Relevance of nitrogen availability on the phytochemical properties of Chenopodium quinoa cultivated in marine hydroponics as a functional food
Introduction
The human population is on its way to reach the 9 billion mark by 2050 (FAO, 2018) while dealing with climate change and competing for natural resources. This increases the relevance of researching new sources of food and sustainable forms of production. Thus, reducing the environmental impact of agricultural practices (Clark and Tilman, 2017) and improving water use efficiency (Wallace, 2000) become major goals in the development of sustainable food growing systems. Hydroponics is a form of plant culture without soil, where the plant roots are suspended in a nutrient rich media (Treftz and Omaye, 2016). It offers several advantages when compared with traditional agriculture, as it enables a more rationale use of water resources and provides better control over the production (Treftz and Omaye, 2016). Hydroponic culture can also be framed within Integrated Multi-Trophic Aquaculture (IMTA) systems, on which selected extractive species are set-up following sequential trophic levels.
In aquaculture, one of the main constituents of the effluents is nitrogen (N), as fish feed is rich in protein and fish excrete ammonia (Granada et al., 2016). Nitrogen, in the form of nitrate, is essential for vegetable crop cultivation (Rakocy et al., 2006). Hence, in an IMTA system the effluents of a fed species are used as an input to cultivate particulate and dissolved organic matter feeders (e.g. deposit feeders and filter feeders) and dissolved inorganic nutrients (e.g. primary producers), allowing the recycling of water and nutrients and reducing the industry's environmental impacts (Granada et al., 2016). On this set-up, hydroponic systems are often referred as aquaponics, as available nutrients are derived from uneaten feed and excretion of the target species being farmed with the use of formulated (pelleted) feeds. This type of production can be practiced either in freshwater or marine environments (Troell, 2009).
Today, consumers value food produced in a sustainable way with high nutritional value, considered fresh, safe and natural (Putnik et al., 2018), leading to new trends in the food industry (Santeramo et al., 2018). Therefore, the interest in functional food research has evolved in the past years (Granato et al., 2020).
Chenopodium quinoa Willd. is considered a functional food due to high protein and lipid content, essential amino acids and minerals in its seeds (Vega-Gálvez et al., 2010). In fact, the high nutritional value of C. quinoa presents multiple advantages over other grain cereals, as it is gluten-free and promotes several beneficial human health effects, particularly in children and elderly, as reviewed by Navruz-Varli and Sanlier (2016). This salt-tolerant plant species native from the Andean region is capable of growing at different altitudes, from sea level to high mountains and at different environmental conditions, from cold to highland and tropical environments (Jacobsen et al., 2003). Its grains have been consumed for thousands of years and, because they can also be milled into flour and used as a cereal crop, this plant is often classified as a pseudo-cereal (Vilcacundo and Hernández-Ledesma, 2017).
Besides minerals, vitamins, phytosterols, saponins and bioactive peptides (Vilcacundo and Hernández-Ledesma, 2017), C. quinoa also presents a high antioxidant capacity due to its richness in phenolic compounds, including flavonoids (Paśko et al., 2009). Plants produce antioxidants as a defense mechanism against abiotic stress and reactive oxygen species (ROS) formation (Gill and Tuteja, 2010). Antioxidants are valuable for human health due to their anti-carcinogenic, anti-ageing and anti-inflammatory properties, as well as reducing the risk of cardiovascular disorders (Pandey and Rizvi, 2009).
Most studies addressing C. quinoa nutritional and phytochemical properties focus on the most commonly used organs for human consumption, the seeds (Graf et al., 2015; Nowak et al., 2016; Filho et al., 2017; Tang and Tsao, 2017). However, other organs of this plant are also edible, such as leaves, which can be eaten in the same way as spinach (Oelke et al., 1992). Additionally, C. quinoa sprouts can also be readily consumed in salads (Schlick and Bubenheim, 1996).
As C. quinoa is a good candidate to act as an IMTA extractive species, including saltwater systems, the main objective of this study was to evaluate its growth performance (i.e., biomass, chlorophyll), production of secondary metabolites (i.e., total phenols and total flavonoids) under different hydroponic media mimicking common features of effluent water from marine aquaculture production systems, in terms of salinity and nitrogen load. Total antioxidant capacity was quantified using oxygen radical absorbance capacity assay (ORAC). The content of other relevant elements and total carbon and nitrogen (C-N) was also assessed. For this purpose, C. quinoa seedlings were cultured under controlled experimental conditions, in which salinity was kept at 20 g l−1 artificial seawater and Hoagland nutrient-rich solution was modified in order to comprise nitrogen concentrations found across different aquaculture effluents used in previous aquaculture (Orellana et al., 2014) and aquaponics studies (as hydroponics is termed when integrated in an aquaculture environment) (Endut et al., 2014; Buhmann et al., 2015; Waller et al., 2015).
The experiment ran for 4 weeks, following the plant life cycle (i.e., from seedling to flowering). Overall, this work aims to promote the potential of C. quinoa cultured under saltwater hydroponic conditions and to investigate the effect of nitrogen availability on its growth morphology, its composition and on the content of secondary metabolites, which are of interest for human consumption as a functional food.
Section snippets
Experimental set up
Seeds of C. quinoa Willd. var. Titicaca were obtained from Sven-Erik Jacobsen, University of Copenhagen, Denmark, but were originally sourced close from Lake Titicaca in Peru. Seeds were sown in propagation soil (Einheitserde, Einheitserdewerk Hameln-Tündern, Germany) and watered with tap water. After 1 week, seedlings were transplanted to pots with sterilized sand (0 to 2 mm grain size, Hornbach, Hannover, Germany) and watered as needed with modified Hoagland solution (Epstein, 1972). After 3
Results
During the experimental period, visual differences started to be observed in the development of plants from the second week. By the third week of hydroponic culture, differences in size and leaf color became more pronounced. In the treatment with the lowest nitrogen availability (N20) C. quinoa leaves became slightly chlorotic whereas growth was reduced in treatments N20 and N40 (Fig. 1). After four weeks, at the end of the experiment, the plants that showed reduced growth and chlorotic leaves
Discussion
Nitrogen is an essential nutrient for plants health status, as it serves as the basis for protein synthesis, the production of vital molecules for plant growth and development, as well as for multiple enzymatic activities of the plant (Silva and Uchida, 2000). Additionally, nitrogen is also important for the chlorophyll molecule and, consequently, for photosynthesis (Silva and Uchida, 2000). Therefore, a deficit of this nutrient in the substrate and/or hydroponic media will be reflected in
Conclusions
This study shows the potential of C. quinoa as an extractive species for saline aquaculture effluents combined with its potential as functional food. When produced in saline hydroponics with low nitrogen availability, C. quinoa presents lower biomass and higher antioxidant content, whereas with a higher availability of this nutrient, an improvement in biomass production is noticed and antioxidant content is lower. Our results suggest that a concentration of 100 mg L−1 of nitrogen in the
Credit author statement
Conceptualization: Jutta Papenbrock, Ariel Turcios, Ana I. Lillebø
Methodology: Jutta Papenbrock, Ariel Turcios
Data curation: Mariana Murteira, Ariel Turcios, Jutta Papenbrock
Writing – original draft preparation: Mariana Murteira
Visualization: Mariana Murteira, Ariel Turcios
Investigation: Mariana Murteira, Ariel Turcios
Supervision: Jutta Papenbrock, Ana I. Lillebø, Ricardo Calado
Validation: Jutta Papenbrock, Ana I. Lillebø, Ricardo Calado
Writing – Reviewing and Editing: Mariana Murteira, Ariel
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
The authors would like to thank Yvonne Leye for taking care of the plants, Julia Volker and María Del Mar Rosales for technical assistance and Sofia Isabell Rupp for performing the ICP-OES analysis.
This work was carried out under the Erasmus+ Programme for Training Mobility (2017-1-PT01-KA103-035263) funded by European Union and acknowledges the Integrated Programme of SR&TD “SmartBioR – Smart Valorization of Endogenous Marine Biological Resources Under a Changing Climate”
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