From green to clean: options for phytoremediation and phytoextraction of organic pollutants

The use of green plants specifically chosen or tailored for the remediation of polluted soils and brownfields, the treatment of industrial wastewater or the removal of volatile organic compounds from indoor or outdoor air is becoming essential for sustainable development. Phytoremediation options are less expensive compared to physico-chemical approaches, even if the time scale required reaching the target end-points can be a limiting factor. Phytotechnologies are now offering efficient tools and environmentally friendly solutions for the cleanup of soils and water contaminated by organic pollutants. However this goal requires a sound understanding of how plants can specifically accumulate, detoxify and metabolise xenobiotic compounds. Significant progress has been made recently to better understand the soil, rhizosphere and plant mechanisms involved in the phytotreatment of organic pollutants; to implement phytoextraction, phytodegradation, rhizofiltration, and rhizodegradation as instruments for the removal and/or management of organic contaminants present in soil and water; and to identify critical points in overcoming bottlenecks in plant removal and detoxification of xenobiotics. Depending on the physico-chemical properties of the organic pollutant to be removed or detoxified, as well as on the specific plant physiology and biochemistry, different phytotreatments are available to decontaminate water and soils. For example, aquatic macrophytes or even terrestrial plants can be grown under hydroponic conditions or in constructed wetlands to remove many xenobiotic compounds, e.g. sulphonated anthraquinones and azo dyes present in wastewater from the dye and textile industries. Advances have also been made to remediate soils contaminated with hydrophobic compounds like PCBs, petroleum hydrocarbons or pesticides (e.g. lindane or DDT), highlighting the respective roles of plants, endophytic and rhizospheric bacteria, and the importance of their interactions. These examples illustrate the potential of plants for the phytotreatment of xenobiotics, as well as their ability to cooperate with microorganisms (phytostimulation). Exploring and exploiting the biological diversity of plant metabolism is necessary. Consideration of plant taxonomy and phytochemistry should be the first steps in the appropriate use of the huge potential of plant species, since plants often produce natural chemicals whose structure is close to foreign compounds. Finally, the success of phytoremediation also largely depends on the ability of plants to tolerate the pollutant(s) to be removed. The possible effects of these contaminants on plant physiology and biochemistry must be addressed, since they will determine the ability of a specific plant to deal with specific pollutants or a mixture of them, and thus affect the efficiency of any phytotreatment. It is thus of utmost importance to determine the maximal possible amount of the xenobiotic compounds that can be accumulated and detoxified without injury, critical stress and disruption of metabolism or redox processes in the plant species under consideration. Such information will help to maintain the plant wellness, a key factor to correctly design and size the constructed wetland to remove the foreign compounds present in a particular wastewater or to estimate the time required to clean up a contaminated soil.

From green to clean: a promising and sustainable approach towards environmental remediation

Jean-Paul Schwitzguebel

2010

Phytoremediation of polluted soils: hype, hope and facts

Jean-Paul Schwitzguebel

Different plant species, ecotypes, varieties or cultivars can be selected, tailored and harnessed for the remediation of polluted soils, sites and brownfields, as well as for the phytotreatment of domestic or industrial wastewater. Several approaches are possible, but phytoremediation does always rely on in situ extraction, detoxification or immobilization of xenobiotic chemicals or trace elements. Phytoremediation has a strong potential as a natural, solar-energy driven approach for soils and sites moderately polluted over large surfaces, if the most appropriate plants have been carefully selected and the adequate agronomic methods are applied to manage the phytoavailability of contaminants. It can already offer a sustainable and less expensive alternative to soils or sites restoration, as compared to traditional physico-chemical techniques, even if the time required reaching the target end-points is often a severe drawback. Depending on the type of soil to be treated, as well as on the pollutants, their concentration and ageing, different approaches can be considered and will be presented with some examples of successful applications, but also highlighting their limitations: • Phytoextraction - uptake of trace elements into roots, then translocation into shoots, followed by the harvest and destruction of the contaminated plants, with possible recycling strategies to recover metals from biomass or ash. Two types of plants can be used: plants able to hyperaccumulate one or several trace elements, but producing low biomass; or plants accumulating moderate amounts of metals or metalloids, but producing high biomass. • Phytostabilisation - based on the immobilization of inorganic contaminants by adsorption to plant roots or soil particles, or precipitation in the root area, thus preventing their migration in soil, groundwater or air, and decreasing erosion, runoff and leaching. For large contaminated areas phytostabilisation is probably the only reasonable option to restore ecosystems. The most effective approach is the use of indigenous plant species, after the addition of appropriate soil amendments. • Phytodegradation - exploiting the huge potential and biodiversity of plant metabolism to detoxify, transform or degrade xenobiotic organic chemicals, like pesticides, explosives or dyes. • Phytostimulation - enhanced microbial metabolism by root exudates; plant/microbial interactions are important for such rhizospheric processes, especially for very hydrophobic compounds. In spite of a growing track record of commercial success, more large-scale trials are needed to definitively prove that phytoremediation is effective and applicable in many different situations, to rigorously assess its economics and to convince stakeholders and local authorities that it is a reality, not a dream. However, to be recognized as a mature and efficient technology, phytoremediation still needs significant progress, even if it is the focus of intensive research and development, from numerous laboratory basic studies and greenhouse experiments to successful demonstration sites. More fundamental research is still required to better understand and control the numerous metabolic processes occurring in the plant and its different organs, as well as the complex interactions between pollutants, soil, plant roots, and the rhizospheric and endophytic microorganisms. However, experimental conditions can modify plant physiology and biochemistry, and it is not obvious if results obtained with young and small plantlets under well-defined laboratory conditions can be extended to real full-scale fields. If the small-scale experimentation in laboratory or in greenhouse is highly valuable to better understand the basic plant molecular and biochemical mechanisms involved in the uptake, translocation, detoxification and sequestration of toxic trace elements and xenobiotic compounds, their direct transposition in the field is somewhat questionable. On the other hand, short-term experimental conditions in small pots used to cultivate plantlets do not allow the normal growth and development of roots and shoots, and thus impose stress which can affect the performance of plants and the efficiency of phytoremediation. In the field the following factors do play a major role, but they cannot be assessed under laboratory conditions: soil heterogeneity, meteorological uncertainty, total concentrations and spatial variability of contaminants, texture and depth of soil layers, nutrient and water availability, problems with the homogeneous input of amendments, differences in rooting depth and density, variability of soil moisture, impacts of pests, pathogens and herbivores. Molecular and biochemical mechanisms of plant adaptation to real stress conditions are still poorly understood and signalling pathways involved remain unclear. However, adaptation to environmental changes is crucial for plants and thus for the efficiency of phytoremediation. Most studies deal either with organic xenobiotics or with trace elements, whereas in the field, a mixed pollution is generally observed. Information on the probable antagonistic or possible synergistic effects of mixed pollutants on their mutual accumulation and detoxification remains however scarce and further studies are urgently needed to better understand the mechanisms involved and improve phytoremediation efficiency. On the other hand, the bioavailable fraction of soil contaminants, but not the total concentration, should be considered as the most important one from an ecological, toxicological and health standpoint, and is determined by the chemical properties of the pollutant, soil characteristics, ageing processes and biota behaviour. Ageing of pollutants usually decreases bioavailability, but root exudates, root-induced rhizosphere changes, mycorrhizal fungi and rhizospheric bacteria play a major role in the dynamics and the ability of pollutants to enter into plants; spreading of pollutants to the surroundings and groundwater can also be affected. The bioavailability of contaminants and their uptake by crops are also essential parameters for establishing risk-based regulatory guidelines and enhancing food safety. Finally, the economics of phytoremediation of organic pollutants is generally favourable, but cost is an acute problem for the treatment of trace elements. Ideally, plants should produce biomass with added value or should be used to recover valuable products. The fate of plant biomass after harvest should thus be considered in the context of biorefineries. Lignocellulosic feedstock can be used for fibers or biofuel production, after extraction of added-value products like oil for lubricants, fragrances or fine chemicals. Incineration of plant material should allow the selective recovery of metals from ash after energy production, thus providing an economically sound process, depending on the type and concentration of metal, as well as on the market price of the trace elements under consideration. With such approaches, marginal contaminated soils or brownfields can be cleaned-up, whereas owners are offered valuable sources of income instead of set-aside scenarios. In such a situation, time is no longer a limiting factor, and the term phytomanagement should be more appropriate than phytoremediation

2014

Do crosstalks with primary and secondary metabolism limit or stimulate the detoxification of xenobiotics?

Jean-Paul Schwitzguebel

Because plants are static and live in a competitive and sometimes hostile environment, they have evolved efficient mechanisms that protect them from abiotic and biotic stresses. These mechanisms include detoxification and sequestration of xenobiotic compounds and of toxic trace elements, exploited in any phytoremediation process. However there must be a limit on the amount of pollutants that can be accumulated and detoxified without disrupting the normal plant biochemistry and physiology. This limit seems to depend not only on plant species, but also on the ecotype or cultivar. The presentation aims to highlight some biochemical mechanisms, suggested or supposed to of importance for the successful phytoremediation of organic contaminants. Enzymes involved in xenobiotics detoxification are often linked to the redox chemistry of the cell. The activities of cytochrome P450 monooxygenase, peroxidase and glutathione transferase have implications on the regulation of cellular redox status, closely related to mitochondrial respiratory chains, also involved in maintaining the cellular and plant energy balance and carbon flow. For example, overloading a plant with high concentrations of xenobiotics requiring oxidation by P450 may compete with the normal functions of these enzymes. An increase in their activity may also impose a major demand on both intracellular O2 and NAD(P)H pools, disturbing plant redox or energy status, and thus affecting both primary and energy metabolism. Plant mitochondrial respiratory chains differ from the mammalian one. In addition to Complex I, they contain at least four other dehydrogenases that enable the controlled oxidation of matrix and cytoplasmic NAD(P)H. Furthermore, plant mitochondria are characterized by the presence of an alternative respiratory pathway, through which reducing equivalents can be transferred to oxygen. This pathway branches at the level of the ubiquinone pool and comprises a single enzyme, the alternative oxidase, not coupled to the synthesis of ATP and insensitive to cyanide. Increase in the expression and/or activity of the alternative oxidase has been observed during temporal events such as seed conditioning, leaf development, elevation of salicylic acid levels, thermogenesis, fruit ripening, oxidative stress, physical wounding and plant pathogenic attack. The alternative pathway is inhibited by benzhydroxamate compounds, antioxidants such as propylgallate and copper chelators such a disulfiram. The alternative oxidase is able to oxidise several added polyphenolic substrates and could also oxidise intracellular polyphenolic compounds. It is not yet known if it could directly participate in the metabolism of some xenobiotics. Depending on the stucture of the organic pollutant to be detoxified, the secondary metabolic processes in the plant could also be affected. Many plant specific metabolites, often involved in plant interactions with its environment, have a structure similar to xenobiotics, and detoxification of the latter does probably use, at least partially, the metabolic pathways of the former. For example, most of the natural anthraquinones are glycosylated, whereas glycosyl-transferases are known to be involved in the conjugation of many xenobiotics, probably including sulphonated anthraquinones. It is not yet known if the detoxification mechanisms of sulphonated aromatic compounds are unique and specific to anthraquinone producing plants. Molecules involved in the conjugation of xenobiotics, like glutathione, also play a major role in normal plant metabolism. The presence of xenobiotic compounds can induce the biosynthesis of glutathione transferases and thus an increased use of glutathione. Plant glutathione level and redox status are thus affected under such conditions. On the other hand, phytochelatins are derived from glutathione and involved in the detoxification of trace elements with their –SH groups. In either case, implications on sulphur supply and metabolism are expected. Experimental conditions do also affect plant physiology and biochemistry, and it is not obvious if results obtained with young and small plantlets under well-defined laboratory conditions can be extended to mature plants in the field. However, the large-scale implementation of phytoremediation will be successful only if the “right plant is used at the right place”. Basic physiological and biochemical knowledge is thus required to select the most appropriate plant species, ecotype or cultivar, tolerant to the contaminants to be treated and able to accumulate and detoxify them without impacting its growth and survival.

2014

From green to clean: a promising and sustainable approach towards environmental remediation

Jean-Paul Schwitzguebel

2010

Do crosstalks with primary and secondary metabolism limit or stimulate the detoxification of xenobiotics?

Jean-Paul Schwitzguebel

2014

Phytoremediation of polluted soils: hype, hope and facts

Jean-Paul Schwitzguebel

2014