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Plant-Bacteria Interactions and Atmospheric Contaminants: History
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Subjects: Agronomy
Contributor: Ana Segura , Pieter van Dillewijn
One of the major health risks for humans, especially for those living in large cities, is air pollution. Air pollution consists mainly of emissions of particulate matter (PM), nitrogen oxides, sulphur dioxide, ammonia and volatile organic compounds (VOCs). The organic carbon fraction of particulate matter is a mixture of hundreds of organic compounds, such as polycyclic aromatic hydrocarbons (PAHs), or polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs), some of which are mutagenic and/or carcinogenic. Because this particulate matter represents a serious threat for human health, measures to reduce emissions and to eliminate contaminants need to be strongly reinforced, with a focus on novel biotechnologies.
  • atmospheric pollutants
  • plant-bacteria interactions
  • rhizoremediation
  • phylloremediation
  • “Green Architecture”

1. Introduction

The number of megacities (those with more than 10 million inhabitants) is predicted to increase from 33 to 43 by 2030 (https://population.un.org/wup/ (accessed on 3 March 2021). One of the major negative impacts for citizens living in large cities is air pollution. By 2030 it is estimated that total premature deaths due to air pollution will reach 3.1 million annually (OECD Environment Outlook to 2030).The management of urban growth in the context of sustainable development must, therefore, maximize the benefits of agglomeration whilst minimizing the potential adverse impacts.
The major source of air pollution in big cities is the combustion of fossil  oil derivatives, although biomass burning, or industrial exhaust, among others, road dust are also important sources of contamination[1]. Air pollution consists mainly of emissions of particulate matter (PM), nitrogen oxides, sulphur dioxide (SO2), ammonia (NH3) and volatile organic compounds (VOCs) [2].  PMs are complex mixtures in which organic carbon (OC) is abundant [3]. OC and VOCs contain compounds such a BTEXs (benzene, toluene, ethylbenzene, and xylenes), PAHs (polycyclic aromatic hydrocarbons), PCBs (polychlorinated biphenyls) and polychlorinated dibenzo–p–dioxins and dibenzofurans (PCDD/Fs), that are mutagenic and/or carcinogenic [4][5]. Removal of some of these atmospheric toxic compounds through associations between plants and bacteria, in the context of Green Architecture, is discussed in this work.
 

2. Origin,Toxicity and Bacterial Degradation of BTEX, PAHs, PCBs and Dioxins

Among the most abundant contaminants in air pollution are BTEX, PAHs, PCBs and dioxins (Fig. 1). BTEX and PAHs are petroleum-derived compounds that are released into the atmosphere as emissions from combustion of fossil fuel derivatives, volcanic eruptions or forest fires, amongst others [6][7]. Many of them are considered carcinogenic and mutagenic[4][5]. PCBs, although banned in 1978 in the US and later on in many other countries, were produced in huge amounts as insulators and dielectric or coolant fluids for cables, electrical apparatus and heat transfer systems [8]. Chlorinated dioxins are generated as unwanted by-products in the chemical syntheses of several pesticides, disinfectants, wood preservatives and in the incineration of PCB-containing plastic insulators [9].  Both chlorodioxins and co-planar PCBs cause immunotoxic and endocrine effects, as well as the induction of malign tumours, neurotoxic and/or immunotoxic effects [4].
 
Figure 1. Chemical structures of different polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs), dioxin and dioxin-like molecules;
 
The toxicity of PAHs, PCBs and chlorodioxins for animals and humans is based on their capacity to bind to the aryl hydrocarbon receptor (AhR), which leads to the transcription of target genes, among them, the genes of the cytochrome P450-monooxygenases (CYP) [10][11].
 
Biodegradation of BTEX and PAHs is performed by a large number of different microorganisms, including bacteria, fungi, and algae [12][13]. Aerobic bacterial biodegradation of these compounds requires the presence of O2 to initiate the enzymatic attack on the aromatic rings of PAHs by a dioxygenase that catalyses the dihydroxylation of PAHs. These dihydroxylated intermediates are then cleaved by ring-cleaving dioxygenases, leading to different compounds that are further converted to tricarboxylic acid (TCA) cycle intermediates, used for anabolic biomass formation and mineralized to CO2 [14]. Only a single specialized bacterium, Sphingomonas wittichii strain RW1, can use the non-chlorinated dibenzo-p-dioxin as its sole carbon- and energy source  and co-metabolize several of its chlorinated derivatives [15]. Other bacterial isolates, with highly similar catabolic genes to that of the S. wittichii strain RW1 are capable of growing using PCBs as the sole carbon source [16].
 

3. Deposition, transport and detoxification of contaminants in plants

Atmospheric contaminants can be deposited directly from the air onto leaves or in soils, and are then adsorbed to roots [17]; they can also be mobilized from soil to leaves by evaporation or wind, or be transported from roots to leaves [18]. The amount of contaminants which finally accumulates in vegetation depends on the physico-chemical properties of the particular contaminant, and also on the characteristics of leaf surfaces and root architecture, as well as on many other environment-related parameters such as wind, rain, temperature, sorption to soils, organic content of soils, and composition of root exudates [19].
After deposition, it is accepted that mobilization of contaminants through the plant is a consequence of two different processes: i) the accumulation of contaminants in plant tissues mainly correlated to their hydrophobicity and plant lipid contents, and ii) the transfer between plant tissues driven mainly via xylema [20]. Once located in the plant interior, contaminants are mainly activated by cytochrome P450 monooxygenases (CYP). The resulting compounds are later conjugated with glucose, glucuronic acid, or glutathione moieties. These conjugates are then sequestered in the cell wall or in vacuoles [21].
Despite evidence for the accumulation and subsequent biotransformation of organic contaminants in plants, it is believed that the contribution of plant uptake for their removal from the environment is very low. Soil-bound contaminants, such as PAHs, are strongly associated with soil organic matter and poorly transferred to plant roots. Furthermore, contaminants or derived products accumulating in plant cell walls or vacuoles may return to the environment after plant decay. However, plants may stimulate organic contaminant degradation through several processes such as by increasing the bioavailability of the contaminants, influencing desorption from soil particles, and stimulating the biodegrading microbiota in the rhizosphere [22][23].

 

4. Plant-Bacteria Associations for the Elimination of Atmospheric Contaminants

Whilst bacteria are armoured with a battery of degradative genes encoding catabolic biocatalysts, plants offer a large surface area to collect air particles, and they are able to stimulate bacterial activities in their rhizosphere [24]. Therefore, the combination of both organisms could be a good solution for the elimination of contaminants [25]. Two different strategies can be used:

4.1. Rhizoremediation

This consists in the elimination of contaminants from the soil surrounding the plant root, and it is based on the nutritional effect of plant roots (that secrete different metabolites that microbes can use as a nitrogen, carbon, sulphur, or phosphorus source); and in the capacity of root exudates to improve the bioavailability of contaminants. Plant roots provide a large surface area on which microorganisms can proliferate and reach high cell densities. There are two crucial aspects for a successful rhizoremediation: i) the pathways for the degradation of contaminants have to be operative and free of catabolite repression effects [26], and ii) the contaminant has to be bioavailable in a form that it can be taken up by the bacterial cell [27]. The elimination of contaminants by bacteria decreases their concentration in the rhizosphere and, therefore, improves plant growth [28].

4.2. Phylloremediation:

The phyllosphere, the surface area of plant leaves and stems, can be 6-14 times greater than the land where the vegetation is growing upon [29]; therefore, it is an important environment for the elimination of atmospheric contaminants. The accumulation of air pollutants and airborne PMs on leaf surfaces is dependent on the plant species, leaf size and structure, but is also affected by the types of waxes which make up the cuticle, the hairs covering the leaf, and leaf smoothness [19][30]. Although this environment is a hostile habitat for microorganisms (exposition at high doses of UV radiation, temperature variations, climatic factors, low nutrient content and pollution [31], it can support bacterial populations of up to 108 bacteria g−1 leaf together with smaller fungal populations [32]. It has been demonstrated that natural populations of phyllospheric bacteria can remove hydrocarbon-related air pollutants [33]; in some cases this capacity was improved by spraying bacteria able to degrade the pollutants [34].
 

5. Removal of air pollutants in the context of Green Architecture

Green Architecture involves the construction of eco-friendly buildings and infrastructures to minimize the harmful effects of urbanization on the environment, including outdoor and indoor air pollution. According to these practices, elements traditionally used for aesthetic reasons are now ecological methods for sustainable edification [35]. Some architectural elements to mitigate air pollution are already being developed such as green wall biofilters in buildings, or green belts established around industrial areas [36][37]. In these elements, plants are normally considered passive accumulators of contaminants. However, improving rhizosphere and phyllosphere bacterial communities in these architectural elements with tailor-made bacterial consortia, which attack diverse organic contaminants, could be considered a way of improving the capacity of plants to remove air pollutants [25].
 
In order to successfully implement the utilization of plant-bacteria combinations as a strategy to ameliorate air pollution in cities, there are still a number of issues that need to be solved: i) Selection of the best bacterial consortia, using  endophytic, phyllospheric and/or rhizospheric bacteria, taking into consideration all environmental requirements; ii) because of the close proximity of green structures to citizens, detailed safety analyses of degrading microorganisms and studies about the accumulation of possible toxic intermediates from degradative pathways should be investigated [38][39]; and iii) the plant and its associated microbiome have co-evolved throughout time, establishing complex interrelationships to function almost as a single supra-organism (holobiont) [40]. During bioremediation, the presence of pollutants and exogenous bacteria can affect the functioning of the holobiont [41]. The study of these new interactions and how the degradation potential of contaminants could be altered by the complex signalization existing in these niches is a novel research field to be explored.
 

6. Conclusions

The successful utilization of plant-bacteria combinations in Green Architecture is a promising technology that will have clear economic implications, less public expenditure in the citizens’ healthcare and lower the costs of contamination control.
 

This entry is adapted from the peer-reviewed paper 10.3390/agronomy11030493

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