Relevance of nitrogen availability on the phytochemical properties of Chenopodium quinoa cultivated in marine hydroponics as a functional food

Highlights

• Chenopodium quinoa is a salt tolerant species with potential to act as extractive species.

• C. quinoa can be grown in hydroponics with the potential to be used as functional food.

• Nitrogen availability influences the concentration of antioxidants in the plant.

• The biomass yield is dependent on the concentration of nitrogen in the culture medium.

Abstract

Chenopodium quinoa is a salt tolerant plant species of high nutritional value with potential to act as an extractive species under marine integrated multi-trophic aquaculture (IMTA). This study aimed to assess the growth performance and antioxidant content and activity of C. quinoa cultivated in saline hydroponics under contrasting nitrogen concentrations mimicking different aquaculture effluents described in literature. Seedlings were cultivated under greenhouse conditions in a modified Hoagland solution with a salinity of 20 g l⁻¹ artificial sea salt and four nitrogen concentrations: 20 mg l⁻¹ (N20); 40 mg l⁻¹ (N40); 100 mg l⁻¹ (N100) and 200 mg l⁻¹ (N200). After 4 weeks, leaf chlorophyll content and biomass gain were determined. Total flavonoids, total phenols and contents of elements were analyzed in C. quinoa leaves and shoot tips. Antioxidant capacity was quantified using oxygen radical absorbance capacity assay (ORAC). In treatments N100 and N200, C. quinoa presented higher biomass gain and lower antioxidant content and activity in its leaves and shoot tips. In contrast, in treatment N20 higher antioxidant content and activity were recorded, revealing the existence of stress inducing conditions during the experimental period. Shoot tips of these plants contained higher nitrogen and mineral contents than leaves. This approach may set the stage to develop a sustainable methodology to modulate the secondary metabolism of C. quinoa and enhance its value as functional food when cultured using marine aquaponics in IMTA systems.

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.