Removal of organic toxic chemicals in the rhizosphere and phyllosphere of plants.

With the ever‐growing increase in quality of life standards and awareness about environmental issues, remediation of polluted sites has become top priority. Because of the high economic cost of physicochemical strategies for remediation, the use of biological tools to clean up contaminated sites has turned out to be a very attractive option. The use of microorganisms associated to plant roots (rhizoremediation) and leaves in the removal of soil and air contaminants is an area in which success is expected in the near future.

In recent years knowledge has been gathered on the removal of contaminants by microbes living in plant niches. Plants provide a series of overlapping niches for microbial development, and culture enrichment approaches and new ‘‐omic’ technologies have demonstrated that the number of microbes in the rhizosphere (soil around the roots) and phyllosphere (leave surfaces) of plants is larger than expected. On the other hand, metabolite analysis and stable isotope probe techniques, as well as other approaches have shown that microbes associated to plants are metabolically active (Fig. 1). The ability of the microorganisms to proliferate to high densities in the plant's niche depends on the plant providing an appropriate surface for the microbes' development and, most importantly, on providing nutrients that fulfil the carbon, nitrogen and other elements demands, as well as energy needs. Looking at microbes as bioremediation catalysts, one can say that proliferation of microbes to high cell densities in the plant niches acts as a multiplier and can lead to an increase in the efficiency of pollutant removal if the resident microbes are endowed with the appropriate catabolic potential.

Figure 1

Molecular approaches in rhizoremediation and phylloremediation.

The above positive view of bioremediation contrasts with some attempts that have been made to re‐introduce microorganisms in soils for pollutant removal, which have turned out to be utterly unsuccessful. For the design of a successful rhizoremediation strategy it is necessary to fulfil at least two minimal requirements: microbes have to be able to proliferate in the root/leave system and catabolic pathways need to be operative. With the advent of micro‐array technology, global approaches in expression of genes in the plant's environment are coming to light. Several recent papers (Matilla ; Attila ) have demonstrated that almost 200 promoters are specifically induced in different strains of the genus Pseudomonas in the presence of root exudates or plant roots. These studies have revealed the mechanisms underlying microbe–plant interactions and we predict that this knowledge will contribute to recognize the best plant–bacteria combination and establish the optimal induction of catabolic pathways in sites undergoing rhizoremediation. To further support our positive view of prospects in bioremediation we can state that some products present in natural root exudates can act as inducers of different catabolic pathways for the degradation of contaminants. Although plants produce a vast amount of secondary metabolites, not all plants can produce every product and these are often generated only during a specific developmental period of the plant. We predict future studies on root/leaf bacterial metabolomes and transcriptomes of plant‐bacteria interactions during remediation to establish the best ways to introduce catabolic pathways in sites undergoing remediation. Having said this, successful rhizosphere colonization does not only depend on the interactions between the plant and the microorganism of interest, but also on the interactions with other microorganisms. New techniques to study population changes have greatly improved over the last few years and they are and will be used to determine the changes that the introduction of new microorganisms in the ecosystem will cause and how it might affect the sustainability of the ecosystem in long run.

An important problem is that of reducing pollutants that are associated to air particles. The main limitation probably comes from the bioavailability of the pollutant deposited on the leaves' surfaces. Most organic contaminants are highly hydrophobic compounds that dissolve poorly in water and many of them can form complexes with airborne particles; this lack of bioavailability may lower removal efficiency. Three recent papers have dealt with the degradation of air pollutants, namely, toluene, phenol and phenanthrene (Molloy, 2006; Sandhu ; Waight ) and studies on the bioavailability of pollutants and on the range of pollutants to be degraded will appear in the next few years. We also envisage advances in unveiling the strategies used by microbes to enhance the bioavailability of hydrophobic compounds [i.e. polycyclic aromatic hydrocarbons (PAHs)] via the production of biosurfactants, extracellular polymeric substances or formation of biofilms. We also envision research in the area of air decontamination to reveal the full remediation potential of microbes in an area where there is little study.

It has been argued that beneficial plant endophytes, bacteria that colonize the internal tissues of the plant without causing negative effects, could be an alternative in bioremediation since microbes would be somehow physically protected from adverse changes in the environment. However, successful remediation by endophytic bacteria requires the transport of the contaminant to the plant's interior. Research in this area will reveal whether or not endophytes are of interest in bioremediation. Barac and colleagues (2004) showed improvement in toluene phytoremediation using engineered endophytic bacteria. The authors transferred the toluene‐2 monooxygenase (TOM) pathway to an endophytic Burkholderia strain, a natural endophyte of yellow lupine. Although the authors showed that the strain was not maintained in the endophytic community, there was horizontal gene transfer of the tom genes to different members of the endogenous endophytic community, demonstrating new avenues to introduce desirable traits into the community.

The use of plant/microorganisms in biorremediation has also got certain drawbacks; pollutants above a certain level can be toxic for the plant and may limit plant growth in polluted sites (van Dillewijn, 2008). Another limitation comes from the fact that the plant can take up some contaminants and transform them into other chemicals whose toxicity would need to be tested. We predict remediation technologies involving plant/microbes risk assessment assays to come into consideration.

Acknowledgements

Research activities of the authors have been supported by two projects from Junta de Andalucía (CV11767 and CVI‐344) and by EC Project SYSMO (GEN2006‐27750‐C5‐5‐E/SYS).