °C with continuous shaking at 200 rpm for 48 h. The cultures were then centrifuged at 6000 rpm for 15 min at 4 °C to separate the cells from the supernatant.

Subsequently, 1 L of the culture filtrate was subjected to liquid-liquid extraction using 250 ml each of ethyl acetate and n-butanol. The extractions were performed sequentially, starting with ethyl acetate, followed by n-butanol.

Each organic phase was individually separated and dried over anhydrous sodium sulphate. The drying process was carried out at room temperature (approximately 25 °C) to prevent any degradation of the bioactive compounds. The solvents were concentrated using a rotary evaporator (ROTAVAP, Büchi, Switzerland) conducted under reduced pressure at 40 °C. Each evaporation step took approximately 1 h to ensure complete removal of solvents.

The concentrated residues were then reconstituted in 10 ml of methanol, achieving a concentration of 1.7 mg/ml for the ethyl acetate extract and 1.5 mg/ml for the n-butanol extract. This resulted in a yield of crude precipitates of 17 mg from the ethyl acetate extraction and 15 mg from the n-butanol extraction.

GC/MS Analysis of B. gottheilii MSB1 Extracts

The GC/MS apparatus was utilized to identify biologically active compounds from the B. gottheilii MSB1 isolate. This analysis was conducted using a Gas Chromatograph (Agilent 7690 A) and a Mass Spectrometer (Agilent 5975 C with Triple Axis Detector) at the National Institute of Oceanography and Fisheries’ Alexandria Branch in Egypt. Specific conditions included: the mass spectrometer detector operating at 70 eV with a source temperature of 325 °C. The injector temperature was maintained at 300 °C, utilizing a splitless injection mode with an injection volume of 1 µl and a purge time of 2 min. Helium served as the carrier gas at a rate of 1.22 ml/min [62]. Separation was conducted on an HP-5MS 5% Phenyl Methyl Siloxane Column (Agilent 19091 S-433) measuring 30 m x 250 μm x 0.25 μm. The oven temperature program began with holding at 90 °C for 1 min, followed by an increase of 8 °C/min to reach 205 °C, held for another minute. It was then increased at 5 °C/min to 240 °C for one minute, and finally at 8 °C/min attaining a peak temperature of 300 °C, which was maintained for 30 min. The total duration of the run was 61.875 min. Following the run, the resulting mass spectra of the components were analyzed and compared.

Fungal isolation, purification and identification

Fungi were extracted from plant leaves and subsequently cultivated in a potato dextrose agar (PDA) medium, which was composed of 200 g of potato, 20 g of glucose, and distilled water for up to 1 L. The cultures were then incubated at 28 °C for a duration of 7 days. Total RNA was isolated from both treated and untreated fungal samples, with the treatment involving an n-butanol extract, following the protocol established by Chomczynski et al. [63].

Reverse transcription reaction-polymerase chain reaction (RT-PCR)

Complementary DNA (cDNA) was synthesized by reverse transcribing total RNA in a 20 µL reaction mixture. The components included: 3 µL of total RNA, 5 µL of oligo(dT) primer (10 pmol/µL), 2.5 µL of dNTPs (10 mM), 2.5 µL of buffer (10x), 0.3 µL of Reverse Transcriptase, and 6.7 µL of sterile distilled water to achieve a final volume of 20 µL. The mixture was gently mixed and placed in a thermocycler. The amplification program consisted of incubation at 37 °C for 1 h, followed by enzyme inactivation at 65 °C for 10 min, and then cooling to 4 °C. The resulting cDNA was stored at -20 °C for further use.

In this study, four primers (PR2, PR3, PR4, and PR5) were employed, as detailed in Table 1. The Real-Time PCR reaction mixture included: 10 µL of SYBR Green, 1 µL of 10 pmol/µL forward primer, 1 µL of 10 pmol/µL reverse primer, 1 µL of cDNA (50 ng), and sterile distilled water to make up a total volume of 20 µL. The Real-Time PCR cycling conditions were: an initial denaturation at 95 °C for 10 min; followed by 45 cycles at 95 °C for 10 s, annealing at 60 °C for 20 s, and extension at 72 °C for 20 s. Data acquisition occurred during the extension phase. This reaction was analyzed using the Rotor-Gene 6000 system from Qiagen (USA).

The difference in quantification cycle values (ΔΔCT) between the reference and the target (treated) was calculated. The threshold cycle for each gene was determined using automated threshold analysis on the ABI system. Gene expression levels were quantified according to the method described by Livak et al. [64]. The CT value for each target gene was normalized to the CT value of the reference gene to obtain ΔCT(target).

Table 1 The specific primers of defense genes used in real-time PCR
Full size table

Statistical analysis

In this study examining the antimicrobial and nematicidal activities of B. gottheilii MSB1 extracts, we utilized statistical approaches to substantiate our findings and ensure scientific rigor. Specifically, the inhibition zones and nematicidal mortality percentages were subjected to one-way analysis of variance (ANOVA) to detect significant differences among treatments. This approach enabled us to assess the relative effectiveness of each extract type (n-butanol, n-hexane, and ethyl acetate) against plant pathogens and nematodes. When ANOVA indicated significant differences at a confidence level of p < 0.05, Tukey’s Honest Significant Difference (HSD) test was subsequently applied. This post-hoc analysis allowed us to determine pairwise differences among group means, providing a clearer understanding of the superior efficacy of particular extracts over others.

Additionally, statistical metrics such as least significant difference (LSD) and confidence intervals were calculated to enhance the reliability of our findings, offering insights into the precision and consistency of the observed effects. Statistical analyses were conducted using SPSS software (version 25), facilitating a robust examination of the dataset and ensuring data integrity. The use of these statistical tools enabled us to critically evaluate the potential of B. gottheilii MSB1 extracts as viable alternatives to conventional chemical pesticides, grounding our claims in quantitative evidence and supporting the exploration of environmentally friendly biocontrol solutions.

Results

The purpose of this study was to assess the ability of marine bacteria associated with sponges to produce antifungal and nematocidal compounds.

Phylogenetic analysis of the selected bacillus sp. isolate

The 16 S rRNA gene sequences were used to identify the chosen isolate. Nucleotide sequence analysis was conducted using the BlastN tool on the NCBI server. The Bacillus sp. isolate, identified as B. gottheilii MSB1, has a sequence length of 1369 bp (Figs: 1, 2 and 3). The sequence of the identified bacterial strain has been submitted to GenBank with the accession number KU199821.

Fig. 1
figure 1

Agarose gel electrophoresis of the amplified region of the isolate Bacillus sp. specific genes with approx. 1369 bp. The full, uncropped gel is shown in the supplementary file, Fig. S1

Full size image
Fig. 2
figure 2

phylogenetic tree for B. gottheilii MSB1 according to specific gene sequencing data

Full size image
Fig. 3
figure 3

B. gottheilii MSB1 cells by scanning electron microscope (SEM)

Full size image

GC/MS analysis of B. gottheilii MSB1 ethyl acetate extract

Using the GC/MS technique, four different chemicals were identified in the ethyl acetate extract of B. gottheilii MSB1 (Table 2; Fig. 3). The identified compounds include 3,5-Di-tert-butylphenol (20.4%), Ethyl 14-methyl-hexadecanoate (4.99%), Phthalic acid isobutyl octadecyl ester (4.83%), and Ethyl 12-oxododecanoate (4.65%).

Figure 3. B. gottheilii MSB1 cells by scanning electron microscope (SEM).

Table 2 GC/MS analysis of ethyl acetate extract of BGMSB1
Full size table

GC/MS analysis of B. gottheilii MSB1 n-butanol extract

The chemical composition of the n-butanol extract from B. gottheilii MSB1 is detailed in Table 3. Using GC/MS, seventeen components were identified in the n-butanol extract. The predominant compounds were Benzeneacetamide (70.0%), 2-Hydroxy-1-[(palmitoyloxy)methyl]ethyl palmitate (36.4%), 3-Methylbutanamide (23.1%), 2,6-Di-tert-butylphenol (9.23%), Ethyl cis, cis-9,12-octadecadienoate (11.7%), (7Z)-7-Nonenamide (9.27%), 2-Methylpropyl hexadecanoate (6.68%), 2-Propyl-1-heptanol (6.03%), 1-Hexadecanol (5.08%), 3,3-Dimethyl-6-(methylsulfanyl)-8-(4-morpholinyl)-3,4-dihydro-1 H-thiopyrano[3,4-c] pyridine-5-carbonitrile (4.65%), (5E)-5-Icosene (3.51%), and (9E)-9-Hexadecen-1-ol (3.19%).

Table 3 GC/MS analysis of B. Gottheilii MSB1 n-butanol extract
Full size table

While this analysis successfully identifies several compounds within the extract, it remains essential to delve deeper into how these compounds exert their biological effects. Future research should prioritize elucidating the underlying mechanisms by which these compounds may disrupt fungal or bacterial growth. Understanding these mechanisms will significantly enhance the study’s scientific contribution and provide insight into potential applications for these bioactive compounds in medical or agricultural fields.

Antibacterial and nematicidal activity of B. gottheilii MSB1 extracts

The antibacterial activity of n-hexane and ethyl acetate extracts from B. gottheilii MSB1 showed no significant impact against plant pathogenic bacteria such as Erwinia carotovora and Ralstonia solanacearum. However, the n-butanol extract demonstrated positive effects, inhibiting these bacteria with inhibition zones of 17 mm and 19 mm, respectively. Erwinia carotovora causes disease in a wide variety of agricultural and horticultural crops, including carrots, cabbage, cucumbers, onions, tomatoes, lettuce, and ornamental plants such as iris. Ralstonia solanacearum is responsible for causing brown (wilt) potato rot. These pathogens continuously attack potatoes and other vegetable crops both in fields and in storage, posing significant agricultural concerns (Table 4).

Table 4 The antibacterial activity for plant pathogenic bacteria
Full size table

In addition, ethyl acetate and n-butanol extracts exhibited in-vitro nematicidal activity against the root-knot nematode (Meloidogyne incognita), which causes serious diseases in vegetable crops. The ethyl acetate extract showed a 90.5% reduction in nematode activity after 12 h and 100% reduction after 24 h and 7 days. The n-butanol extract showed an 85.7% reduction after 12 h and 24 h, and a 90.5% reduction after 7 days. In contrast, the n-hexane extract showed no significant effects (Table 5). We employed a negative control consisting of only the testing medium without any extracts to establish a baseline for natural nematode mortality, which remained consistently low (4.2% mortality across all time points), confirming that the observed reductions were due to the active compounds in the extracts.

Table 5 In-vitro nematicidal activity (Meloidogyne incognita), data are means of 3 replicates
Full size table

Antifungal activity of B. gottheilii MSB1 n-butanol extract

The in vitro antifungal activity of the n-butanol extract against the plant pathogenic fungi Fusarium oxysporum and Alternaria alternata is presented in Table 6, with results expressed as IC50 values. Most of the tested compounds showed inhibitory effects against the fungi. Concerning Fusarium oxysporum, the extract exhibited significantly potent antifungal activity with an IC50 of 0.086 mg/L. Similarly, for Alternaria alternata, the extract demonstrated an IC50 of 0.061 mg/L (Figs; 4 and 5).

Table 6 The in vitro antifungal activity of B. Gottheilii MSB1 n-butanol extract against F. Oxysporum AND A. Alternaria by Mycelia radial growth technique
Full size table
Fig. 4
figure 4

The antifungal activity of the B. gottheilii MSB1 n-butanol extract (from left to right, 0, 4, 8, 12and 15 mg/L respectively) against F. oxysporum

Full size image
Fig. 5
figure 5

The antifungal activity of the B. gottheilii MSB1 n-butanol extract (from left to right, 0, 4, 8, 12 and 15 mg/L respectively) against A. Alternaria

Full size image

Quantitative real-time PCR (QRT-PCR)

Real-time PCR was employed to quantify the relative mRNA levels of four related protein genes in two plant pathogenic fungi, Alternaria alternata and Fusarium oxysporium, treated with extract No. 3. The analyzed defense genes include β-1, 3-glucanases (PR2), PR3, PR4, and thaumatin-like proteins (PR5). Results were normalized using the elongation factor β-actin gene as a reference or housekeeping gene. The quantitative analysis revealed that PR4 expression had the highest level with A. alternata (3.58) at times 8 and 12, respectively. Conversely, the lowest values (12) were observed with A. alternata for PR2. Moreover, for F. oxysporium, the highest expression levels were noted for PR5, PR3 and PR2 when treated with concentrate 4, whereas the lowest expression (PR4) was detected when treated with concentrate 12 (Figs: 6 and 7).

Fig. 6
figure 6

Histogram of the quantitative estimation for PR2, PR3, PR4 and PR5 gene expressions in Alternaria treated with B. gottheilii MSB1 n-butanol extract

Full size image
Fig. 7
figure 7

Histogram of the quantitative estimation for PR2, PR3, PR4 and PR5 gene expressions in Alternaria treated with B. gottheilii MSB1 n-butanol extract

Full size image

Discussion

Plant diseases caused by various microorganisms, including viruses, bacteria, fungi, protozoa, and nematodes, significantly affect agricultural practices, resulting in substantial crop losses [69, 70]. Fungal pathogens are a primary cause of plant diseases, infecting a majority of plants. Agrochemicals are vital in plant disease management to achieve a sustainable and productive agricultural system [71, 72]. However, the extensive use of chemicals has detrimental effects on human health, ecosystem functionality, and agricultural sustainability. Sustainable agriculture can be achieved by reducing or eliminating the use of fertilizers and agrochemicals, thereby minimizing environmental impact [73, 74].

Despite considerable efforts in managing plant pathogens, there is still significant potential to discover stable solutions. Various agronomical, biochemical, chemical, cultural, and biotechnological approaches have been employed to address plant pathogen issues, each with varying degrees of success. The use of bioactive secondary metabolites produced by biocontrol agents has emerged as a promising, eco-friendly approach for managing plant pathogens [75].

Sponge-associated bacteria and fungi are known to produce antimicrobial compounds with unique biologically important properties [76]. The majority of these antimicrobial compounds are produced by bacteria (90%), with fungi accounting for approximately 10% [77]. The interactions between sponges and bacteria in the marine environment are not well understood, but symbiotic relationships are generally believed to exist between sponges and microorganisms [78, 79].

Symbiotic functions attributed to microbial flora include nutrient acquisition, stabilization of the sponge skeleton, processing of metabolic waste, and secondary metabolite production [80]. Some bacteria are also thought to chemically defend their host against microbial infection [81]. Our study has confirmed that Bacillus sp. is predominantly represented, and its occurrence in the marine environment is well documented [82].

Sponge-associated Bacillus species, such as Bacillus cereus, Bacillus flexus, Bacillus pumilus, Bacillus licheniformis, Bacillus megaterium, Bacillus amyloliquefaciens, and Bacillus subtilis, offer significant potential as sources of antimicrobial substances [37, 83,84,85,86,87,88,89,90,91,92]. Numerous microbial isolates from these species have been reported to inhibit pathogenic reference strains in vitro and synthesize active substances effective against various infectious agents [39, 93,94,95]. These Bacillus species produce a wide array of pharmacologically and agriculturally active compounds and are recognized as industrially important microorganisms for their ability to generate numerous novel secondary metabolites [96, 97].

Optimizing culture conditions is essential to achieve high yields of these metabolites. Therefore, an attempt was made to optimize nutritional sources, including carbon, nitrogen, and minerals, as well as environmental factors such as time, pH, and temperature, for the production of antimicrobial metabolites by Bacillus strains [98, 99]. Competition among microbes for space and nutrients in the marine environment serves as a powerful selection pressure, encouraging marine microorganisms to produce natural products with significant agricultural, medical, and industrial applications [100].

The marine environment remains a critical area of research for scientists globally. The extreme conditions of temperature and salinity in marine ecosystems provide a unique and largely untapped microbiome [101]. These unique environmental conditions offer opportunities for the exploration of new microbes and their secondary metabolites [102].

The marine sponge Hyrtios erecta was found to harbor potent bacterial strains, particularly B. gottheilii MSB1, when screened against various pathogenic bacteria and fungi. The presence of antimicrobial activity was confirmed [103, 104]. Symbiotic and endophytic microorganisms have been identified as promising natural sources of antimicrobial and biocontrol agents (herbicides, pesticides), offering a viable approach to reducing the use of agrochemicals [105, 106].

GC/MS analysis of ethyl acetate and n-butanol extracts of B. gottheilii MSB1 revealed a diverse array of bioactive secondary metabolites with antimicrobial properties, which likely contribute to its strong antagonistic activity against Fusarium oxysporum and Alternaria alternata [107, 108]. Additionally, these extracts exhibited significant in-vitro nematicidal activity against the root-knot nematode (Meloidogyne incognita), with reduction rates of 90.5% after 12 h and 100% after 24 h and 7 days for ethyl acetate, and 85.7% after 12 and 24 h, and 90.5% after 7 days for n-butanol, while the n-hexane extract was ineffective [7, 109].

Among the potent identified bioactive secondary metabolites, the volatile phenolic compounds 2,4-ditert-butylphenol and 3,5-ditert-butylphenol displayed significant toxicity against a wide range of organisms, demonstrating antimicrobial, insecticidal, and nematicidal activities [110, 111]. The fatty acid derivatives, including butyl 13-methyltetradecanoate, 2-hydroxy-1-[(palmitoyloxy)methyl]ethyl palmitate, and others, produced by marine B. gottheilii MSB1, have been reported to exhibit antibacterial and antifungal properties [112, 113]. Other bioactive compounds such as 4-amino-6-hydroxy-2-methyl-5-nitrosopyrimidine, 3,3-dimethyl-6-(methylsulfanyl)-8-(4-morpholinyl)-3,4-dihydro-1 H-thiopyrano[3,4-c]pyridine-5-carbonitrile, and others demonstrated mild anxiolytic, antifungal, antibacterial, antioxidant, and antimalarial activities [114, 115].

The modes of action of many antimicrobials are complex and may affect multiple targets. The phenomenon of membrane bleeding has been observed with several antimicrobial agents [116]. For instance, phenolic and flavonoid compounds exert their effects through various mechanisms, including membrane disruption [117], protein binding, inhibition of protein synthesis, enzyme inhibition, and production of cell wall complexes [118]. Alkaloids may inhibit critical enzymes or act as DNA-intercalating agents [119]. Lysozymes affect bacterial cell walls and membranes, leading to membrane disruption, release of intracellular contents, and subsequent bacterial cell death [120].

Rongai et al. [121]. reported that certain plant groups, including Asteraceae, Oleaceae, and Lamiaceae, exhibit fungicidal action against Alternaria and Fusarium species. Chandel and Kumar also confirmed that the extract from Calliandra callothyrsus inhibits the growth of Alternaria alternata, Alternaria solani, Phoma sp., Fusarium sp., and Aspergillus sp., and promotes pea germination.

According to Daradka et al. [122], plants analyzed belonged to several families. Three dosages of plant extracts (10, 50, and 100 mg/ml) were tested against A. alternata and F. oxysporum by determining the inhibition zone of fungal mycelial growth using the disc-diffusion method on Potato Dextrose Agar (PDA), yielding significant results. The antifungal activity of plant extracts (50–100 mg/mL) against A. alternata and F. solani was assessed by monitoring mycelium radial growth and calculating the minimum inhibitory concentration (MIC) according to Lira-De et al. [123].

In the present study, we report the first isolation of B.gottheilii MSB1 from a marine sponge. Previously, this bacterium was isolated from mangrove sediment in Peninsular Malaysia [124]. B. gottheilii MSB1 is a Gram-positive, rod-shaped, motile, strictly aerobic, endospore-forming bacterium with potential applications in pharmaceutical production [125]. We investigated the antimicrobial and nematicidal activities of B. gottheilii MSB1 extracts in vitro, as well as its biocontrol efficacy against Fusarium oxysporum, Alternaria alternata, and Meloidogyne incognita under laboratory conditions. The results revealed that the extracts exhibit significant antimicrobial and nematicidal effects, which are consistent with previous studies [29, 126].

In considering the promising antimicrobial and nematicidal properties of B. gottheilii MSB1, it is essential to explore the broader implications of these findings, particularly in sustainable agriculture and pest management. The potential reduction in chemical pesticide use offers significant environmental and health benefits, aligning with global efforts to reduce chemical footprints in agricultural practices. However, the pathway to practical application is not without challenges. Implementing these biocontrol strategies on a large scale requires a thorough analysis of economic feasibility, logistical considerations, and farmer adoption hurdles. Factors such as production costs, delivery mechanisms, compatibility with existing agricultural systems, and regulatory approvals must be addressed to ensure that these biological solutions are not only effective but also accessible and attractive to farmers worldwide. Furthermore, understanding the long-term impact on ecosystems and crop yield stability will be crucial to guarantee that such innovations contribute positively to sustainable agricultural landscapes [127,128,129,130]. By engaging in a comprehensive evaluation of these elements, stakeholders can better facilitate the integration of B. gottheilii MSB1 into real-world agricultural settings, thereby maximizing its potential benefits .

This study demonstrates the potential of B. gottheilii MSB1, isolated from the marine sponge Hyrtios erecta, as a source of bioactive secondary metabolites with significant antimicrobial and nematicidal properties. These findings support the viability of marine microorganisms as eco-friendly alternatives for managing plant pathogens, reducing agrochemical use, and enhancing sustainable agriculture. The identified bioactive compounds, such as volatile phenolic compounds and fatty acid derivatives, show promising applications in agriculture and pharmaceuticals.

Nonetheless, the study has limitations; the activity of B. gottheilii MSB1 could vary with environmental conditions, which were not fully examined here. Furthermore, while several bioactive compounds were identified, the specific mechanisms by which they disrupt fungal or bacterial growth remain unclear. Future research should focus on elucidating these mechanisms to maximize the scientific contribution and potential applications of these compounds. Challenges such as large-scale production and purification also need addressing to facilitate practical use, ensuring B. gottheilii MSB1’s efficacy as a biocontrol agent across different environments.

Conclusions

This study confirms that Bacillus species, including B. gottheilii MSB1, exhibit potential as agents against plant pathogens, such as fungi and nematodes, suggesting their possible role as producers of antibacterial, antifungal, nematicidal, and biocontrol agents in agricultural contexts. While these findings highlight the potential of Bacillus species in integrated pest management strategies, it is important to acknowledge that the current research primarily reflects laboratory results. The translation of these findings to real-world agricultural applications requires further steps, including comprehensive field trials and toxicity assessments, to validate their efficacy and safety on a large scale. Additionally, the study does not yet explore how these applications may directly contribute to environmental sustainability and the United Nations’ Sustainable Development Goals (SDGs). Therefore, while promising, further research is essential to establish the practical, sustainable use of B. gottheilii MSB1 extracts in agriculture.

Data availability

All data generated or analyzed during this study are included in this manuscript and its information files and supplementary file.

Abbreviations

QRT-PCR:

Quantitative Real-Time PCR

PR2 :

β-1,3-glucanases

PR3 :

Pathogenesis-related protein 3

PR4 :

Pathogenesis-related protein 4

PR5 :

Thaumatin-like proteins

EF:

Elongation factor

VOC:

Volatile Organic Compounds

VOCs:

Volatile Organic Compounds (plural)

A. alternata :

Alternaria alternata

F. oxysporum :

Fusarium oxysporum

References

  1. Webster PJ, Moore AM, Loschnigg JP, Leben RR. Coupled ocean–atmosphere dynamics in the Indian Ocean during 1997–98. Nature. 1999;401(6751):356–60.

    Article  CAS  PubMed  Google Scholar 

  2. Mahmood I, Imadi SR, Shazadi K, Gul A, Hakeem KR. Effects of pesticides on environment. Plant soil Microbes: 1: Implications crop Sci 2016:253–69.

  3. Akhtar N, Wani AK, Mir T, Kumar N, Mannan M. Sapindus Mukorossi: Ethnomedicinal uses, phytochemistry, and pharmacological activities. Plant Cell Biotechnol Mol Biol. 2021;22:300–19.

    Google Scholar 

  4. Majewski MS, Coupe RH, Foreman WT, Capel PD. Pesticides in Mississippi air and rain: a comparison between 1995 and 2007. Environ Toxicol Chem. 2014;33(6):1283–93.

    Article  CAS  PubMed  Google Scholar 

  5. Helfrich CD, Li Y-F, Sharp ND, Sales AE. Organizational readiness to change assessment (ORCA): development of an instrument based on the Promoting Action on Research in Health Services (PARIHS) framework. Implement Sci. 2009;4:1–13.

    Article  Google Scholar 

  6. Debbab A, Aly AH, Lin WH, Proksch P. Bioactive compounds from marine bacteria and fungi. Microb Biotechnol. 2010;3(5):544–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Khan RAA, Najeeb S, Mao Z, Ling J, Yang Y, Li Y, Xie B. Bioactive secondary metabolites from Trichoderma spp. against phytopathogenic bacteria and root-knot nematode. Microorganisms. 2020;8(3):401.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Cárdenas-Laverde D, Barbosa-Cornelio R, Coy-Barrera E. Antifungal activity against Fusarium oxysporum of botanical end-products: an integration of chemical composition and antifungal activity datasets to identify antifungal bioactives. Plants. 2021;10(12):2563.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Rashad YM, Abdalla SA, Shehata AS. Aspergillus flavus YRB2 from Thymelaea hirsuta (L.) Endl., a non-aflatoxigenic endophyte with ability to overexpress defense-related genes against Fusarium root rot of maize. BMC Microbiol. 2022;22(1):229.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Karthikeyan A, Joseph A, Nair BG. Promising bioactive compounds from the marine environment and their potential effects on various diseases. J Genetic Eng Biotechnol. 2022;20(1):14.

    Article  Google Scholar 

  11. Macedo MWFS, Cunha NBd, Carneiro JA, Costa RAd A, SAd, Cardoso MH, Franco OL, Dias SC. Marine organisms as a rich source of biologically active peptides. Front Mar Sci. 2021;8:667764.

    Article  Google Scholar 

  12. Taylor MW, Radax R, Steger D, Wagner M. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev. 2007;71(2):295–347.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Gerwick WH, Fenner AM. Drug discovery from marine microbes. Microb Ecol. 2013;65:800–6.

    Article  CAS  PubMed  Google Scholar 

  14. Abdelrazek HM, Shams El-Din NG, Ghozlan HA, Sabry SA, Abouelkheir SS. Distribution and functional perspective analysis of epiphytic and endophytic bacterial communities associated with marine seaweeds, Alexandria shores, Egypt. BMC Microbiol. 2024;24(1):293.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Vinatoru M. An overview of the ultrasonically assisted extraction of bioactive principles from herbs. Ultrason Sonochem. 2001;8(3):303–13.

    Article  CAS  PubMed  Google Scholar 

  16. Putz A. P P Proksch 2010 Chemical defence in marine ecosystems. Annual Plant Reviews 39: Funct Biotechnol Plant Secondary Metabolites 39 162–213.

    CAS  Google Scholar 

  17. Anteneh YS, Yang Q, Brown MH, Franco CMM. Antimicrobial activities of Marine Sponge-Associated Bacteria. Microorganisms 2021, 9(1).

  18. Campana S, Busch K, Hentschel U, Muyzer G, de Goeij JM. DNA-stable isotope probing (DNA-SIP) identifies marine sponge-associated bacteria actively utilizing dissolved organic matter (DOM). Environ Microbiol. 2021;23(8):4489–504.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Sarjito Sarjito RA, Sabdaningsih A. The Evaluation of Marine Sponge–Associated Bacteria Microcapsule to Control Vibriosis in the Shrimp Culture International Journal of Chemical and Biochemical Sciences (ISSN 2226–9614) 2024, 25(19) 9–20.

  20. Wibowo JT, Bayu A, Aryati WD, Fernandes C, Yanuar A, Kijjoa A, Putra MY. Secondary metabolites from Marine-Derived Bacteria with antibiotic and Antibiofilm activities against drug-resistant pathogens. Mar Drugs 2023, 21(1).

  21. Bibi F, Faheem M, Azhar EI, Yasir M, Alvi SA, Kamal MA, Ullah I, Naseer MI. Bacteria from Marine sponges: a source of New drugs. Curr Drug Metab. 2017;18(1):11–5.

    Article  CAS  PubMed  Google Scholar 

  22. Hentschel U, Piel J, Degnan SM, Taylor MW. Genomic insights into the marine sponge microbiome. Nat Rev Microbiol. 2012;10(9):641–54.

    Article  CAS  PubMed  Google Scholar 

  23. Ebada SS, Proksch P. The chemistry of marine sponges∗. Handb Mar Nat Prod 2012:191.

  24. Laport M, Santos O, Muricy G. Marine sponges: potential sources of new antimicrobial drugs. Curr Pharm Biotechnol. 2009;10(1):86–105.

    Article  CAS  PubMed  Google Scholar 

  25. Food and Agriculture Organization of the United Nations. Sponges and Their Role in the Marine Environment; FAO: Rome I, 2017.: Sponges and Their Role in the Marine Environment. FAO: Rome, Italy 2017.

  26. Chin Y-W, Balunas MJ, Chai HB, Kinghorn AD. Drug discovery from natural sources. AAPS J. 2006;8:E239–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Ganesan A. The impact of natural products upon modern drug discovery. Curr Opin Chem Biol. 2008;12(3):306–17.

    Article  CAS  PubMed  Google Scholar 

  28. Mandal S, Kar NR, Jain AV, Yadav P. Natural products as sources of Drug Discovery: Exploration, Optimisation, and translation into clinical practice. Afr J Biol Sci (South Africa). 2024;6(9):2486–504.

    Google Scholar 

  29. Xiao S, Chen N, Chai Z, Zhou M, Xiao C, Zhao S, Yang X. Secondary metabolites from marine-derived Bacillus: a comprehensive review of origins, structures, and bioactivities. Mar Drugs. 2022;20(9):567.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Mawlankar R, Thorat MN, Krishnamurthi S, Dastager SG. Bacillus cellulasensis sp. nov., isolated from marine sediment. Arch Microbiol. 2016;198:83–9.

    Article  CAS  PubMed  Google Scholar 

  31. Sharma D, Singh SS, Baindara P, Sharma S, Khatri N, Grover V, Patil PB, Korpole S. Surfactin like broad spectrum antimicrobial lipopeptide co-produced with sublancin from Bacillus subtilis strain A52: dual reservoir of bioactives. Front Microbiol. 2020;11:1167.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Aboul-Ela HM, et al. Isolation, Antimicrobial and cytotoxic activity of Bioactive secondary metabolites from Marine Sponge-Associated Bacteria. Egypt J Aquat Biology Fisheries. 2023;27(5):249–63.

    Article  Google Scholar 

  33. Hamburger M, Hostettmann K. 7. Bioactivity in plants: the link between phytochemistry and medicine. Phytochemistry. 1991;30(12):3864–74.

    Article  CAS  Google Scholar 

  34. Molinski TF. NMR of natural products at the ‘nanomole-scale’. Nat Prod Rep. 2010;27(3):321–9.

    Article  CAS  PubMed  Google Scholar 

  35. Daniotti S, Re I. Marine biotechnology: challenges and development market trends for the enhancement of biotic resources in industrial pharmaceutical and food applications. A statistical analysis of scientific literature and business models. Mar Drugs. 2021;19(2):61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Hentschel U, Usher KM, Taylor MW. Marine sponges as microbial fermenters. FEMS Microbiol Ecol. 2006;55(2):167–77.

    Article  CAS  PubMed  Google Scholar 

  37. Béahdy J. Recent developments of antibiotic research and classification of antibiotics according to chemical structure. Adv Appl Microbiol. 1974;18:309–406.

    Article  Google Scholar 

  38. Chaurasia B, Pandey A, Palni LMS, Trivedi P, Kumar B, Colvin N. Diffusible and volatile compounds produced by an antagonistic Bacillus subtilis strain cause structural deformations in pathogenic fungi in vitro. Microbiol Res. 2005;160(1):75–81.

    Article  CAS  PubMed  Google Scholar 

  39. Zhang D, Yu S, Yang Y, Zhang J, Zhao D, Pan Y, Fan S, Yang Z, Zhu J. Antifungal effects of volatiles produced by Bacillus subtilis against Alternaria solani in potato. Front Microbiol. 2020;11:1196.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Harish B, Nagesha S, Ramesh B, Shyamalamma S, Nagaraj M, Girish H, Pradeep C, Shiva Kumar K, Tharun Kumar K, Pavan S. Molecular characterization and antifungal activity of lipopeptides produced from Bacillus subtilis against plant fungal pathogen Alternaria alternata. BMC Microbiol. 2023;23(1):179.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Poulaki EG, Tjamos SE. Bacillus species: factories of plant protective volatile organic compounds. J Appl Microbiol. 2023;134(3):lxad037.

    Article  PubMed  Google Scholar 

  42. Garrido A, Atencio LA, Bethancourt R, Bethancourt A, Guzmán H, Gutiérrez M, Durant-Archibold AA. Antibacterial activity of volatile organic compounds produced by the octocoral-associated bacteria bacillus sp. BO53 and Pseudoalteromonas sp. GA327. Antibiotics. 2020;9(12):923.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. He C-N, Ye W-Q, Zhu Y-Y, Zhou W-W. Antifungal activity of volatile organic compounds produced by Bacillus methylotrophicus and Bacillus thuringiensis against five common spoilage fungi on loquats. Molecules. 2020;25(15):3360.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Ling L, Luo H, Yang C, Wang Y, Cheng W, Pang M, Jiang K. Volatile organic compounds produced by Bacillus velezensis L1 as a potential biocontrol agent against postharvest diseases of wolfberry. Front Microbiol. 2022;13:987844.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Minerdi D, Bossi S, Gullino ML, Garibaldi A. Volatile organic compounds: a potential direct long-distance mechanism for antagonistic action of Fusarium oxysporum strain MSA 35. Environ Microbiol. 2009;11(4):844–54.

    Article  CAS  PubMed  Google Scholar 

  46. Heydari A, Pessarakli M. A review on biological control of fungal plant pathogens using microbial antagonists. J Biol Sci. 2010;10(4):273–90.

    Article  Google Scholar 

  47. Fialho MB, Toffano L, Pedroso MP, Augusto F, Pascholati SF. Volatile organic compounds produced by Saccharomyces cerevisiae inhibit the in vitro development of Guignardia citricarpa, the causal agent of citrus black spot. World J Microbiol Biotechnol. 2010;26:925–32.

    Article  CAS  Google Scholar 

  48. Parafati L, Vitale A, Restuccia C, Cirvilleri G. Performance evaluation of volatile organic compounds by antagonistic yeasts immobilized on hydrogel spheres against gray, green and blue postharvest decays. Food Microbiol. 2017;63:191–8.

    Article  CAS  PubMed  Google Scholar 

  49. Tilocca B, Cao A, Migheli Q. Scent of a killer: microbial volatilome and its role in the biological control of plant pathogens. Front Microbiol. 2020;11:41.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Martinko K, Ivanković S, Lazarević B, Đermić E, Đermić D. Control of early blight fungus (Alternaria alternata) in tomato by boric and phenylboronic acid. Antibiotics. 2022;11(3):320.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Seepe HA, Nxumalo W, Amoo SO. Natural products from medicinal plants against phytopathogenic Fusarium species: current research endeavours, challenges and prospects. Molecules. 2021;26(21):6539.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Dias MC. Phytotoxicity: an overview of the physiological responses of plants exposed to fungicides. J Bot. 2012;2012(1):135479.

    Google Scholar 

  53. Corkley I, Fraaije B, Hawkins N. Fungicide resistance management: maximizing the effective life of plant protection products. Plant Pathol. 2022;71(1):150–69.

    Article  Google Scholar 

  54. Baayen RP, O’Donnell K, Bonants PJ, Cigelnik E, Kroon LP, Roebroeck EJ, Waalwijk C. Gene genealogies and AFLP analyses in the Fusarium oxysporum complex identify monophyletic and nonmonophyletic formae speciales causing wilt and rot disease. Phytopathology. 2000;90(8):891–900.

    Article  CAS  PubMed  Google Scholar 

  55. Keller C. Die spongiefauna des rothen meeres. Wilhelm Engelmann; 1889.

  56. van Soest R, Hooper J, Hiemstra F. Taxonomy, phylogeny and biogeography of the marine sponge genus Acarnus (Porifera: Poecilosclerida). Beaufortia. 1991;42(3):49–88.

    Google Scholar 

  57. Sundaram Ravikumar SR, Samikan Krishnakumar SK, Inbaneson S, Murugesan Gnanadesigan MG. Antagonistic activity of marine actinomycetes from Arabian Sea coast. 2010.

  58. Mondol MAM, Shin HJ, Islam MT. Diversity of secondary metabolites from marine Bacillus species: chemistry and biological activity. Mar Drugs. 2013;11(8):2846–72.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Jahangirian H, Haron MJ, Shah MH, Abdollahi Y, Rezayi M, Vafaei N. Well diffusion method for evaluation of antibacterial activity of copper phenyl fatty hydroxamate synthesized from canola and palm kernel oils. Digest J Nanomaterials Biostructures. 2013;8(3):1263–70.

    Google Scholar 

  60. Webster N, Hill R. The culturable microbial community of the Great Barrier Reef sponge Rhopaloeides odorabile is dominated by an α-Proteobacterium. Mar Biol. 2001;138:843–51.

    Article  CAS  Google Scholar 

  61. Li W, Zhang Y, Liu Y, Yue F, Lu Y, Qiu H, Gao D, Gao Y, Wu Y, Wang Z. In vitro kinetic evaluation of the free radical scavenging ability of propofol. J Am Soc Anesthesiologists. 2012;116(6):1258–66.

    CAS  Google Scholar 

  62. Jerković I, Tuberoso CIG, Baranović G, Marijanović Z, Kranjac M, Svečnjak L, Kuś PM. Characterization of summer savory (Satureja hortensis L.) honey by physico-chemical parameters and chromatographic/spectroscopic techniques (GC-FID/MS, HPLC-DAD, UV/VIS and FTIR-ATR). Croat Chem Acta. 2015;88(1):15–22.

    Article  Google Scholar 

  63. Chomczynski P, Sacchi N. The single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction: twenty-something years on. Nat Protoc. 2006;1(2):581–5.

    Article  CAS  PubMed  Google Scholar 

  64. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 – ∆∆CT method. methods 2001, 25(4):402–408.

  65. Pasumarthy KK, Mukherjee SK, Choudhury NR. The presence of tomato leaf curl Kerala virus AC3 protein enhances viral DNA replication and modulates virus induced gene-silencing mechanism in tomato plants. Virol J. 2011;8:1–14.

    Article  Google Scholar 

  66. Floryszak-Wieczorek J, Arasimowicz-Jelonek M, Izbiańska K. The combined nitrate reductase and nitrite-dependent route of NO synthesis in potato immunity to Phytophthora infestans. Plant Physiol Biochem. 2016;108:468–77.

    Article  CAS  PubMed  Google Scholar 

  67. Wang X, El Hadrami A, Adam L, Daayf F. Differential activation and suppression of potato defence responses by Phytophthora infestans isolates representing US-1 and US‐8 genotypes. Plant Pathol. 2008;57(6):1026–37.

    Article  CAS  Google Scholar 

  68. Mukherjee AK, Lev S, Gepstein S, Horwitz BA. A compatible interaction of Alternaria brassicicola with Arabidopsis thaliana ecotype DiG: evidence for a specific transcriptional signature. BMC Plant Biol. 2009;9:1–11.

    Article  Google Scholar 

  69. Anderson PK, Cunningham AA, Patel NG, Morales FJ, Epstein PR, Daszak P. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol Evol. 2004;19(10):535–44.

    Article  PubMed  Google Scholar 

  70. Burketova L, Trda L, Ott PG, Valentova O. Bio-based resistance inducers for sustainable plant protection against pathogens. Biotechnol Adv. 2015;33(6):994–1004.

    Article  CAS  PubMed  Google Scholar 

  71. Waard MD, Georgopoulos S, Hollomon D, Ishii H, Leroux P, Ragsdale N, Schwinn F. Chemical control of plant diseases: problems and prospects. Annu Rev Phytopathol. 1993;31(1):403–21.

    Article  Google Scholar 

  72. Carvalho FP. Agriculture, pesticides, food security and food safety. Environ Sci Policy. 2006;9(7–8):685–92.

    Article  Google Scholar 

  73. Chou C. Role of allelopathy in sustainable agriculture: use of allelochemicals as naturally occurring bio-agrochemicals. Allelopathy J. 2010;25(1):3–16.

    Google Scholar 

  74. Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Woo SL, Lorito M. Trichoderma–plant–pathogen interactions. Soil Biol Biochem. 2008;40(1):1–10.

    Article  CAS  Google Scholar 

  75. Hyde K, Soytong K. The fungal endophyte dilemma. Fungal Divers. 2008;33(163):e173.

    Google Scholar 

  76. Liang J, She J, Fu J, Wang J, Ye Y, Yang B, Liu Y, Zhou X, Tao H. Advances in natural products from the marine-sponge-associated microorganisms with antimicrobial activity in the last decade. Mar Drugs. 2023;21(4):236.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Ashforth EJ, Fu C, Liu X, Dai H, Song F, Guo H, Zhang L. Bioprospecting for antituberculosis leads from microbial metabolites. Nat Prod Rep. 2010;27(11):1709–19.

    Article  CAS  PubMed  Google Scholar 

  78. Webster NS, Taylor MW. Marine sponges and their microbial symbionts: love and other relationships. Environ Microbiol. 2012;14(2):335–46.

    Article  CAS  PubMed  Google Scholar 

  79. Lee Y-K, Lee J-H, Lee H-K. Microbial symbiosis in marine sponges. J Microbiol. 2001;39(4):254–64.

    Google Scholar 

  80. Hentschel U, Hopke M Jr, Friedrich AB, Wagner M, Hacker BS Jr. Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol. 2002;68(9):4431–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Engel S, Jensen PR, Fenical W. Chemical ecology of marine microbial defense. J Chem Ecol. 2002;28:1971–85.

    Article  CAS  PubMed  Google Scholar 

  82. Ivanova EP, Vysotskii MV, Svetashev VI, Nedashkovskaya OI, Gorshkova NM, Mikhailov VV, Yumoto N, Shigeri Y, Taguchi T, Yoshikawa S. Characterization of Bacillus strains of marine origin. Int Microbiol. 1999;2(4):267–71.

    CAS  PubMed  Google Scholar 

  83. Aboul-Ela M, FA Azzam H, Shreadah NA, Kelly M. Antimicrobial activities of five bacterial isolates associated with two Red Sea sponges and their potential against multidrug-resistant bacterial pathogens. Egypt J Aquat Biology Fisheries. 2019;23(4):551–61.

    Article  Google Scholar 

  84. Sumi CD, Yang BW, Yeo I-C, Hahm YT. Antimicrobial peptides of the genus Bacillus: a new era for antibiotics. Can J Microbiol. 2015;61(2):93–103.

    Article  CAS  PubMed  Google Scholar 

  85. Nikapitiya C. Bioactive secondary metabolites from marine microbes for drug discovery. Adv Food Nutr Res. 2012;65:363–87.

    Article  PubMed  Google Scholar 

  86. Richardson LL, Goldberg WM, Kuta KG, Aronson RB, Smith GW, Ritchie KB, Halas JC, Feingold JS, Miller SL. Florida’s mystery coral-killer identified. Nature. 1998;392(6676):557–8.

    Article  CAS  Google Scholar 

  87. Stein T. Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol. 2005;56(4):845–57.

    Article  CAS  PubMed  Google Scholar 

  88. Santos OC, Pontes PV, Santos JF, Muricy G, Giambiagi-deMarval M, Laport MS. Isolation, characterization and phylogeny of sponge-associated bacteria with antimicrobial activities from Brazil. Res Microbiol. 2010;161(7):604–12.

    Article  CAS  PubMed  Google Scholar 

  89. Su P, Wang D-X, Ding S-X, Zhao J. Isolation and diversity of natural product biosynthetic genes of cultivable bacteria associated with marine sponge Mycale sp. from the coast of Fujian, China. Can J Microbiol. 2014;60(4):217–25.

    Article  CAS  PubMed  Google Scholar 

  90. Flemer B, Kennedy J, Margassery L, Morrissey J, O’Gara F, Dobson A. Diversity and antimicrobial activities of microbes from two Irish marine sponges, Suberites carnosus and Leucosolenia Sp. J Appl Microbiol. 2012;112(2):289–301.

    Article  CAS  PubMed  Google Scholar 

  91. Hentschel U, Schmid M, Wagner M, Fieseler L, Gernert C, Hacker J. Isolation and phylogenetic analysis of bacteria with antimicrobial activities from the Mediterranean sponges Aplysina aerophoba and Aplysina cavernicola. FEMS Microbiol Ecol. 2001;35(3):305–12.

    Article  CAS  PubMed  Google Scholar 

  92. Anand TP, Bhat AW, Shouche YS, Roy U, Siddharth J, Sarma SP. Antimicrobial activity of marine bacteria associated with sponges from the waters off the coast of South East India. Microbiol Res. 2006;161(3):252–62.

    Article  PubMed  Google Scholar 

  93. Nagai K, Kamigiri K, Arao N, Suzumura K-i, Kawano Y, Yamaoka M, Zhang H, Watanabe M, Suzuki K. YM-266183 and ym-266184, novel thiopeptide antibiotics produced by Bacillus cereus isolated from a marine sponge i. taxonomy, fermentation, isolation, physico-chemical properties and biological properties. J Antibiot. 2003;56(2):123–8.

    Article  CAS  Google Scholar 

  94. Suzumura K-I, Yokoi T, Funatsu M, Nagai K, Tanaka K, Zhang H, Suzuki K. YM-266183 and YM-266184, novel thiopeptide antibiotics produced by Bacillus cereus isolated from a marine sponge II. Structure elucidation. J Antibiot. 2003;56(2):129–34.

    Article  CAS  Google Scholar 

  95. Pabel CT, Vater J, Wilde C, Franke P, Hofemeister J, Adler B, Bringmann G, Hacker J, Hentschel U. Antimicrobial activities and matrix-assisted laser desorption/ionization mass spectrometry of Bacillus isolates from the marine sponge Aplysina aerophoba. Mar Biotechnol. 2003;5:424–34.

    Article  CAS  Google Scholar 

  96. Bibb MJ. Regulation of secondary metabolism in streptomycetes. Curr Opin Microbiol. 2005;8(2):208–15.

    Article  CAS  PubMed  Google Scholar 

  97. Schäfer H, Wink M. Medicinally important secondary metabolites in recombinant microorganisms or plants: progress in alkaloid biosynthesis. Biotechnol Journal: Healthc Nutr Technol. 2009;4(12):1684–703.

    Article  Google Scholar 

  98. Singh C, Parmar RS, Jadon P, Kumar A. Optimization of cultural conditions for production of antifungal bioactive metabolites by Streptomyces spp. isolated from soil. Int J Curr Microbiol Appl Sci. 2017;6(2):386–96.

    Article  CAS  Google Scholar 

  99. Rana M, Dahot MU. Optimization of culture conditions to produce secondary metabolites by Pleurotus Ostreatus. Pakistan J Biotechnol. 2017;14(2):251–6.

    Google Scholar 

  100. Pai A. A review on marine natural products and their application in modern medicine. Int J Green Pharm (IJGP) 2018, 12(01).

  101. Thomas TRA, Kavlekar DP, LokaBharathi PA. Marine drugs from sponge-microbe association—A review. Mar Drugs. 2010;8(4):1417–68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Srinivasan R, Kannappan A, Shi C, Lin X. Marine bacterial secondary metabolites: a treasure house for structurally unique and effective antimicrobial compounds. Mar Drugs. 2021;19(10):530.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Bibi F, Yasir M, Al-Sofyani A, Naseer MI, Azhar EI. Antimicrobial activity of bacteria from marine sponge Suberea Mollis and bioactive metabolites of Vibrio sp. EA348. Saudi J Biol Sci. 2020;27(4):1139–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Abdelmohsen UR, Pimentel-Elardo SM, Hanora A, Radwan M, Abou-El-Ela SH, Ahmed S, Hentschel U. Isolation, phylogenetic analysis and anti-infective activity screening of marine sponge-associated actinomycetes. Mar Drugs. 2010;8(3):399–412.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Palmieri D, Ianiri G, Del Grosso C, Barone G, De Curtis F, Castoria R, Lima G. Advances and perspectives in the use of biocontrol agents against fungal plant diseases. Horticulturae. 2022;8(7):577.

    Article  Google Scholar 

  106. Jacquet F, Jeuffroy M-H, Jouan J, Le Cadre E, Litrico I, Malausa T, Reboud X, Huyghe C. Pesticide-free agriculture as a new paradigm for research. Agron Sustain Dev. 2022;42(1):8.

    Article  Google Scholar 

  107. Vizcaino JA, Luis S, Basilio A, Vicente F, Gutierrez S, Hermosa MR, Monte E. Screening of antimicrobial activities in Trichoderma isolates representing three Trichoderma sections. Mycol Res. 2005;109(12):1397–406.

    Article  CAS  PubMed  Google Scholar 

  108. Tong X, Shen X-Y, Hou C-L. Antimicrobial activity of fungal endophytes from Vaccinium dunalianum var. Urophyllum. Sains Malaysiana. 2018;47(8):1685–92.

    Article  Google Scholar 

  109. Verdejo-Lucas S, Cortada L, Sorribas F, Ornat C. Selection of virulent populations of Meloidogyne javanica by repeated cultivation of Mi resistance gene tomato rootstocks under field conditions. Plant Pathol. 2009;58(5):990–8.

    Article  Google Scholar 

  110. Zhao F, Wang P, Lucardi RD, Su Z, Li S. Natural sources and bioactivities of 2, 4-di-tert-butylphenol and its analogs. Toxins. 2020;12(1):35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Gazoni VF, Balogun SO, Arunachalam K, Oliveira DM, Cechinel Filho V, Lima SR, Colodel EM, Soares IM, Ascêncio SD, de Oliveira Martins DT. Assessment of toxicity and differential antimicrobial activity of methanol extract of rhizome of Simaba Ferruginea A. St.-Hil. And its isolate canthin-6-one. J Ethnopharmacol. 2018;223:122–34.

    Article  CAS  PubMed  Google Scholar 

  112. Selvin J. Exploring the antagonistic producer Streptomyces MSI051: implications of polyketide synthase gene type II and a ubiquitous defense enzyme phospholipase A2 in the host sponge Dendrilla nigra. Curr Microbiol. 2009;58:459–63.

    Article  CAS  PubMed  Google Scholar 

  113. Graça AP, Viana F, Bondoso J, Correia MI, Gomes L, Humanes M, Reis A, Xavier JR, Gaspar H, Lage OM. The antimicrobial activity of heterotrophic bacteria isolated from the marine sponge Erylus deficiens (Astrophorida, Geodiidae). Front Microbiol. 2015;6:389.

    PubMed  PubMed Central  Google Scholar 

  114. Adnan M, Nazim Uddin Chy M, Mostafa Kamal A, Azad MOK, Paul A, Uddin SB, Barlow JW, Faruque MO, Park CH, Cho DH. 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(7):1367.

    Article  PubMed  PubMed Central  Google Scholar 

  115. Khatua S, Pandey A, Biswas SJ. Phytochemical evaluation and antimicrobial properties of Trichosanthes dioica root extract. J Pharmacognosy Phytochemistry. 2016;5(5):410–3.

    Google Scholar 

  116. Tsuchiya H. Membrane interactions of phytochemicals as their molecular mechanism applicable to the discovery of drug leads from plants. Molecules. 2015;20(10):18923–66.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Plaper A, Golob M, Hafner I, Oblak M, Šolmajer T, Jerala R. Characterization of quercetin binding site on DNA gyrase. Biochem Biophys Res Commun. 2003;306(2):530–6.

    Article  CAS  PubMed  Google Scholar 

  118. Zhang L, Kong Y, Wu D, Zhang H, Wu J, Chen J, Ding J, Hu L, Jiang H, Shen X. Three flavonoids targeting the β-hydroxyacyl‐acyl carrier protein dehydratase from Helicobacter pylori: crystal structure characterization with enzymatic inhibition assay. Protein Sci. 2008;17(11):1971–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Tanaka J, Da Silva C, De Oliveira A, Nakamura C, Dias Filho B. Antibacterial activity of indole alkaloids from Aspidosperma Ramiflorum. Braz J Med Biol Res. 2006;39:387–91.

    Article  CAS  PubMed  Google Scholar 

  120. Saito H, Sakakibara Y, Sakata A, Kurashige R, Murakami D, Kageshima H, Saito A, Miyazaki Y. Antibacterial activity of lysozyme-chitosan oligosaccharide conjugates (LYZOX) against Pseudomonas aeruginosa, Acinetobacter baumannii and Methicillin-resistant Staphylococcus aureus. PLoS ONE. 2019;14(5):e0217504.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Rongai D, Milano F, Sciò E. Inhibitory effect of plant extracts on conidial germination of the phytopathogenic fungus Fusarium oxysporum. 2012.

  122. Daradka HM, Saleem A, Obaid WA. Antifungal effect of different plant extracts against phytopathogenic fungi alternaria alternata and fusarium oxysporum isolated from tomato plant. J Pharm Res Int. 2021;33(31A):188–97.

    Article  Google Scholar 

  123. Lira-De León KI, Ramírez-Mares MV, Sánchez-López V, Ramírez-Lepe M, Salas-Coronado R, Santos-Sánchez NF, Valadez-Blanco R, Hernández-Carlos B. Effect of crude plant extracts from some oaxacan flora on two deleterious fungal phytopathogens and extract compatibility with a biofertilizer strain. Front Microbiol. 2014;5:383.

    PubMed  PubMed Central  Google Scholar 

  124. Auta H, Emenike C, Fauziah S. Screening of Bacillus strains isolated from mangrove ecosystems in Peninsular Malaysia for microplastic degradation. Environ Pollut. 2017;231:1552–9.

    Article  CAS  PubMed  Google Scholar 

  125. Seiler H, Wenning M, Schmidt V, Scherer S. Bacillus gottheilii sp. nov., isolated from a pharmaceutical manufacturing site. Int J Syst Evol MicroBiol. 2013;63(Pt3):867–72.

    Article  CAS  PubMed  Google Scholar 

  126. Sholkamy EN, Muthukrishnan P, Abdel-Raouf N, Nandhini X, Ibraheem IB, Mostafa AA. Antimicrobial and antinematicidal metabolites from Streptomyces cuspidosporus strain SA4 against selected pathogenic bacteria, fungi and nematode. Saudi J Biol Sci. 2020;27(12):3208–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Wink M. Modes of Action of Herbal Medicines and Plant secondary metabolites. Med (Basel Switzerland). 2015;2(3):251–86.

    CAS  Google Scholar 

  128. Cragg GM, Newman DJ. Natural products: a continuing source of novel drug leads. Biochim Biophys Acta. 2013;1830(6):3670–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Saklani A, Kutty SK. Plant-derived compounds in clinical trials. Drug Discovery Today. 2008;13(3–4):161–71.

    Article  CAS  PubMed  Google Scholar 

  130. Koehn FE, Carter GT. The evolving role of natural products in drug discovery. Nat Rev Drug Discovery. 2005;4(3):206–20.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Many thanks to Prof. Rob. W. M. van Soest at Department of Marine Zoology, Netherlands Centre for Biodiversity, the Netherlands, Prof. Michele Kelly at National Institute of Water and Atmospheric Research (NIWA) Ltd., Auckland, New Zealand for the helping in the taxonomy of sponge samples. Also, we would like to thank Dr. Rehab Yassin Ghareeb, Associate professor at Plant Protection and Bimolecular Diagnosis Department (ALCRI), City of Scientific Research and Technological Applications (SRTA, City), for her helpful and deep thanks to Prof. Faida Hassan Ali Bamane Professor of Organic Chemistry, Department of Clinical Biochemistry, Faculty of Medicine, Jeddah, King Abdullaziz University, K. S. A. for her kind help and vital support to achieve the goals of this work. This work was experimentally supported by Marine Biotechnology and Natural Product Lab, Environment Division, National Institute of Oceanography and Fisheries and Green Materials Technology Department, Environment and Natural Materials Research Institute (ENMRI), City of Scientific Research and Technological Applications (SRTA-City), New Borg El-Arab City, Alexandria 21934, Egypt, with Plant Protection and Biomolecular Diagnosis Department, City of Scientific Research and Technological Applications.

Funding

Not applicable.

Open access funding provided by The Science, Technology & Innovation Funding Authority (STDF) in cooperation with The Egyptian Knowledge Bank (EKB).

Author information

Author notes

  1. Ahmed. S. Shehata and Ahmed A. Saleh contributed equally to this work.

Authors and Affiliations

  1. Marine Biotechnology and Natural Product Lab., Environment Division, National Institute of Oceanography and Fisheries, NIOF, Alexandria City, Egypt

    Ahmed. S. Shehata & Aida M. Farag

  2. Green Materials Technology Department, Environment and Natural Materials Research Institute (ENMRI), City of Scientific Research and Technological Applications (SRTA), New Borg El-Arab City, Alexandria, 21934, Egypt

    Ahmed. S. Shehata

  3. Plant Protection and Biomolecular Diagnosis Department, Arid Lands Cultivation Research Institute, City of Scientific Research and Technological Applications, New Borg El-Arab City, Alexandria, 21934, Egypt

    Marwa A. Samy, Sherien E. Sobhy & Elsayed E. Hafez

  4. Department of Nanomaterial Science, Zewil City, Egypt

    Ibrahim M. El-Sherbiny

  5. Animal and Fish Production Department, Faculty of Agriculture (Al-Shatby), Alexandria University, Alexandria City, 11865, Egypt

    Ahmed A. Saleh

  6. Chemistry Department, Faculty of Science, Mansoura University, Mansoura, 35316, Egypt

    Mamdouh Abdel-Mogib

  7. College of Fisheries and Aquaculture Technology, Arab Academy for Science, Technology and Maritime Transport, Abu Qir, Alexandria, Egypt

    Haiam M. Aboul-Ela

Authors
  1. Ahmed. S. Shehata
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Marwa A. Samy
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Sherien E. Sobhy
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Aida M. Farag
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Ibrahim M. El-Sherbiny
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Ahmed A. Saleh
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Elsayed E. Hafez
    View author publications

    You can also search for this author inPubMed Google Scholar

  8. Mamdouh Abdel-Mogib
    View author publications

    You can also search for this author inPubMed Google Scholar

  9. Haiam M. Aboul-Ela
    View author publications

    You can also search for this author inPubMed Google Scholar

Contributions

A.S.S., M.A.S., S.E.S., A.M.F and A.A.S.: Writing – review & editing, Writing – original draft, Methodology, Investigation, Formal analysis, Data curation. I.M.E., E.E.H., M.A.M., H.M.A. : Writing – review & editing, Supervision, Investigation, Formal analysis, Conceptualization. All authors.

Corresponding author

Correspondence to Ahmed A. Saleh.

Ethics declarations

Ethics approval and consent to participate

The Faculty of Science, El-Menoufia University, Egypt, oversaw and sanctioned the sampling procedures for this experiment (Approval Code: MU08220231117). All methods and protocols employed adhered strictly to the Guide for the Care and Use of Agricultural Samples as stipulated by El-Menoufia University.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Material 1

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shehata, A.S., Samy, M.A., Sobhy, S.E. et al. Isolation and identification of antifungal, antibacterial and nematocide agents from marine bacillus gottheilii MSB1. BMC Biotechnol 24, 92 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12896-024-00920-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12896-024-00920-y

Keywords

BMC Biotechnology

ISSN: 1472-6750

Contact us