Research review paperMicroalgae as multi-functional options in modern agriculture: current trends, prospects and challenges
Introduction
Biofertilizers are gaining significance in sustainable agriculture as a means of enhancing crop productivity, in an environmentally friendly and economically viable manner, and reducing the polluting effects of synthetic fertilizers (Singh et al., 2011a, Singh et al., 2011b). Among the various types of biofertilizers, formulations based on photosynthetic organisms, including eukaryotic microalgae, anoxygenic phototrophs and cyanobacteria, are gaining importance because of their significant contributions, particularly to the maintenance of soil fertility and enhancing crop yields (Li et al., 2017; Thilagar et al., 2016).
Algae constitute a broad group of photosynthetic organisms, including eukaryotic microalgae and prokaryotic cyanobacteria, besides macro-forms such as seaweeds and other marine forms (Lee, 2008). The morphological characteristics of eukaryotic microalgae and prokaryotic cyanobacteria resemble a thallus, i.e. not differentiated into root or shoots, and comprise unicellular, multicellular, aggregates, colonial to filamentous unbranched and branched forms. The filamentous cyanobacteria may be further divided into heterocystous (inclusive of specialized cells for N fixation) and non-heterocystous forms. Most of the algae, both micro- and macro- forms play an important role in environmental carbon sequestration and are responsible for 50% of the total photosynthesis on the earth (Moroney and Ynalvez, 2009). The involvement of cyanobacteria and eukaryotic green microalgae in the mineralization, mobilization of organic and inorganic, major and micronutrients, production of bioactive compounds, (polysaccharides, growth hormones, antimicrobial compounds, etc.) can improve the plant growth and thus makes them suitable as biofertilizing options (Gantar and Elhai, 1999; Gayathri et al., 2015; Hernández-Carlos and Gamboa-Angulo, 2011; Jäger et al., 2010; Nilsson et al., 2002; Stirk et al., 2013; Prasanna et al., 2016a; Venkataraman, 1972). They have a key role in maintaining the productivity of terrestrial and aquatic ecosystems through photosynthesis and N fixation, and improving the availability of nutrients through cycling and transformations (Moroney and Ynalvez, 2009). Application of N (nitrogen)-fixing cyanobacteria, termed as “Algalization” not only enhances the N status of soil and plant, but also minimizes the use of chemical N fertilizer (Venkataraman, 1972, Venkataraman, 1981; Etesami and Alikhani, 2016; Prasanna et al., 2016b; Swarnalakshmi et al., 2013). Being all-pervasive in nature and pioneers in inhospitable habitats, including metal contaminated lands, salt affected sites, wastelands etc., microalgae can survive and proliferate and even dominate such niches (Apte and Thomas, 1997; Chaillan et al., 2006; Pandey et al., 2005). They may also facilitate the reclamation of such inhospitable habitats (Apte and Thomas, 1997; Pandey et al., 2005).
Microalgae, particularly cyanobacteria are also considered as potential biocontrol agents as they exhibit antagonistic effect against many plant pathogens such as bacteria, fungi and nematodes, mainly as a result of production of hydrolytic enzymes and biocidal compounds such as benzoic acid, majusculonic acid, etc. (Chandel, 2009; Chaudhary et al., 2012; Prasanna et al., 2008b; Gupta et al., 2013). These antimicrobial compounds can suppress pathogenic microbes through the disruption of the cytoplasmic membrane, and inhibition of protein synthesis etc. (Swain et al., 2017). The ability of cyanobacteria in persisting in plant rhizosphere and colonize plant parts is an indirect mechanism supplementing the antagonistic effects on the plant pathogens and pests through the production and release of hydrolytic enzymes, antimicrobial metabolites, thus elicit the activity of plant defense enzymes. Electron microscopic analyses and soil/plant DNA fingerprints have helped to validate their establishment in the plant rhizosphere and colonization of roots and shoot regions (Karthikeyan et al., 2009; Babu et al., 2015a, Babu et al., 2015b; Bidyarani et al., 2015; Nilsson et al., 2002). The inoculation of these organisms influences various metabolic processes in plants as they elicit the activity of plant defense enzymes, thereby transporters, chelating agents etc. that lead to enhanced plant immunity to pathogens, and increase in plant growth and crop yields (Gupta et al., 2013).
The deployment of cyanobacteria in agriculture has been well documented in terms of their potential in enhancing plant growth, crop yields, modulation of soil microbial activity and nutrient characteristics (Table 1). In addition, recent studies have also revealed the potential use of green microalgae as biofertilizer, for enhanced soil fertility, plant growth, fruit quality and nutritional characteristics and grain yield (Coppens et al., 2016). Extensive research on the use of cyanobacteria as biofertilizer and soil conditioner has proved the potential of these organisms in sustainable agriculture (Venkataraman, 1972, Venkataraman, 1981; Gupta et al., 2013; Wuang et al., 2016; Garcia-Gonzalez and Sommerfeld, 2016). Most of the previous research focused on the N fertilization through the diazotrophic cyanobacteria (Kaushik, 1998) and other beneficial aspects were less explored (Mandal et al., 1999). However, recent studies showed that the inoculation of cyanobacteria could also increase the availability of other micro- (Zinc (Zn), Copper (Cu) Iron (Fe), etc.) and macronutrients (carbon (C), nitrogen (N), phosphorus (P), potassium (K)) in soil and their translocation inside plants, upto grains (Coppens et al., 2016; Nisha et al., 2007; Rana et al., 2012). Formerly, the use of cyanobacteria, particularly heterocystous (N fixing) strains as biofertilizer was restricted to rice crop. However, research in last two decades showed possibilities of their wide use as biofertilizer beyond rice, where both heterocystous and non-heterocystous forms and their consortia with agriculturally beneficial green algae, bacteria, fungi, have shown promise. Cyanobacterial inoculation in the soil, as seed dressings or broadcasting in fields or dipping in biofertilizer slurry and/or seed priming are reported to increase seed germination rate, plant growth and yield in variety of cereal, horticultural and vegetable crops (Karthikeyan et al., 2007; Prasanna et al., 2013a, Prasanna et al., 2015a, Prasanna et al., 2015b; Prasanna et al., 2016a; Prasanna et al., 2016b, Prasanna et al., 2017).
The present review highlights the prospects of cyanobacteria and green algae as options for biofertilization, bioremediation, and as agents for improving soil structure and functioning, and enhancing plant growth and yields. Recent developments and environmental benefits of these organisms and future interventions required to meet the demands of modern agriculture are also discussed.
Section snippets
Microalgae as biofertilizers, plant growth promoters and soil fertility enhancing options
In nature, algae are cosmopolitan, and exist even in hot and cold deserts, soil crusts, in rock crevices, or in ocean depths. In these habitats, microalgae predominantly comprise unicellular, colonial forms, besides being associated with fungi as lichens, and contribute significantly towards carbon sequestration in such habitats. Algae also show positive impacts on soil quality for sustainable agriculture. Algae increase the soil fertility by increasing the overall soil microbial activity and
Pest and disease management using microalgae
The use of chemical biocides against pathogen and pest control in agricultural practices is hazardous to the sustainability of agroecosystems. This has led to an urge in the exploration of alternative sustainable approaches for pathogen control. The use of biological options represents effective and environmentally friendly strategies for the control of soil borne pathogens (Spadaro and Gullino, 2005). The most commonly identified organisms for biocontrol include some bacteria and fungi (
Improving soil structure
Soil erosion, or the exclusion of top most fertile soil due to physical forces such as water, wind, and farming activities affects the fertility and productivity of agricultural soil. Many green algae and cyanobacterial species are reported to produce and excrete EPS in the surrounding environment (Weiss et al., 2012; Xiao and Zheng, 2016). Besides having a role in contribution to soil organic carbon, EPS facilitate the prevention of soil erosion and maintenance of appropriate soil structure (
Modes of deployment of microalgae
Significant advances have been made in the use of algal biofertilizers in the last three decades. The use of cyanobacteria and green algae based consortia, bioflocs and biofilms are emerging as latest trends to increase the establishment and effectiveness of algae biofertilizers; it may be interesting and crucial to study the compatibility and ability of different partners to grow together, for their successful deployment.
Biotechnological advances in the use of algae biofertilizers
Algal biotechnology has significantly developed in last decade; sequencing of whole genome of several algae has been completed and some are still in the pipeline. Genetic modifications of algae have been undertaken, in the context of their wide ranging applications, particularly for their use as biofuels and biofertilizers. Cyanobacteria such as Nostoc and Anabaena strains are the common model organisms for use as biofertilizers, due to their capability of fixing atmospheric N and preponderance
Biorefinery approach
As the cultivation of algal fertilizers requires large amount of water and fertilizers, this often questions their environmental and economic feasibility. Therefore, integration of biofertilizer production with non-potable water sources, cheap source of nutrients, or increasing the value chain and by products from the production technologies seem to be viable trends for the future. Fig. 3 depicts the integrated biorefinery approach of microalgae for its various applications.
Commercial aspects of microalgae in agriculture
The colossal amount of nutrients is required to serve the commercial agriculture needs. To supply these nutrients in the form of microalgal biofertilizer will require huge amount of microalgal biomass. In chemical fertilizers, anhydrous ammonia contains 82% N; while microalgal biomass comprises of 1%‑10% nitrogen (N) (Cabanelas et al., 2013). Therefore, it may be assumed that approximately 15 times more microalgae material will be required to attain similar level of fertilization. According to
Conclusions
Recent developments on the utilization of consortia/biofilms of green algae and cyanobacteria with different agriculturally beneficial microbes as biofertilizer have proved promising potential. Algal biofertilizers offer additional benefits such as biocontrol of plant pathogens, reduced use of chemicals and minimized greenhouse gas emissions, besides their use as nutrient supplements. However, the success of algal fertilizers is highly dependent on the economics of their biomass production.
Acknowledgements
Author, Nirmal Renuka is thankful to NRF-SARChI (South Africa) for postdoctoral fellowship. Authors hereby acknowledge the Durban University of Technology South Africa, National Research Foundation (South Africa) (NRF SARChI UID 84166), for financial contribution.
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