Cost-effective phytohormone extraction of Sargassum swartzii from the Persian Gulf using Magnetic Ionic Liquid

doi:10.21203/rs.3.rs-4149369/v1

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Cost-effective phytohormone extraction of Sargassum swartzii from the Persian Gulf using Magnetic Ionic Liquid

https://doi.org/10.21203/rs.3.rs-4149369/v1

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Introduction

Algae extracts are applicable as biofertilizers instead of chemical fertilizers in agriculture. Algae have a high content of plant hormones such as Gibberellin, Salicylic acid, Abscisic Acid, and Brassinosteroids are available in algae.

Objective

The main objective of this study is to increase the extraction yield and simultaneously extraction of hormones required for plant growth from Sargassum swartzii using Magnetic recoverable ionic liquid (IL).

Methods

Extraction is done by acidic digestion with acetic acid and then alkaline digestion with potassium hydroxide.

Results

The results showed the ionic liquid effect in extraction yield by 266 percent. The extracted phytohormones were analyzed by HPLC methods. High level of Gibberellin, Salicylic acid, Abscisic Acid and Brassinosteroids in improved algae extraction shows seaweed extract could be used as environmentally friendly liquid bio fertilizers to replace chemical fertilizers and could play a crucial role in organic farming on the way to sustainable agriculture. Recoverability of ionic liquid for eight times with negligible leaching make introduced procedure cost effective.

Conclusion

The reported procedure for algae extraction improved by using an acidic/primary ionic liquid environment. This procedure is economic because of the simply reusability of ionic liquid due to its magnetic features.

Magnetic ionic liquid

Marine algae

Phytohormone

Green extraction

Persian Gulf

Bio fertilizer

Food production importance encouraged scientists to develop new fertilizers to increase agricultural product yield. The excessive use of chemical fertilizers in agriculture is costly, hurts the physicochemical properties of soil, plants, animals, and humans, and causes the accumulation of nitrates and other chemicals in agricultural products (Jha, Pathania et al. 2023). These factors have caused a change in the approach toward using bio-based fertilizers in producing healthy foods. Biofertilizers are derived from natural sources of living organisms and improve soil structure and water-holding capacity, reduce soil crust problems, reduce water, and wind erosion and provide a slow and steady release of nutrients (Patel, Pandya et al. 2017). Phytohormones or plant hormones are naturally occurring small organic molecules or substances which influence physiological processes in plants at deficient concentrations. In other words, phytohormones are chemical messengers that coordinate the cellular activities of plants (Su, Xia et al. 2017).

The algae extract is one of the main bio-fertilizers (Rashad and A El-Chaghaby 2020). Algal phytohormones such as abscisic acid (ABA) affect cell metabolism in treated plants to enhance growth and yield. Ascophyllum Nodosum extract directly stimulate vegetative growth, flowering, and fruit formation due to having large amounts of cytokinin and gibberellin hormones, and includes some valuable compounds such as mannitol, vitamins, betaine, amino acids, and alginic acid (Repke, Silva et al. 2022). In a study conducted in 2010, Sivasangari Ramya et. al investigated the fertilizing efficiency of sargassum wightii and Ulva lactuca on growth, biochemical and yield parameters of Cyamopsis tetragonolaba (L.) Taub. Gibberellin content of seaweed extract was 5.5% mg/L and 4.2% mg/L, respectively (Ramya, Nagaraj et al. 2010). In another study conducted by Bharath et. al in 2018, the amount of Gibberellin obtained from Sargassum polycystum extract was 4.15 mg/L, was extracted by hot water extraction (Boobalan, S et al. 2018). Battah et. al in 2021, investigated the physiological response of fenugreek (Trigonella foenum-graecum L.) plant treated by farmyard manure and two seaweeds as biofertilizers. The amount of Gibberellin obtained respectively from Jania rubens and Ulva lactuca extract was 11 mg/L and 3.7 mg/L, was extracted by maceration extraction with MeOH (Battah, Mostfa et al. 2021).

Various extraction methods can be used to produce seaweed-based fertilizers. The qualitative and quantitative extractions of bioactive compounds from marine sources mostly rely on selecting the proper extraction method as the first step of any bio-fertilizer preparation, which plays a significant and crucial role in the final result and outcome. The efficiencies of conventional and non-conventional extraction methods mainly depend on the nature of the plant matrix and the chemistry of bioactive compounds (Azmir, Zaidul et al. 2013). Conventional extraction methods, such as Soxhlet are still considered as one of the reference methods. Non-conventional methods, which are more environmentally friendly due to decreased use of synthetic and organic chemicals, reduced operational time, and better yield and quality of extract, have been developed during the last 50 years. The use of new methods such as microwaves has increased the efficiency of extracting hormones and active substances from algae extract. Microwave-assisted extraction (MAE) has proposed as an environmentally friendly extraction method for the production of bio fertilizer from algal biomass (González-Hernández, Valdez-Cruz et al. 2024, Irianto, Naryaningsih et al. 2024). On the contrary, radio waves, ultrasonic waves act mechanically and cause the creation of tiny bubbles in plant tissue and the destruction of cell membranes and finally, the release of biological molecules (Kadam, Tiwari et al. 2015, Kadam, Tiwari et al. 2015).

The absorbed energy of radio waves by molecules causes’ heat, which ultimately destroys bonds, destruction of cell membranes and the penetration of more solvents into the cell and facilitate the extraction (Yuan and Macquarrie 2015, Yuan, Zhang et al. 2018). Ultrasound-assisted extraction is another environmentally friendly method to isolate numerous bioactive compounds, including laminarin. Enzyme-assisted extraction (EAE) is an environmentally friendly and efficient extraction method because there are no solvents for this process been used to extract bioactive compounds from seaweed (Irianto, Naryaningsih et al. 2024). Reported water-based methods are effective for plant hormone-like compound extraction (Sharma, Fleming et al. 2014). Acid hydrolysis methods have used to extract sulfated polysaccharides containing fucose that promote plant growth (Jannin, Arkoun et al. 2013). The alkaline hydrolysis method is the most widely used industrially for the production of algae extract (Craigie 2011). In addition, the simultaneous use of alkaline and acid hydrolysis increases extraction efficiency (Shukla, Mantin et al. 2019). In this regard, to enhance yield extraction of bioactive components from marine sources thought non-conventional methods, pulsed electric field, extrusion, supercritical fluids and accelerated solvents have been studied (Irianto, Naryaningsih et al. 2024).

Ionic liquids as accelerated solvents have been proposed to permeabilize the robust microalgal cell wall for an effective extraction of bioactive compounds (Khoo, Ooi et al. 2021, Sheng, Zhan et al. 2021). These organic salts, due to their unique properties, in addition to their ability to extract bioactive compounds, have been used in the synthesis of nanoparticles (Zarei-Ahmady and Heidarizadeh 2008), Pesticides (Javani, Zarei Ahmady et al. 2023), and active pharmaceutical Ingredients. Magnetic ionic liquids (MIL), as a new member in IL family, can combine the advantages of magnetism and green solvent, which make their use more convenient for various purposes of catalysis, synthesis and extraction (Schlosser, Marták et al. 2018). Chatzimitakos et al. proposed an extraction method for acidic pharmaceuticals and phenolic compounds by using MIL, which is recovered by an external magnetic field to avoid the use of volatile organic solvents or adsorbents (Chatzimitakos, Binellas et al. 2016). Trujillo-Rodríguez and his co-workers successfully used MIL a solvent for the extraction of polycyclic aromatic hydrocarbons (An, Rahn et al. 2017). Beiraghi et al. (Akbari 2016) and Wang et al. (Wang, Sun et al. 2015) also used MIL in the extraction and achieved good separation by magnetic field. However, the purpose of the above studies was mainly quantitative analysis, and there is no research focusing on the preparative separation for several useful products at present and the research is still in the initial stage. The application of MILs to plant growth hormone extraction is rare, and the methods for the extraction and separation of natural active ingredients have not been systematically developed. Furthermore, the application of magnetic ionic liquids in the preparation of bioactive products is little (Feng, Zhang et al. 2018). The focus of present paper is to provide a different method for extraction of bioactive compounds emphasizing to determination the ionic liquid effect in yield and effective growth hormones extraction from sargassum algae collected from the Persian Gulf.

2.1. Materials and Reagents

Acetic Acid, K₂EDTA, Potassium Hydroxide, and Orthophosphoric acid (H₃PO₄) were purchased from Merck Company (Darmstadt, Germany). Other compounds were analytical grade were utilized without additional purification and bought from Sigma-Aldrich. The algae, S. swartzii was collected from Bandar-e-Dayyer, Bushehr province, Iran. HPLC (Shimadzu, Japan) and was used for analysis. Star Lab Scientific (Xi’an, China) XChroma universal-C18 column (5 µm, 120 Å, 4.6×250 mm) was used as the separation channel. The pH measured with pH meter (Elico, India).

2.2. Collection of Algae

In May 2022, the algae, S. swartzii was collected from the coastal region of Bandar-e-Dayyer, Bushehr province, Iran (27°50′30′′ N and 51°56′22′′ E) (Fig. 1). To establish the genus and species of algae, the appearance characteristics of the algae analyzed, and C. Agardh, (1820) employed a regional identification key to establishing the sex and species type used. The collected plants from the beaches washed twice with seawater to remove sand, epiphytes and other tiny organisms attached. Morphologically distinct thallus of algae were placed separately in new polythene bags and were kept in an icebox containing slush ice and transported to the laboratory.

2.3. Algae pre-Extraction

The samples were washed thoroughly from minor pollution using Water City to remove the salt from the sample's surface. The water was drained off, and thallus was spread on blotting paper to remove the excess water. Algae sample should be kept in the shade of the sun for seven days and direct sunlight should be strictly avoided because it may destroy the active chemical inside the sample. After identification, the cleaned samples are finely milled.

2.4. Magnetic Ionic liquid preparation

Methylimidazole (1 mmol) is refluxed (72 h) with 1-chlorobutane (1.1 mmol) in chloroform (25 mL). Then the solvent is evaporated under reduced pressure and washed with hexane (4 x 25 ml) under ultrasound and the resulting ionic liquid is dried under vacuum at 60 ^oC for 12 hours. Identification is done by Infrared spectroscopy, nuclear magnetic resonance of hydrogen (¹H NMR) and carbon (¹³C NMR) in D₂O solvent and ESI-MS mass spectrometry (Keshavarz, Karami et al. 2014). The resulting 1-Ethyl-3-methylimidazolium chloride with a molar ratio equal to FeCl₃.6H₂O is metathesized in ethanol at room temperature under nitrogen for 4 hours. After evaporation of the solvent, 1-Ethyl-3-methylimidazolium tetrachloroiron ionic liquid washed with deionized water to remove unreacted FeCl₃ and dried at 80 ^oC for 48 hours under reduced pressure and characterized by elemental analysis and visible spectroscopy (Hou, Liu et al. 2013, Gouveia, Jorge et al. 2014).

2.5. Preparation of crude extract using ionic liquid as extraction solvent

Powdered algae (70 g) placed in a beaker and 40 ml of ionic liquid (10% (v/v)) added and wait for 30 minutes until it is thoroughly wet and soft. Then dissolve 5 mg of K₂EDTA in 50 ml of glacial acetic acid, add to soaked algae, and heat for 2 hours at 55 ^oC to perform acid digestion and then for 24 hours at the medium is placed to complete the acid digestion. Then 3% potassium hydroxide (15 ml) added to the mixture of the previous step and the resulting mixture heated for 3 hours at 85 ^oC. The mixture is kept at room temperature for 24 hours until the alkaline digestion is complete. Then the mixture is smoothed with a muslin linen cloth (cheesecloth, cleaning cloth) and then with Whatman No. 1 filter paper the resulting viscose mixture is centrifuged at 4000 rpm for further purification. The pH of the obtained extract is about 11.5. By using concentrated phosphoric acid and adding dropwise, we bring the pH of the solution to about 9–10 (Meeder 2014). The ionic liquid is separated with a magnet (kept for the recovery study) and solvent evaporated.

The ratio of IL/H₂O optimized based on the crude extract yield (Calla-Quispe, Robles et al. 2020). Also, for emphasizing to ionic liquid effect, this procedure has done without ionic liquid (Table 1). The crude extract was used for evaluation through hormone analysis. The color of the Seaweed Liquid Extract (SLE) was observed visually and recorded.

2.3. Phytohormone analysis

The optimized SLE (Table 1, Row 5) passed through a 45% poly Tetrafluoroethylene (PTFE) filter and then injected into the HPLC column. The solution components obtained by HPLC using a C18 column (5 µm, 120 Å, 4.6 × 250 mm) as the separation channel and UV/Vis detector. The mobile phase composed MeOH: H₂O (90:10, v/v), both acidified with acetic acid 0.2%, and the flow rate was 0.7 mL/min at 40°C (Hau, Riediker et al. 2000). All samples were analyzed in three repetitions.

2.4. Recovery and reuse of ionic liquid

The ionic liquid separated from the extraction solution with a magnet and used in the following times to determine the recoverability of ionic liquid (Fig. 2).

The color of the optimized SLE (Table 1, Row 5) of S. swartzii was Dark Brown and the pH was 9–10.

3.1 Optimization of extraction

For the ionic liquid effect and optimization, we examine extractions using different amounts of ionic liquid (Table 1).

Table 1

Optimization and magnetic ionic liquid effect study on extraction
Row	Percent of IL as solvent	Yield (%)
1	0	15
2	10	21
3	20	37
4	30	49
5	40	55
6	50	56
7	60	54
8	70	46

3.2. Phytohormone analysis

The hormone analysis of S. swartzii SLE is depicted in Table 2 and Fig. 2.

3.3. Recoverability study of ionic liquid

Recovered ionic liquid with magnet evaluated for leaching detection and used for another runs of extraction (Fig. 2).

Biological fertilizers improve the chemical and biological aspects of soil, restore soil fertility, and promote plant growth. These fertilizers increase production capacity in the long term (Pathak, Verma et al. 2022). On the other hand, the excessive and long-term use of chemical or synthetic fertilizers has led to contamination that would ultimately lead to an imbalance in the ecosystem. Unlike chemical fertilizers, using algae extracts as fertilizer prevents the destruction of the environment and does not cause dangerous pollution to humans, animals, and birds due to its non-toxicity. Today, algae extract is often used as a critical product to reduce the damage caused by living and non-living stresses and to increase the yield of plant products (Fernández, Ayastuy et al. 2022). The absence of algae extracts from weed seeds and toxic elements is one of the critical features of this biofertilizer. Algae, mainly brown algae (Ascophyllum nodosum, Padina, Fucus, Sargassum, Laminaria and Macrocystis) due to having a variety of nutritious compounds, vitamins, and stimulants needed for plant growth and easily accessible are excellent sources of fertilizer (El-Beltagi, Mohamed et al. 2022).

Plants need different growth hormones such as gibberellin, Abscisic Acid, Salicylic acid, and Brassinosteroids (Ali, Said et al. 2022). All these substances are considered to be eco-friendly and safe for the environment in organic farming and are available in algae extract.

Algae extract was prepared using the acid-alkaline hydrolysis method. The reason for using an acidic environment is that the calcium alginate in the brown algae cell wall is converted to alginic acid. The reason for using alkali is to penetrate the cell wall of algae and destroy its tissue to release alginic acid. In addition, the hormone-like compounds of auxin, cytokinin, and gibberellin are better separated in an alkaline environment. In addition, the alkaline and acidic environment causes the hydrolysis of proteins and turns them into the desired amino acid, they do not undergo any change in the acidic and alkaline environment, and their properties do not disappear and do not cause problems for the customer when using seaweed extract. To overcome the meager yield of extraction in this method, we improve acid-alkaline hydrolysis extraction method using recoverable magnetic ionic liquid.

Ionic liquids (ILs) can of dissolving and extracting the most abundant organic and inorganic compounds. In reported extraction method 1-ethyl-3-methylimidazolium tetrachloroiron as solvent increase from 15 to 55 percent, it is notable the present of water is very important in extraction efficiency. Also, using the reported method, we found that the amount of Gibberellin, Salicylic acid, Abscisic Acid and Brassinosteroids increased 58, 7, 12, 83 percent respectively by using ionic liquid.

Very simply a magnet used to recovery 1-ethyl-3-methylimidazolium tetrachloroiron and the reusability study of ionic liquid showed its possibility for eight times by a low leaching of catalyst and recusing activity.

The reported procedure for algae extraction improved by using an acidic/primary ionic liquid environment. The extraction improved not only quantify examined by extraction yield but also qualify by the percent of essential compounds, such as Gibberellin, Salicylic acid, Abscisic Acid and Brassinosteroids in extract. The alkaline digestion stage to destroy the algae tissue and separate the insoluble alginate of the algae in the form of soluble potassium alginate is very important. This procedure is economic because of the simply reusability of ionic liquid due to its magnetic features.

CRediT authorship contribution statement

Ali Rajabiyan: Conceptualization, Supervision, Investigation, Writing – original draft, Writing – review & editing. Mohammad Izadi: Conceptualization, Writing – original draft, Writing – review & editing, Resources. Fatemeh Kardani: Writing – original draft, Formal analysis, Resources. Amanollah Zarei Ahmady: Conceptualization, Supervision, Investigation, Writing – original draft, Writing – review & editing, Resources, Funding acquisition

Funding

This work is financially supported by a grant (U-98103) from the Vice Chancellor for Research Affairs of Ahvaz Jundishapur University of Medical Sciences.

Data availability

No data was used for the research described in the article

Declaration of interest statement

The authors report no conflict of interest.

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Cost-effective phytohormone extraction of Sargassum swartzii from the Persian Gulf using Magnetic Ionic Liquid

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Abstract

Figures

1. Introduction

2. Materials and methods

2.1. Materials and Reagents

2.2. Collection of Algae

2.3. Algae pre-Extraction

2.4. Magnetic Ionic liquid preparation

2.3. Phytohormone analysis

2.4. Recovery and reuse of ionic liquid

3. Results

3.1 Optimization of extraction

3.2. Phytohormone analysis

3.3. Recoverability study of ionic liquid

4. Discusion

5. Conclusion

Declarations

References

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