Use of plant growth-promoting bacteria to facilitate phytoremediation

Abstract

Here, phytoremediation studies of toxic metal and organic compounds using plants augmented with plant growth-promoting bacteria, published in the past few years, were summarized and reviewed. These studies complemented and extended the many earlier studies in this area of research. The studies summarized here employed a wide range of non-agricultural plants including various grasses indigenous to regions of the world. The plant growth-promoting bacteria used a range of different known mechanisms to promote plant growth in the presence of metallic and/or organic toxicants and thereby improve the phytoremediation ability of most plants. Both rhizosphere and endophyte PGPB strains have been found to be effective within various phytoremediation schemes. Consortia consisting of several PGPB were often more effective than individual PGPB in assisting phytoremediation in the presence of metallic and/or organic environmental contaminants.

Keywords: environmental contamination; metal contaminants; organic contaminants; phytoremediation; plant growth-promoting bacteria; soil bacteria.

Figure 1.. Comprehensive overview of the major mechanisms of phytoremediation and of the way in which PGPB colonizing plants can assist phytoremediation of both inorganic and organic pollutants. Phytostabilization involves the use of plants able to absorb or precipitate the pollutant (blue circles) through immobilization of the molecules in the rhizosphere thus reducing the bioavailability of the contaminant and preventing its diffusion into ground water. Phytoextraction is based on the plant's ability to absorb contaminants (black stars) at the root level and translocate them to the shoots. This mechanism is mainly used for restoring soils from heavy metal pollution and has the advantage of recovering high amounts of metals from leaf and stem tissues. Phytodegradation is mainly used in the remediation of organic pollutants and takes advantage of the capability of the plant to metabolize or detoxify the contaminant (red circles) by the synthesis of specific enzymes thereby producing compounds that are less toxic (yellow open circles). Phytovolatilization is based on the ability of a plant to take up pollutant molecules at the root level, transfer them to the leaves and transform them into volatile compounds which are then released into the environment (purple circles). This tool is often exploited in mercury and arsenic remediation. Rhizodegradation (or Phytostimulation) consists of the degradation of organic pollutants by the microorganisms living in the rhizosphere or inside the plant tissues (endophytes). This is a cooperative degradation process where the plants support microbial survival through root exudation and microorganisms living on and in the root metabolize the pollutant (red closed circles) and release the product into the soil (yellow open circles). Here, PGPB support plant growth by direct (auxin synthesis, siderophores, improvement of nutrient availability) and indirect (biocontrol) mechanisms. PGPB can also favor plant development in a polluted site by relieving contaminant toxicity. The main mechanisms used by PGPB are the synthesis of ACC deaminase (and the reduction of the stress ethylene level), bioaccumulation and bioprecipitation (lowering the pollutant availability), direct catabolism on the contaminant, production of EPS and biofilm formation (EPS can interact with pollutant molecules via several mechanisms leading to increased bioavailability and easier and faster enzymatic breakdown) and release of antioxidant enzymes (protecting the plant against pollutant toxicity). This figure has been created using BioRender™.

Figure 2.. Schematic overview of the main physiological traits of PGPB involved in plant growth promotion including both direct and indirect mechanisms. This figure has been created with BioRender.com.

Figure 3.. Overview of the main mechanisms used by bacterial cells to cope with toxic metals (black circles). Bioaccumulation is based on the active uptake of the metal (mostly Pb, Ni, Ag, Hg, and Cd) through the membrane via metal transporter proteins (green rectangle) and subsequent concentration inside the cell. Biosorption relies on the capability of the bacterial cells to passively capture metal ions on external cellular surfaces. Bacterial polymers such as exopolysaccharides (EPS; red curved lines) favors metal biosorption, through the establishment of an electrostatic interaction between surface functional groups and the metal ions. Moreover, EPS synthesis leads to biofilm development creating a protective barrier against environmental stresses. Detoxification occurs through the influx of the metal and its sequestration by bacterial cytoplasmic metallothioneins (red circle) or by the release of siderophores (yellow open circle) with a high affinity for iron and other metal ions such as Cd, Cu and Hg. Internalization of the metal-siderophore complex is mediated by specific membrane receptors. Bioprecipitation is based on the binding between the metal and anionic groups located on the cell envelope. Biotransformation involves the chemical transformation of metals (mostly As, Hg, and Cr) into a different molecular form through metabolic reactions such as methylation and demethylation, isomerization, reduction/oxidation. If the product of this reaction is less harmful, the process may also result in detoxification. Bioleaching exploits the ability of some bacterial species (mainly belonging to Acidophiles) to transform the metal in a solid form into a soluble form (blue circle). This bacterial feature may be used to recover metals from ore or metallic alloys. This figure has been created using Biorender™.

Figure 4.. Assisted phytoremediation of organic pollutants: Plants can immobilize organic pollutants in the roots, volatilize them from the leaves or the shoot, or metabolize them both in the root and in the shoot through transformation (redox or hydrolysis reactions), conjugation with molecules in order to reduce the toxicity, and compartmentalization in the vacuole or in cell wall. Moreover, organic pollutants can be degraded by plant-associated bacteria living in the rhizosphere via intra- and extra-cellular enzymes, thus reducing their phytotoxicity. While plants support the growth of root associated bacteria by the rhizodeposition, bacteria behaving as PGPB promote plant growth via direct and indirect mechanisms. This figure was created with BioRender.com.