A B S T R A C T

The efficiency of hemp (Cannabis sativa L.) in remediating sites contaminated with heavy metals has received

great attention in recent years. The main advantage of this technology relies on its inherent sustainability with a

potential re-utilization of the significant amount of produced biomass which acts as a valuable flow resource. In

this study, a combined system consisting of Cannabis sativa L. (hemp) and the blue-green alga Arthrospira platensis

(spirulina) was tested to clean up soils contaminated with cadmium, chromium, copper, nickel, lead, and zinc.

The application of non-targeted NMR methods combined with ICP-AES quantification provided an efficient

strategy for detecting residual heavy metals within plant tissues and soil. Importantly, non-targeted metabolomic

analysis helped to reveal the relationships between metabolites distribution in hemp tissues and the sequestered

metals. It was demonstrated that hemp accumulates copper, chromium, nickel, and zinc preferentially in the

leaves, while lead is distributed mainly in the stems of the plant. Moreover, it was found that, at higher con-

centrations, spirulina acts as a growth promoter, contributing to an increase in the final generated biomass.

Results reported in this work indicate that the hemp/spirulina system represents a suitable tool for remediation

of metal contaminated soils by modulating biomass production and metals uptake.

1. Introduction

Dispersion of heavy metals in soils is an age-old problem deriving

from both natural and anthropic sources (Awa and Hadibarata, 2020).

Among the anthropic contribution to soil contamination by metals, land

application of treated wastewater, sewage sludge, fertilizers, and in-

dustrial activities are major concerns (Vareda et al., 2019). Unbalanced

amounts of heavy metals may cause perturbation of soil parameters with

consequent toxic effects on plants, in the nearby water supplies, and,

ultimately, in the whole food chain (Arora et al., 2008; Kumar et al.,

2019; Manzoor et al., 2018). Typically, elements, such as copper (Cu),

nickel (Ni), zinc (Zn), and chromium (Cr) are biologically essential for

plant growth but become toxic for animals and plants when their con-

centrations exceed certain threshold levels (Edelstein and Ben-Hur,

2018; Rizvi et al., 2020; Tiwari and Lata, 2018). Other heavy metals

often found in contaminated soils, such as cadmium (Cd) and lead (Pb)

are not essential for plants growth, and many studies associated their

presence with neurological and endocrinological toxicity for humans

along with carcinogenic effects (Ali and Khan, 2019; Pratush et al.,

2018; Rehman et al., 2018).

Since heavy metals are not biodegradable, they tend to accumulate in

the environment becoming a high risk for biota over several years after

their introduction in an ecosystem (Olsson et al., 1998; Tchounwou

et al., 2012; Zwolak et al., 2019). The search for new solutions that can

remediate heavy metals-contaminated soil is a critical prerequisite for

the sustainable development of agriculture (Edelstein and Ben-Hur,

2018; ; Vardhan et al., 2019; Wuana and Okieimen, 2011), thus repre-

senting a topic of paramount importance. The most consolidated stra-

tegies to remediate heavy-metals contaminated soils include physical

and chemical approaches, like isolation, through capping and subsurface

* Corresponding authors at: Department of Civil, Environmental, Land, Building Engineering and Chemistry (DICATECh), Polytechnic University of Bari, Via

Orabona, 4, Bari 70125, Italy.

E-mail addresses: biagia.musio@poliba.it (B. Musio), vito.gallo@poliba.it (V. Gallo).

Contents lists available at ScienceDirect

Environmental Advances

journal homepage: www.sciencedirect.com/journal/environmental-advances

https://doi.org/10.1016/j.envadv.2021.100144

Received 4 October 2021; Received in revised form 17 November 2021; Accepted 19 November 2021