Submitted Successfully!
To reward your contribution, here is a gift for you: A free trial for our video production service.
Thank you for your contribution! You can also upload a video entry or images related to this topic.
Version Summary Created by Modification Content Size Created at Operation
1
Amer Chabili
 -- 3036 2024-01-09 11:16:10 |
2 layout & references
Sirius Huang
 Meta information modification 3036 2024-01-10 02:18:00 |

Video Upload Options

Do you have a full video?
Send video materials Upload full video

Confirm

Are you sure to Delete?
Yes No
Cite
If you have any further questions, please contact Encyclopedia Editorial Office.
Chabili, A.; Minaoui, F.; Hakkoum, Z.; Douma, M.; Meddich, A.; Loudiki, M. Cyanobacteria and Microalgae-Based Biostimulants. Encyclopedia. Available online: https://encyclopedia.pub/entry/53601 (accessed on 07 July 2024).
Chabili A, Minaoui F, Hakkoum Z, Douma M, Meddich A, Loudiki M. Cyanobacteria and Microalgae-Based Biostimulants. Encyclopedia. Available at: https://encyclopedia.pub/entry/53601. Accessed July 07, 2024.
Chabili, Amer, Farah Minaoui, Zineb Hakkoum, Mountasser Douma, Abdelilah Meddich, Mohammed Loudiki. "Cyanobacteria and Microalgae-Based Biostimulants" Encyclopedia, https://encyclopedia.pub/entry/53601 (accessed July 07, 2024).
Chabili, A., Minaoui, F., Hakkoum, Z., Douma, M., Meddich, A., & Loudiki, M. (2024, January 09). Cyanobacteria and Microalgae-Based Biostimulants. In Encyclopedia. https://encyclopedia.pub/entry/53601
Chabili, Amer, et al. "Cyanobacteria and Microalgae-Based Biostimulants." Encyclopedia. Web. 09 January, 2024.
Cyanobacteria and Microalgae-Based Biostimulants
Edit
This entry is adapted from the peer-reviewed paper 10.3390/plants13020159

Significant progress has been achieved in the use of biostimulants in sustainable agricultural practices. These new products can improve plant growth, nutrient uptake, crop yield and quality, stress adaptation and soil fertility, while reducing agriculture’s environmental footprint. Although it is an emerging market, the biostimulant sector is very promising, hence the increasing attention of the scientific community and agro-industry stakeholders in finding new sources of plant biostimulants. Pro- and eucaryotic microalgae have gained prominence and can be exploited as biostimulants due to their ability to produce high-value-added metabolites. Several works revealed the potential of microalgae- and cyanobacteria-based biostimulants (MCBs) as plant growth promoters and stress alleviators, as well as encouraging results pointing out that their use can address current and future agricultural challenges.

microalgae cyanobacteria green microalgae diatoms biostimulants sustainable agriculture

1. Introduction

Global agricultural production and consumption are anticipated to increase by 60% in 2050 [1], an increase that lines up with the augmentation of necessities, especially food production. Rather than addressing the problems of resource use, current agricultural practices only focus on increasing yields, suggesting the excessive use of chemicals fertilizers [2][3]. The overuse of chemical inputs ultimately alters the quality of soils, diminishing their fertility and weakens microbial activity within [4]. Emerging solutions were suggested to improve crop yields, in particular biotechnological ones as they have the ability to revolutionize agricultural systems and contribute to solving current and future problems [5][6]. The use of such bio-based and renewable products that stimulate plant growth through different mechanisms is already a well-established reality for the cultivation of a variety of agricultural crops [7]. Soil conditioners, organic fertilizers, biofertilizers, and biostimulants were suggested as emerging and ecofriendly solutions. Biostimulants have the potential to naturally promote plant growth, boost soil fertility, and improve microbial activity in the soil [8]. The earliest definitions described plant biostimulants as materials or agents different than fertilizers, that when used at low quantities, stimulate plant growth [9]. Recently, the European Biostimulants Industry Council (EBIC) defined plant biostimulants as substances or microorganisms that, when administered to plants or the rhizosphere, can enhance natural mechanisms for nutrient uptake efficiency, tolerance to abiotic stress, and crop quality regardless of nutrient amount [10]. Biostimulants can be applied at low doses and they can affect plants’ physiological processes through different metabolic pathways, whereas biofertilizers comprised of natural substances and microorganisms can prompt plant growth and affect soil fertility [11][12][13].
Regardless of the amount of nutrients present, biostimulants are effective in small concentrations for crop trait improvement; moreover, biostimulants can be obtained from both organic and inorganic sources [12]. Organic sources include a diverse group of substances, such as protein hydrolysates, amino acids, humic acids, biopolymers, algal extract or living microorganisms as bacteria, yeasts, fungi and microalgae, while the inorganic sources include beneficial chemical elements as trace elements or inorganic salts in the example of phosphite salts or silicon [14][15]. Apart from that, biostimulants are versatile when it comes to application methods, which can range between direct use as inoculum to use as extracts or hydrolysates.
Cyanobacteria and eukaryotic microalgae are not homogeneous monophyletic groups but rather belong to diverse bacterial or eukaryotic evolutionary lines and phylogenetically distinct groups. Due to their diversity and metabolic plasticity, microalgae represent a potently fertile source of high-value-added metabolites, including proteins, amino acids, enzymes, pigments, polyunsaturated fatty acids, polysaccharides, vitamins, antioxidants and phytohormones [13][16]. As a result, MCBs represent one of the promising solutions for their potential as growth promoters, biotic and abiotic stress alleviators [13][17]. To date, research into MCBs is prevailing compared to macroalgae-based ones that are mainly harvested from marine waters and have been well explored. In fact, microalgae represent a promising alternative and viable platform of biostimulants in addition to the option of producing specific bioactive molecules under controlled conditions [18]. In agriculture, farmers’ interests are increased in using biostimulants and biofertilizers [2][13][16], as several MCBs are available in the market and already in use, predominated by marine and freshwater microalgae-based products, while the exploration of the biostimulant potential of soil microalgae is in its early stages.

2. Microalgae-Based Biostimulants: From Phototrophic Microorganisms to Biostimulants

2.1. Selection of Microalgae Strains with High Biostimulant Potential

Despite the important potential inputs of microalgae in agriculture, choosing adequate and promising strains still poses multiple challenges. Selecting highly potent cyanobacteria and microalgae strains is subjected to several criteria. One of the most important criteria is to achieve a fast and homogeneous growth and productivity as well as an easy cultivation scheme (growth in a nutrient medium and waste resources) to produce sufficient biomass for crop trials. Strains with a high cell growth rate are recommended for their relatively short doubling time. Microalgae such as Chlamydomonas reinhardtii, Chlorella vulgaris, Dunaliella tertiolecta, Haematococcus spp., and Scenedesmus spp. are well known for their high growth rate and short doubling time [19]. Adaptation to a large spectrum of temperature, light, moisture and daily and seasonal variations is also necessary, especially in the case of open production systems under an arid climate. The selection and choice of microalgae strains also depend on the metabolic growth model. For instance, in a photoautotrophic model, strains with high carbon dioxide fixation and high light use efficiency are favored, whereas using conventional and cheap carbon sources is highly recommended in heterotrophic model (a biorefinery approach). Furthermore, selected strains must have remarkable physiological and biochemical traits, such as atmospheric N2 fixation in the case of cyanobacteria as it contributes immensely to nitrogen inputs in soils [20]. Additionally, microalgae and cyanobacteria are capable of symbiotic interactions with soil microorganisms which are highly potent as they can co-exist in the phycosphere while benefiting from each other’s production of bioactive compounds (e.g., exopolysaccharides, amino acids, proteins, and vitamins) or high auxin- and/or cytokinin-like activity [21][22]. Overall, strain selection highly influences production modes and technologies, in addition to affecting the production of added-value metabolites and controls the choice of processing methods [23].

2.2. Microalgae Cultivation and Biomass Production

Due to their capacity to produce primary and secondary metabolites, microalgae are referred to as microscopic machineries offering many advantages exploitable in many sectors. Microalgae can be cultivated under different metabolic growth models and production systems depending on energy and carbon sources, including autotrophy, heterotrophy, mixotrophy, and photoheterotrophy [24][25]. The cultivation of microalgal biomass can be achieved either by open or closed production systems, with both offering advantages as well as drawbacks. For instance, the use of open production systems includes using natural waters and fabricated aquaculture systems in which construction fees, maintenance costs and energy consumption are relatively low. However, the algal biomass yield is usually lower and the open pond is always subject to a higher risk of microbial contamination due to direct contact with air [26]. On the other hand, closed production systems emphasize using column, tubular, and flat plate photobioreactors, whereas construction fees, maintenance fees and energy consumption are relatively high in comparison to open systems, but the biomass yield is higher [25]. Exorbitant costs of biomass production, use of large volumes of water, added to high energy inputs are three of many constraints making microalgae biomass production and resource use economically inefficient. Moreover, there is an additional cost due to the nutrient supply, notably the nitrogen source, as it was reported that the production of 1.8 tons of biomass/year requires a total of 16,160 EUR/year for the nitrogen source [27].
The need for new approaches to production without extra water and a greater energy footprint is imperative. In this context, approaches such as biorefineries and a circular economy can be integrated to address these challenges. In this case, a microalgae biorefinery can be defined as a process in which the complete utilization of algal biomass is attainable after its production, and this concept is based on the sustainability of microalgal production by integrating the production along with recovering industrially valuable molecules [28].
To achieve the above, the use of treated wastewater to produce microalgae biomass is one of many promising solutions, since using wastewater as a production medium provides a culture with necessary nutrients such as phosphorus and nitrogen, thereby permitting a decrease in the production footprint [21][29]. Table 1 encompasses some successful experiences in growing microalgae using biorefinery approaches while exploiting the produced biomass as biostimulants.
Table 1. Biostimulant effects of some green microalgae strains produced via biorefinery approaches.
Green Microalgae Strains Biomass Growth Medium Application Methods/Crop Plants or Seeds Biostimulant Effects Reference
Scenedesmus obliquus Pretreated brewery wastewater Centrifuged, ultrasonicated, and enzyme hydrolyzed biomass applied on watercress seeds (Lepidium sativum), mung bean (Vigna radiata), and cucumber (Cucumis sativus L.)
  • 40% higher watercress seed germination indices, suggesting Gibberellin-like effects;
  • 60% higher root formation in mung bean and cucumber, suggesting auxin-like effects;
  • 87.5% higher cotyledon expansion in cucumber, suggesting cytokinin-like effects.
 [30]
Tetradesmus obliquus; Chlorella protothecoides Piggery wastewater Fresh microalgal biomass applied on cucumber (Cucumis sativus), barley (Hordeum vulgare), wheat (Triticum aestivum), soybean (Glycine max), watercress (Nasturium officinale), and tomato (Lycopersicon esculentum)
  • T. obliquus increased the germination index in barley, watercress, and cucumber, whereas GI increased by 100%;
  • Soybean plant shoot length was increased by 90% when using C. protothecoides;
  • A slight increase in chlorophyll a content in cucumber and tomato when using T. obliquus.
 [31]
Chlorella vulgaris UAL-1;
Chlorella sp. UAL-2;
Chlorella vulgaris UAL-3;
Chlamydopodium fusiforme UAL-4		 Secondary-treated urban wastewater
supplemented with concentrate		 Aqueous extracts applied on watercress (Lepidium sativum L.), soybean (Glycine max L.), cucumber (Cucumis sativus L.), and wheat (Triticum aestivum L.) seeds
  • Increased watercress germination index by 3.5% when using C. vulgaris UAL-1;
  • Adventitious root formation in soybean seeds promoted by 220% and 493% when using 2 concentrations of C. vulgaris UAL-1;
  • C. vulgaris UAL-1 promoted chlorophyll retention in wheat leaves.
 [32]
Chlorella vulgaris (13–1);
Scenedesmus obliquus (B2-2)		 Untreated
municipal wastewater		 Algal biomass (intact and broken cells) and culture supernatant applied on tomato (Solanum lycopersicum) and barely (Hordeum vulgare) seeds
  • 0.5- and 0.25-days faster germination time in tomato and barley seed when using C. vulgaris;
  • Faster mean germination time with S. obliquus intact cells and supernatant;
  • A higher germination index with broken cell treatment up to 9% higher.
 [33]
The biorefinery approach can also be incorporated in agriculture, since successful experiences of microalgae cultivation with agricultural effluents have been reported. Nwuche et al. [34] disclosed that Chlorella sorokiniana cultivated in membrane-filtrated palm oil mill effluent (POME) produced a higher dry cell weight among tested batches and control. Moreover, when palm oil mill effluent wastewater was used as a culture medium for Botryoccoccus sudeticus and Chlorella vulgaris, it was found that biomass productivity and lipid yield were significantly increased, especially in the case of B. sudeticus [35]. Successful trials using wastewater-grown microalgal biomass as biofertilizers demonstrated the efficiency of the approach—for instance, the use of wastewater-grown cyanobacteria and microalgae biomass as wheat biofertilizer resulted in an increase in available nutrients, and microbial biomass carbon in the soil, whereas significant increases in plant and spike dry as well as the values of 1000-grain weight by 7–33%, 10%, and 5.6–8.4%, respectively [36]. Recently, in an attempt to produce biostimulants and biofertilizers with a zero-waste process, Ferreira et al. [37] used wastewater-grown Tetradesmus obliquus biomass as biofertilizer in wheat crops, resulting in an increase in the germination index.
Just as the use of treated wastewaters or agricultural effluents for microalgae cultivation offers advantages, it is crucial to check biomass for pathogens, heavy metal concentration as well as contaminants of emerging concern before any use in agricultural practices [38]. Once microalgal biomass is produced with sufficient quantities, it can be directly used or processed via numerous techniques to formulate biostimulants.

2.3. Extraction and Application Methods of Microalgae- and Cyanobacteria-Based Biostimulants

As extracts offer many advantages efficiency wise, the use of cyanobacteria and microalgae extracts as biostimulants is gaining its place in agricultural practices. The main advantage of extraction-based methods is the removal of cell walls which assist the release of intracellular bioactive compounds. The extraction of bioactive molecules can be achieved via several methods. The extraction process comprises the penetration of the solvent into the matrix, solute dissolution and release out of the matrix to be collected afterwards [39]. Extraction efficiency depends on numerous factors including solvent properties, material size, extraction temperature and duration [40][41].
Michalak and Chojnacka [42][43] reported the development of numerous extraction methods aiming to harvest biologically active compounds from the algal cellular matrix. The process of extraction is not unidirectional but it goes through three steps: biomass pretreatment, extraction, and formulation of the extract. Microalgal biomass pretreatment consists of two steps, first is washing and/or drying and second is biomass processing for the extraction. The first steps consist of washing the biomass to eliminate any bonding particles and then drying it either via solar drying, freeze-drying or convective drying [44], whereas the second step consists of processing the biomass by disrupting cell walls to release bioactive compounds, hence increasing the extraction yield [45]. Cell wall disruption can be achieved through three main pathways: mechanical/physical, chemical, and enzymatic disruption [23][42].
Extraction methods comprise traditional methods based on extraction with water such as autoclaving, boiling, and homogenization, plus hydrolysis methods including alkaline, neutral, and acid hydrolysis. Conventional solvent extraction includes liquid–liquid extraction, liquid–solid extraction, and Soxhlet extraction. Additionally, novel extraction methods or assisted methods include microwave and ultrasound-assisted extractions, as well as supercritical fluid and pressurized liquid extractions (Figure 1) [16][42].
Plants 13 00159 g001
Figure 1. Microalgal biomass extraction methods [42][43] (made with Biorender.com).
The comparison of disruption techniques as well as extraction methods revealed an effect of disruption/extraction method choice on yield and quality of the extracts. In a comparison between disruption techniques, Lee et al. [46] compared autoclaving, bead-beating, microwaves, sonication, and a 10% NaCl solution. Results approved the effect of disruption technique choice, whereas lipid content differed significantly among techniques in which using microwaves resulted in the highest extraction yield. Furthermore, the effects of extraction method choice on the biostimulant effects of microalgae extracts are not yet well documented, as available studies indicate that using different extraction processes method wise and solvent wise affect the biostimulant potential of microalgae.
The comparison of extractor systems also revealed an effect of extraction method on biostimulant performance. For example, Navarro-López et al. [47] compared different extractor systems to detect the optimal formulation of a Scenedesmus almeriensis-based biostimulant. They revealed that the use of organic green solvents (acetone or ethanol) resulted in a higher germination index in watercress seeds compared to distilled water and ethanol:hexane:water mixture.
The cost/efficiency criterion differs among extraction methods; for example, putting together chemical, mechanical, physical, and enzymatic methods, the cost/efficiency increases, respectively [16]. Novel techniques focus mainly on solvent-free methods or non-toxic solvent use, which makes them environmentally friendly approaches. Nevertheless, investigating the potential to scale-up from laboratory to industry pilot as well as a cost–benefit analysis of MCB extraction are critical steps to take into account before mass production and formulation of such biostimulants.
Microalgae- and cyanobacteria-based biostimulants can be administrated either in the form of extracts, dry biomass, or whole cultures; spent medium or supernatant; cell suspensions [48]. Therefore, the application method depends on the condition of the biostimulants. These forms can be applied via several application methods such as foliar spray eligible for use on foliar surface, seed treatments or primers used on plant seeds, and through fertigation or soil drench by flooding planted soils (Figure 2). Application of MCBs in the way of foliar spray has been shown to enhance plant growth and yield by improving photosynthesis, nutrient uptake, and stress tolerance [49][50][51][52]. Moreover, MCBs can also be used as seed priming or treatments improving seed germination and seedling vigor, leading to better plant growth and yield [51][53][54][55][56]. Extracts, whole cultures, spent/supernatant medium, and cell suspensions can also be used through soil drenching, which improves soil health and fertility, nutrient availability for plants as well as enhancing soil microbial activity, nutrient cycling, and plant growth [57][58][59]. In a similar manner, they can also be used in hydroponic systems to improve nutrient uptake and plant growth in soilless environments [60][61][62].
Plants 13 00159 g002
Figure 2. Microalgae- and cyanobacteria-based biostimulant application methods (made with Biorender.com).
Hence, the biostimulant effects may vary to a marked extent depending on the extraction and/or application method. Furthermore, species, season, sampling site, environmental conditions, and culture conditions, especially energy, carbon and nitrogen supply, are all variables affecting the content and concentration of active compounds in algae [23][24].
In addition to the cultivation of microalgal biomass, pretreatments and extraction, another often overlooked challenge in the process of formulating MCBs is the storage and shelf life of these products. Stirk et al. [63] demonstrated the influence of storage time and conditions on the bioactivity of freeze-dried Chlorella vulgaris biomass. The key findings highlighted by the authors were that the storage time, temperature, and lighting conditions affected root stimulation, antioxidant and antibacterial activity of C. vulgaris over storage time, which alluded that those bioactive metabolites are prone to be degraded with long storage periods.

2.4. Mechanisms and Modes of Action of Microalgae- and Cyanobacteria-Based Biostimulants

Mechanisms underlying the effects of biostimulants on plants in general remain insufficiently elucidated. As efforts are still undergoing, the complexity of studying such mechanisms is still challenging. The diversity of compounds or their complexity has made tracing mechanisms that underlies the biostimulant effect rather complicated. However, biostimulant mechanisms of action in the case of microorganisms can be categorized into two categories: direct effects and indirect effects. The first effects incorporate the synthesis of bioactive molecules increasing nutrient uptake and stress alleviation, while indirect effects incorporate physiological traits of microorganisms like phosphorus solubilization and nitrogen fixation [64][65].
The modes of action will differ according to the nature of the substance enclosed in the biostimulant product [66]. Bhupenchandra et al. [67] indicated that the possible modes of action can be correlated to several physicochemical modifications in plants, such as decreased membrane lipid peroxidation, increased chlorophyll content, and improved antioxidant activities. Biostimulants can be considered as enablers that can affect plants either directly or indirectly. Direct effects encompass photosynthesis stimulation, upgrading nutrient uptake efficiency, gene and metabolic pathway regulation, and modulating phytohormone excretion, while indirect effects include soil microbiome modulation, soil structure improvement, and organic matter degradation [68][69] (Figure 3).
Plants 13 00159 g003
Figure 3. Modes of action of microalgae- and cyanobacteria-based biostimulants on crops (made with Biorender.com).
However, the shortcomings in understanding how biostimulants work can be addressed using new methods such as omics approaches. For instance, computational metabolomics tools have been successfully used to reveal mechanisms underlying the effect of biostimulants on maize plants under drought stress. Results unveiling those alterations in primary and secondary metabolism have led to an enhancement of drought resistance traits which is due to a biostimulant-induced remodeling of the maize metabolism [70].

References

  1. FAO. The future of food and agriculture—Alternative pathways to 2050|Global Perspectives Studies|Food and Agriculture Organization of the United Nations. In Food and Agriculture Organization; FAO: Rome, Italy, 2018; p. 224. ISBN 978-92-5-130158-6.
  2. Bulgari, R.; Cocetta, G.; Trivellini, A.; Vernieri, P.; Ferrante, A. Biostimulants and crop responses: A review. Biol. Agric. Hortic. 2014, 31, 1–17.
  3. González-Pérez, B.K.; Rivas-Castillo, A.M.; Valdez-Calderón, A.; Gayosso-Morales, M.A. Microalgae as biostimulants: A new approach in agriculture. World J. Microbiol. Biotechnol. 2021, 38, 4.
  4. Pahalvi, H.N.; Rafiya, L.; Rashid, S.; Nisar, B.; Kamili, A.N. Microbiota and Biofertilizers, Ecofriendly Tools for Reclamation of Degraded Soil Environs; Springer: Berlin/Heidelberg, Germany, 2022; Volume 2, ISBN 9783030610098.
  5. Calabi-Floody, M.; Medina, J.; Rumpel, C.; Condron, L.M.; Hernandez, M.; Dumont, M.; Mora, M.d.L. Smart Fertilizers as a Strategy for Sustainable Agriculture, 1st ed.; Elsevier Inc.: Amsterdam, The Netherlands, 2018; Volume 147.
  6. Abinandan, S.; Subashchandrabose, S.R.; Venkateswarlu, K.; Megharaj, M. Soil microalgae and cyanobacteria: The biotechnological potential in the maintenance of soil fertility and health. Crit. Rev. Biotechnol. 2019, 39, 981–998.
  7. Bomfim, C.A.; Coelho, L.G.F.; do Vale, H.M.M.; de Carvalho Mendes, I.; Megías, M.; Ollero, F.J.; dos Reis Junior, F.B. Brief history of biofertilizers in Brazil: From conventional approaches to new biotechnological solutions. Braz. J. Microbiol. 2021, 52, 2215–2232.
  8. Yousfi, S.; Marín, J.; Parra, L.; Lloret, J.; Mauri, P.V. A Rhizogenic Biostimulant Effect on Soil Fertility and Roots Growth of Turfgrass. Agronomy 2021, 11, 573.
  9. Kauffman, G.L.; Kneivel, D.P.; Watschke, T.L. Effects of a Biostimulant on the Heat Tolerance Associated with Photosynthetic Capacity, Membrane Thermostability, and Polyphenol Production of Perennial Ryegrass. Crop Sci. 2007, 47, 261–267.
  10. European Commission. Regulation of the European Parliament and of the Council Laying down Rules on the Making Available on the Market of EU Fertilising Products and Amending Regulations (EC) No 1069/2009 and (EC) No 1107/2009 and Repealing Regulation (EC) No 2003/2003. Off. J. Eur. Union 2019, 2019, 114.
  11. du Jardin, P. Plant Biostimulants: Definition, Concept, Main Categories and Regulation. Sci. Hortic. 2015, 196, 3–14.
  12. Yakhin, O.I.; Lubyanov, A.A.; Yakhin, I.A.; Brown, P.H. Biostimulants in Plant Science: A Global Perspective. Front. Plant Sci. 2017, 7, 2049.
  13. Ronga, D.; Biazzi, E.; Parati, K.; Carminati, D.; Carminati, E.; Tava, A. Microalgal Biostimulants and Biofertilisers in Crop Productions. Agronomy 2019, 9, 192.
  14. Guntzer, F.; Keller, C.; Meunier, J.-D. Benefits of plant silicon for crops: A review. Agron. Sustain. Dev. 2012, 32, 201–213.
  15. Du Jardin, P.; Xu, L.; Geelen, D. Agricultural Functions and Action Mechanisms of Plant Biostimulants (PBs): An Introduction. Chem. Biol. Plant Biostimul. 2020, 1, 3–30.
  16. Chiaiese, P.; Corrado, G.; Colla, G.; Kyriacou, M.C.; Rouphael, Y. Renewable Sources of Plant Biostimulation: Microalgae as a Sustainable Means to Improve Crop Performance. Front. Plant Sci. 2018, 871, 01782.
  17. Van Oosten, M.J.; Pepe, O.; De Pascale, S.; Silletti, S.; Maggio, A. The role of biostimulants and bioeffectors as alleviators of abiotic stress in crop plants. Chem. Biol. Technol. Agric. 2017, 4, 5.
  18. Kapoore, R.V.; Wood, E.E.; Llewellyn, C.A. Algae biostimulants: A critical look at microalgal biostimulants for sustainable agricultural practices. Biotechnol. Adv. 2021, 49, 107754.
  19. Cadoret, J.-P.; Bernard, O. La Production de Biocarburant Lipidique Avec Des Microalgues: Promesses et Défis. J. Soc. Biol. 2008, 202, 201–211.
  20. Issa, A.A.; Hemida Abd-Alla, M.; Ohyam, T. Nitrogen Fixing Cyanobacteria: Future Prospect. Adv. Biol. Ecol. Nitrogen Fixat. 2014, 1, 24–48.
  21. Sankaran, R.; Show, P.L.; Nagarajan, D.; Chang, J.S. Exploitation and Biorefinery of Microalgae; Elsevier B.V.: Amsterdam, The Netherlands, 2018; ISBN 9780444639929.
  22. Singh, S. A review on possible elicitor molecules of cyanobacteria: Their role in improving plant growth and providing tolerance against biotic or abiotic stress. J. Appl. Microbiol. 2014, 117, 1221–1244.
  23. Górka, B.; Korzeniowska, K.; Lipok, J.; Wieczorek, P.P. The Biomass of Algae and Algal Extracts in Agricultural Production. Algae Biomass Charact. Appl. 2018, 8, 103–114.
  24. Márquez-Rocha, F.J.; Palma-Ramírez, D.; García-Alamilla, P.; López-Hernández, J.F.; Santiago-Morales, I.S.; Flores-Vela, A.I. Microalgae Cultivation for Secondary Metabolite Production. Microalgae Physiol. Appl. 2020, 11, 193–204.
  25. Vuppaladadiyam, A.K.; Prinsen, P.; Raheem, A.; Luque, R.; Zhao, M. Microalgae cultivation and metabolites production: A comprehensive review. Biofuels Bioprod. Biorefin. 2018, 8, 743.
  26. Liang, Y.; Kashdan, T.; Sterner, C.; Dombrowski, L.; Petrick, I.; Kröger, M.; Höfer, R. Algal Biorefineries; Elsevier B.V.: Amsterdam, The Netherlands, 2015; ISBN 9780444634535.
  27. Branco-Vieira, M.; Mata, T.; Martins, A.; Freitas, M.; Caetano, N. Economic analysis of microalgae biodiesel production in a small-scale facility. Energy Rep. 2020, 6, 325–332.
  28. Ummalyma, S.B.; Sahoo, D.; Pandey, A. Microalgal Biorefineries for Industrial Products. In Microalgae Cultivation for Biofuels Production; Academic Press: Cambridge, MA, USA, 2020; pp. 187–195.
  29. Al-Jabri, H.; Das, P.; Khan, S.; Thaher, M.; AbdulQuadir, M. Treatment of Wastewaters by Microalgae and the Potential Applications of the Produced Biomass—A Review. Water 2020, 13, 27.
  30. Navarro-López, E.; Ruíz-Nieto, A.; Ferreira, A.; Acién, F.G.; Gouveia, L. Biostimulant Potential of Scenedesmus obliquus Grown in Brewery Wastewater. Molecules 2020, 25, 664.
  31. Ferreira, A.; Melkonyan, L.; Carapinha, S.; Ribeiro, B.; Figueiredo, D.; Avetisova, G.; Gouveia, L. Biostimulant and biopesticide potential of microalgae growing in piggery wastewater. Environ. Adv. 2021, 4, 100062.
  32. Morillas-España, A.; Lafarga, T.; Sánchez-Zurano, A.; Acién-Fernández, F.G.; González-López, C. Microalgae based wastewater treatment coupled to the production of high value agricultural products: Current needs and challenges. Chemosphere 2022, 291, 132968.
  33. Alling, T.; Funk, C.; Gentili, F.G. Nordic microalgae produce biostimulant for the germination of tomato and barley seeds. Sci. Rep. 2023, 13, 3509.
  34. Nwuche, C.O.; Ekpo, D.C.; Eze, C.N.; Aoyagi, H.; Ogbonna, J.C. Use of Palm Oil Mill Effluent as Medium for Cultivation of Chlorella sorokiniana. Br. Biotechnol. J. 2014, 4, 305–316.
  35. Selmani, N.; Mirghani, M.E.S.; Alam, Z. Study the Growth of Microalgae in Palm Oil Mill Effluent Waste Water. IOP Conf. Ser. Earth Environ. Sci. 2013, 16, 12–16.
  36. Priya, H.; Prasanna, R.; Ramakrishnan, B.; Bidyarani, N.; Babu, S.; Thapa, S.; Renuka, N. Influence of cyanobacterial inoculation on the culturable microbiome and growth of rice. Microbiol. Res. 2015, 171, 78–89.
  37. Ferreira, A.; Figueiredo, D.; Ferreira, F.; Marujo, A.; Bastos, C.R.; Martin-Atanes, G.; Ribeiro, B.; Štěrbová, K.; Marques-Dos-Santos, C.; Acién, F.G.; et al. From piggery wastewater to wheat using microalgae towards zero waste. Algal Res. 2023, 72.
  38. Álvarez-González, A.; Uggetti, E.; Serrano, L.; Gorchs, G.; Casas, M.E.; Matamoros, V.; Gonzalez-Flo, E.; Díez-Montero, R. The potential of wastewater grown microalgae for agricultural purposes: Contaminants of emerging concern, heavy metals and pathogens assessment. Environ. Pollut. 2023, 324, 121399.
  39. Zhang, Q.-W.; Lin, L.-G.; Ye, W.-C. Techniques for extraction and isolation of natural products: A comprehensive review. Chin. Med. 2018, 13, 20.
  40. Li, P.; Xu, G.; Li, S.-P.; Wang, Y.-T.; Fan, T.-P.; Zhao, Q.-S.; Zhang, Q.-W. Optimizing Ultraperformance Liquid Chromatographic Analysis of 10 Diterpenoid Compounds in Salvia miltiorrhiza Using Central Composite Design. J. Agric. Food Chem. 2008, 56, 1164–1171.
  41. Du, G.; Zhao, H.; Song, Y.; Zhang, Q.; Wang, Y. Rapid simultaneous determination of isoflavones in Radix puerariae using high-performance liquid chromatography-triple quadrupole mass spectrometry with novel shell-type column. J. Sep. Sci. 2011, 34, 2576–2585.
  42. Michalak, I.; Chojnacka, K. Algal extracts: Technology and advances. Eng. Life Sci. 2014, 14, 581–591.
  43. Michalak, I.; Chojnacka, K. Algae as production systems of bioactive compounds. Eng. Life Sci. 2015, 15, 160–176.
  44. Kim, G.M.; Kim, Y.K. Drying Techniques of Microalgal Biomass: A Review. Appl. Chem. Eng. 2022, 33, 145–150.
  45. Wiltshire, K.H.; Boersma, M.; Möller, A.; Buhtz, H. Extraction of pigments and fatty acids from the green alga Scenedesmus obliquus (Chlorophyceae). Aquat. Ecol. 2000, 34, 119–126.
  46. Lee, J.Y.; Yoo, C.; Jun, S.Y.; Ahn, C.Y.; Oh, H.M. Comparison of Several Methods for Effective Lipid Extraction from Micro-algae. Bioresour. Technol. 2010, 101, S75–S77.
  47. Navarro-López, E.; Gallardo-Rodríguez, J.J.; Cerón-García, M.d.C.; Gallego-López, I.; Acién-Fernández, F.G.; Molina-Grima, E. Extraction of phytostimulant molecules from Scenedesmus almeriensis using different extractor systems. J. Appl. Phycol. 2023, 35, 701–711.
  48. Gitau, M.M.; Farkas, A.; Balla, B.; Ördög, V.; Futó, Z.; Maróti, G. Strain-Specific Biostimulant Effects of Chlorella and Chlamydomonas Green Microalgae on Medicago truncatula. Plants 2021, 10, 1060.
  49. Bayona-Morcillo, P.J.; Plaza, B.M.; Gómez-Serrano, C.; Rojas, E.; Jiménez-Becker, S. Effect of the foliar application of cyanobacterial hydrolysate (Arthrospira platensis) on the growth of Petunia x hybrida under salinity conditions. J. Appl. Phycol. 2020, 32, 4003–4011.
  50. Refaay, D.A.; El-Marzoki, E.M.; Abdel-Hamid, M.I.; Haroun, S.A. Effect of foliar application with Chlorella vulgaris, Tetradesmus dimorphus, and Arthrospira platensis as biostimulants for common bean. J. Appl. Phycol. 2021, 33, 3807–3815.
  51. Supraja, K.V.; Behera, B.; Balasubramanian, P. Efficacy of microalgal extracts as biostimulants through seed treatment and foliar spray for tomato cultivation. Ind. Crop. Prod. 2020, 151, 112453.
  52. La Bella, E.; Baglieri, A.; Rovetto, E.I.; Stevanato, P.; Puglisi, I. Foliar Spray Application of Chlorella vulgaris Extract: Effect on the Growth of Lettuce Seedlings. Agronomy 2021, 11, 308.
  53. Puglisi, I.; Barone, V.; Fragalà, F.; Stevanato, P.; Baglieri, A.; Vitale, A. Effect of Microalgal Extracts from Chlorella vulgaris and Scenedesmus quadricauda on Germination of Beta vulgaris Seeds. Plants 2020, 9, 675.
  54. Rupawalla, Z.; Shaw, L.; Ross, I.L.; Schmidt, S.; Hankamer, B.; Wolf, J. Germination screen for microalgae-generated plant growth biostimulants. Algal Res. 2022, 66, 102784.
  55. Jafarlou, M.B.; Pilehvar, B.; Modarresi, M.; Mohammadi, M. Performance of Algae Extracts Priming for Enhancing Seed Germination Indices and Salt Tolerance in Calotropis procera (Aiton) W.T. Iran. J. Sci. Technol. Trans. A Sci. 2021, 45, 493–502.
  56. Van Do, T.C.; Tran, D.T.; Le, T.G.; Nguyen, Q.T. Characterization of Endogenous Auxins and Gibberellins Produced by Chlorella sorokiniana TH01 under Phototrophic and Mixtrophic Cultivation Modes toward Applications in Microalgal Biorefinery and Crop Research. J. Chem. 2020, 2020, 4910621.
  57. Suchithra, M.; Muniswami, D.M.; Sri, M.S.; Usha, R.; Rasheeq, A.A.; Preethi, B.A.; Dineshkumar, R. Effectiveness of green microalgae as biostimulants and biofertilizer through foliar spray and soil drench method for tomato cultivation. S. Afr. J. Bot. 2021, 146, 740–750.
  58. El-Eslamboly, A.A.S.A.; El-Wanis, M.M.A.; Amin, A.W. Algal application as a biological control method of root-knot nematode Meloidogyne incognita on cucumber under protected culture conditions and its impact on yield and fruit quality. Egypt. J. Biol. Pest Control. 2019, 29, 18.
  59. Chanda, M.; Benhima, R.; Elmernissi, N.; Kasmi, Y.; Karim, L.; Sbabou, L.; Youssef, Z.; ElArroussi, H. Screening of microalgae liquid extracts for their bio stimulant properties on plant growth, nutrient uptake and metabolite profile of Solanum lycopersicum L. Sci. Rep. 2020, 10, 2820.
  60. Ergun, O.; Dasgan, H.; Isık, O. Effects of microalgae Chlorella vulgaris on hydroponically grown lettuce. Acta Hortic. 2020, 1273, 169–175.
  61. Dasgan, H.Y.; Kacmaz, S.; Arpaci, B.B.; Ikiz, B.; Gruda, N.S. Biofertilizers Improve the Leaf Quality of Hydroponically Grown Baby Spinach (Spinacia oleracea L.). Agronomy 2023, 13, 575.
  62. Santini, G.; Rodolfi, L.; Biondi, N.; Sampietro, G.; Tredici, M.R. Effects of cyanobacterial-based biostimulants on plant growth and development: A case study on basil (Ocimum basilicum L.). J. Appl. Phycol. 2022, 34, 2063–2073.
  63. Stirk, W.A.; Bálint, P.; Vambe, M.; Kulkarni, M.G.; van Staden, J.; Ördög, V. Effect of storage on plant biostimulant and bioactive properties of freeze-dried Chlorella vulgaris biomass. J. Appl. Phycol. 2021, 33, 3797–3806.
  64. Kumar, S.; Korra, T.; Singh, U.B.; Singh, S.; Bisen, K. Microalgal Based Biostimulants as Alleviator of Biotic and Abiotic Stresses in Crop Plants. In New and Future Developments in Microbial Biotechnology and Bioengineering; Elsevier: Amsterdam, The Netherlands, 2022; pp. 195–216.
  65. Kumari, M.; Swarupa, P.; Kesari, K.K.; Kumar, A. Microbial Inoculants as Plant Biostimulants: A Review on Risk Status. Life 2023, 13, 12.
  66. Parađiković, N.; Teklić, T.; Zeljković, S.; Lisjak, M.; Špoljarević, M. Biostimulants research in some horticultural plant species—A review. Food Energy Secur. 2019, 8, e00162.
  67. Bhupenchandra, I.; Devi, S.H.; Basumatary, A.; Dutta, S.; Singh, L.K.; Kalita, P.; Bora, S.S.; Saikia, A.; Sharma, P.; Bhagowati, S.; et al. Biostimulants: Potential and Prospects in Agriculture. Int. Res. J. Pure Appl. Chem. 2020, 21, 20–35.
  68. Renuka, N.; Guldhe, A.; Prasanna, R.; Singh, P.; Bux, F. Microalgae as multi-functional options in modern agriculture: Current trends, prospects and challenges. Biotechnol. Adv. 2018, 36, 1255–1273.
  69. Ramakrishnan, B.; Maddela, N.R.; Venkateswarlu, K.; Megharaj, M. Potential of microalgae and cyanobacteria to improve soil health and agricultural productivity: A critical view. Environ. Sci. Adv. 2023, 2, 586–611.
  70. Tinte, M.M.; Masike, K.; Steenkamp, P.A.; Huyser, J.; van der Hooft, J.J.J.; Tugizimana, F. Computational Metabolomics Tools Reveal Metabolic Reconfigurations Underlying the Effects of Biostimulant Seaweed Extracts on Maize Plants under Drought Stress Conditions. Metabolites 2022, 12, 487.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.
Upload a video for this entry
Information
Subjects: Biotechnology & Applied Microbiology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Amer Chabili
,
Farah Minaoui
,
Zineb Hakkoum
,
Mountasser Douma
,
Abdelilah Meddich
,
Mohammed Loudiki
View Times: 152
Revisions: 2 times (View History)
Update Date: 10 Jan 2024
Table of Contents
    1000/1000
    Hot Most Recent
    Video Production Service
    Feedback