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Review Article

Reduction and control of air pollution: based on plant-microbe interactions

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Article: 2173657 | Received 03 Nov 2022, Accepted 23 Jan 2023, Published online: 17 Feb 2023

ABSTRACT

Economic development brings environmental challenges of which air pollution poses serious risks to humans and ecosystems. Air pollutants include volatile organic compounds (VOCs), inorganic air pollutants (IAPs) and particulate matter (PMs). Plant leaves may reduce such air pollution through adsorption and stomatal absorption. At the same time, air pollutants enter soil and root zones due to its content in rain and leaf fall. Microorganisms degrade and transform air pollutions. However, the efficiency of phytoremediation and bioremediation is slow and the use of plant-microbe interactions may therefore greatly enhance the efficiency of phytoremediation. The release of chemicals from plants leads to a mutual interaction with the microbiome that promotes the growth of the plant itself, thus enhancing degradation and detoxification of interleaf and inter-root air pollutants. Here we review the current research progress on combined plant-microbe action and discusses the interaction between plants and associated microorganisms while providing perspectives for future research in phytotechnologies.

Graphical Abstract

Introduction

With economic and industrial development, a series of environmental pollution problems have emerged in cities. Severe air pollution causes damage to buildings and cash crops, induces human cardiovascular and respiratory diseases, causes the greenhouse effect and global warming, and poses a risk to economic development, human health, and ecosystem security [Citation1, Citation2–6]. Usually, natural events such as forest fires, wind and dust, and volcanic eruptions produce air pollution, but it is mainly caused by anthropogenic sources such as construction, agricultural materials, industrial emissions, oil and coal combustion, and vehicle emissions [Citation7–10].

Plants can perform intensive gas exchange in polluted air, a process that transforms and accumulates air pollutants through a series of cellular activities within the plant [Citation11]. The use of plants to reduce and control pollution is called phytoremediation. Phytoremediation is a cost-effective and environmentally friendly remediation strategy [Citation12,Citation13]. However, the efficiency of phytoremediation of air pollution is slow, and the slow efficiency of air pollution remediation can be solved by plant-microbe interactions. Bacteria and fungi help plants to cope with stress and thereby promoting growth. Microorganisms growing on leaves and roots of plants’ phyllosphere and rhizosphere helpto transform and reduce the toxicity of pollutants through biodegradation [Citation14]. Here we review air pollutants and their hazards and plant remediation of air pollution including the combined effects of plants and microorganisms by some tree species including future research directions.

1. Common air pollution and hazards

All negative consequences of any source that result in atmospheric pollution or ecosystem destruction are collectively referred to as air pollution [Citation15]. Volatile organic compounds (VOCs), inorganic air pollutants (IAPs), and particle matter (PMs) are examples of common air pollutants [Citation16–19]. Major indoor air contaminants include Benzene, formaldehyde, polycyclic aromatic hydrocarbons (PAHs), xylene (BTEX), ethylbenzene, and toluene [Citation20,Citation21]. IAPs include carbon dioxide (CO2), sulfur dioxide (SO2), nitrogen oxides (NOx), and ozone (O3) [Citation22]. shows the sources of air pollutants. Emissions of SO2 and NOx contribute to acid rain [Citation23]. And excess CO2 can contribute to global warming and sea level rise.

Figure 1. Sources of air pollutants.

Figure 1. Sources of air pollutants.

Short-term exposure to these air pollutants may cause headaches, eye and skin irritation, and lung damage [Citation24,Citation25], and after long-term exposure, some of these pollutants enter the body into the alveoli, and the other part dissolves in the blood [Citation26], induce asthma, aplastic anemia, leukemia and even lead to miscarriage or fetal malformation [Citation27,Citation28]. The occurrence of cardiovascular disease is also associated with Long-term exposure to VOCs has been associated with PM pollution [Citation29–32]. In addition, high concentrations of formaldehyde and PM enter the airways and alveoli, which induce lung fibrosis and inflammation, leading to lung cancer [Citation33–35]. Airborne NOx is associated with central nervous system damage, cognitive decline, and increased risk of dementia [Citation36,Citation37]. An illustration of air pollutants enter the human body is shown in .

Figure 2. Air pollutants enter the human body and induce diseases.

Figure 2. Air pollutants enter the human body and induce diseases.

When SO2 enters the plant stomata, it is reduced to substances that are beneficial for plant growth and development. However, when the sulfur concentration is too high, plant stomata close, thus preventing the plant from photosynthesizing and causing the leaves to scorch and fall off, affecting plant development [Citation22]. NOx is also converted to substances required for plant growth, but large amounts of nitrogen deposition inhibit plant photosynthesis causing leaf vein necrosis and leaf abscission [Citation38,Citation39]. Exposure to moderate to high concentrations of O3 can cause damage or death of plant cells [Citation40]. The chlorophyll content, carotenoid content and water content of plants exposed to VOCs for a long time will decrease [Citation41]. Species with high PM capture have higher oxidative stress [Citation42]. This oxidative stress reduces chlorophyll content, decreases photosynthetic rates, and ultimately leads to plant death [Citation42–46].

2. The mechanisms of phytoremediation

The use of plants and associated microorganisms to eliminate or reduce the effects or toxicity of contaminants in the environment is known as phytoremediation. There are five general pathways of phytoremediation, namely phytoextraction, phytostabilization, phytovolatilization, phytotransformation and phytofiltration. Phytoextraction is the extraction of pollutants through the soil and their transport to the above-ground parts of the plant, involving the interleaf and inter-root of the plant [Citation47,Citation48]. Using this method pollutants can be hyperaccumulated in the plant leaf rings [Citation16]. Citation47,found that flowers, leaves, and stems of Rosmarinus officinalis L can be enriched in Pb, Zn, Cu and Cd; which can be a reliable option for remediation of pollution. Plant stabilization is the precipitation of pollutants through the accumulation and uptake of roots and root secretions that reduces the mobility of pollutants [Citation49]. Reduction of contaminants through wind, precipitation, soil migration and groundwater contamination [Citation50]. Unlike other methods plant stabilization is the accumulation or deposition of pollutants in the roots, which is somewhat low cost and easy to implement [Citation51]. Plant volatilization appear when the conversion of pollutants in the atmosphere as well as in the soil into volatile products in the plant, which are released in the atmosphere through the plant stomata [Citation52]. Since some of the volatiles released are also air pollutants, plants simply reduce their toxicity [Citation53]. Plant transformation occur as a metabolic conversion of pollutants by plant enzymes (e.g. nitroreductase) to substances that plants need for their own growth [Citation16]. Phytofiltration uses plant roots to absorb or adsorb pollutants from water bodies [Citation54,Citation55]. This method is similar to phytoextraction and can be used for remediation of groundwater contamination [Citation56]. shows the phytoremediation mechanism diagram.

Figure 3. Diagram of phytoremediation of air pollutants. Air pollutants are reduced through phytoremediation.

Figure 3. Diagram of phytoremediation of air pollutants. Air pollutants are reduced through phytoremediation.

3. Plant-microbial interactions remediation mechanism

The stomata on plant surfaces and leaves are the main parts that absorb pollutants, the surface of plant leaves can accumulate PM and effectively filter the air [Citation57]. However, pollutants are absorbed into the soil matrix through stomatal diffusion or due to rainfall or leaf fall, and pollutants adsorbed in the phyllosphere are transferred to the soil and inter-rhizosphere and degraded by inter-rhizosphere microbes [Citation58]. shows a schematic representation of air pollutants entering the soil and inter-rhizosphere. Microorganisms regulate plant response to stress by regulating nutrients, reducing heavy metal stress, promoting plant development, and enhancing heavy metal host uptake [Citation59–63]. shows the studies on pollutions removal by plants and microorganisms. In terms of the removal of p-toluene, rhododendrons inoculated with Pseudomonas putida TVA8 were more efficient than those uninoculated [Citation64]. Citation65,found in the experiment that the mineralization rate of p-toluene of bacteria isolated from rhizosphere was 43% at toluene concentration of 0.05μCi/mL. At 0.2 μCi/mL, the mineralization rate was 49%. After the addition of endophytic bacterium Bacillus cereus ERBP to Zamioculcas zamiifolia, O3 was removed in the continuous system, and the addition of endophytic bacteria protected Zamioculcas zamiifolia from O3 stress. It appears that the addition of microorganisms to a plant contributes to the plant’s repair potential and can also protect the plant from stress.To obtain ecological sustainability, an environment suitable for microbial growth should be created in conjunction with existing studies [Citation40,Citation66,Citation67].

Figure 4. Schematic diagram of air pollutants entering soil and rhizosphere.

Figure 4. Schematic diagram of air pollutants entering soil and rhizosphere.

Table 1. The studies on pollutions removal by plants and microorganisms.

3.1. Plant-microbe interactions remediation of PMs

PMs are carriers of most organic compounds and heavy metals, which attach to PMs to make them more toxic, making PMs one of the most serious air pollutants (Citation81, Citation82]. According to the mean aerodynamic diameter particles are usually classified as < 10 μm (PM10), < 2.5 μm (PM2.5) and < 0.1 μm (PM0.1) [Citation83].

In general, leaf-attached bacteria of plants promote the occurrence of nitrogen fixation, indoleacetic acid (IAA) production, and phosphate solubilization during plant growth to enhance plant biomass and improve the ability of plants to adsorb PMs [Citation84,Citation85]. In response to stress, bacteria reduce plant production of ethylene and promote plant growth by producing 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase [Citation86,Citation87]. In addition to indirectly reducing PM concentrations by promoting plant growth, urban air pollution can be mitigated directly through plant-microbe interactions that can degrade pollutants such as ultrafine particles and black carbon [Citation88].

Citation89, found that forest cover is inversely related to average PM10 concentrations. Plants are efficient PM biofilters and usually retain these on the leaves and stems through dry deposition processes including gravitational deposition, inertia, particle collisions, interception and Brownian diffusion, which reduce airborne levels [Citation90–94]. This make the leaf area of trees correlates well with PM deposition [Citation95,Citation96]. Of the total PM deposited by each species of 17 plants, an average of 35% was deposited in wax and 65% on leaf surfaces [Citation16,Citation97], of which some is removed by plants’ own metabolism [Citation11,Citation98].

Due to their large total leaf area, trees are generally considered to be effective in removing PM [Citation89]. Other studies have found that lianas and shrubs also have strong scavenging abilities [Citation99]. Citation100,found in their study that mosses capture more PM on a dry weight basis than the leaves of Pittosporum undulatum, a native Australian tree. In addition, rainfall can enhance the absorptive capacity of trees, leading to leaf expansion and accumulation of water-soluble ions on the leaf surface, which on average account for 28% of the total PM mass [Citation97]. shows the PM removal efficiency of some plants.

Table 2. The particulate removal efficiency of different plants.

3.2. Plant-microbe interactions remediation of VOCs

VOCs include anthropogenic (AVOCs] and biogenic (BVOCs), which are numerous and ubiquitous [Citation22]. AVOCs are generally generated due to building materials and various indoor materials and are more harmful to humans [Citation107]. The removal of VOCs by plants acts through direct uptake and microbial transformation mechanisms [Citation108]. According to Citation109, formaldehyde elimination is directly proportional to stomatal conductance. Plants absorb VOCs through stomata and surface cuticles, hydrophilic VOCs diffuse into the cell interstices and react with water membranes and inner leaf surfaces, and lipophilic VOCs are transferred to various plant organs through the bast [Citation22,Citation110]. Due to runoff and defoliation, VOCs adsorbed on the leaf surface enter the soil and the root zone, where they are decomposed by inter-rooted bacteria, and the plant exchanges gases through photosynthesis [Citation111]. shows the removal efficiency of some plants for VOCs.

Table 3. The efficiency of VOCs removal by different plants.

In studies on Chlorophytum comosum L., Nicotiana tabacum L. and Glycine max L., it was found that formaldehyde is oxidized by formaldehyde dehydrogenase to CO2, which undergoes the Calvin cycle and is eventually converted to amino acids, free sugars and cell wall components [Citation121]. In addition to the conversion of formaldehyde by plants themselves, formaldehyde dehydrogenase is also present in microorganisms [Citation122]. In addition to the conversion of formaldehyde by plants themselves, formaldehyde dehydrogenases are also present in microorganisms [Citation122]. In their study, Citation65,isolated and identified rhizosphere bacteria with a role in toluene metabolism, and the isolated strains were positive for the toluene monooxygenase gene, confirming their genetic potential to metabolize toluene. Likewise, Citation123,found in their experiments that at least at the lower end of the concentration range, a synergistic reaction exists in binary mixtures and the presence of toluene accelerates the removal of m-xylene by potted plants. To support this, Citation124,found that the abundance of microorganisms containing hydrocarbon degradation genes was positively correlated with their concentrations when atmospheric pollutants were deposited on leaves at higher concentrations and demonstrated that microorganisms had hydrocarbon degradation genes for the removal of PAHs. In addition, methylotrophic bacteria use pollutants as carbon sources through serine assimilation [Citation125], and Bacillus through the ribulose monophosphate (RuMP) assimilation pathway [Citation126]. In response to air pollution, the natural microenvironment of plants changes [Citation60].

3.3. Plant-microbe interactions remediation of IAPs

CO2 can act as a natural carbon sink. Atmospheric CO2 is stored by plants through photosynthesis and some of the deposited ones are converted into humus by plants and are stored for a long time in a process called carbon sequestration [Citation127–129]. Citation130,suggest that 50% – 70% of stored carbon comes from roots and root-associated fungi. The CO2 enters the plant mainly through stomata, wax layers and cuticles [Citation11]. Plants effectively remove CO2 under adequate light conditions [Citation131]. Another experiment found that planting Haloxylon ammodendron increased carbon sequestration by 24.46 t/ha, with soil organic carbon sequestration of 13.9 t/ha [Citation132]. Thus carbon sequestration can be used to effectively respond to the increase in atmospheric CO2 concentration. A carbon enrichment mechanism also exists in fungi [Citation133,Citation134]. Microorganisms influence humus production and composition [Citation22]. Citation135,found that CO2 affects fungal traits and interactions within the microbiome. When CO2 in the air increases, plant photosynthetic rate increases, carbon input to the soil and root secretion increases, significantly altering the structure of the inter-root microbiome [Citation136].

Airborne SO2 produces large amounts of sulfate through active atmospheric chemical processes [Citation137]. Sulfate-reducing bacteria reduce sulfate to sulfide, and sulfur-oxidizing bacteria oxidize sulfide to elemental sulfur [Citation138]. Elemental sulfur is in turn oxidized to produce sulfate, which is ultimately assimilated through the sulfate activation pathway [Citation139]. Sulfate-reducing bacteria have been shown to colonize foliage using hydrocarbons in pure cultures and can be used for remediation of air pollutants and remediation of benzene, toluene, ethylbenzene and xylene in soil [Citation140]. Brassica campestris will be able to use atmospheric SO2 as a source of sulfur [Citation141]. SO2 diffuses through plant stomata, it is absorbed by the chloroplasts and reacts with water to form bisulfite, part of which is oxidized to sulfate [Citation142]. The other part is reduced and assimilated in the chloroplast through the sulfur cycle to products of the plant root uptake cycle, such as sulfur amino acids, which are taken up by the root system to promote plant growth [Citation16,Citation22].

The growth process of plants is inseparable from the existence of nitrogen, and NOx in the atmosphere can be used as a nitrogen source for plants. Rhizobia and nitrogen-fixing bacteria are known to fix atmospheric nitrogen [Citation143]. Some fungi, such as Arbusobacteria, also can fix nitrogen [Citation144]. These microorganisms are usually found in the roots of plants. [Citation62], found in their study that the canopy of Castanea Henryi could retain about 30–50% of nitrogen. NO2 is a relatively stable presence in NOx, and other NOx will be transformed into NO2 after certain conditions [Citation110]. NO2 is mainly deposited in leaves through the stomatal trunk of plants and is reduced to ammonium (NH4+) by nitrate reductase in chloroplasts and then converted to glutamate (Glu) required for growth [Citation62]. Increased nitrogen content increases plant growth, CO2 assimilation and photosynthesis per unit area of forest. Plants with large leaves have a stronger ability to absorb NOx, so evergreen trees have the best effect [Citation110].

When VOCs and NOx undergo photochemical reactions with the help of light, O3 is produced [Citation145]. O3 is bactericidal and can inactivate bacteria [Citation146]. Therefore, microorganisms may only reduce O3 toxicity [Citation22]. Stomata, which react with organic molecules in the apoplast and gas phase to form reactive oxygen species, are the primary means by which plants remove O3 via stomata [Citation147,Citation148]. The leaf surface’s glandular trichomes have a major role in lowering ozone toxicity. Under O3 stress, the glandular trichomes on the surface of the leaf consume O3 on the leaf surface to minimize O3 absorption by the stomata, hence indirectly minimizing O3 damage [Citation40]. Glandular trichomes secrete diterpenoids and non-volatile or poorly volatile compounds may help plants to resist stresses and challenges [Citation40]. Citation149,found that the diterpenoid cis-carvacrol secreted by tobacco leaves can deplete O3 from the leaf surface and prevent stomatal uptake of O3. There are still relatively few studies on the role of different plants in resistance to O3.

4. Future studies needed

Future research directions can be considered from the followings. [1) Suitable growing medium. Citation150,found in his study that among the three substrates of expanded clay, soil and activated carbon, soil had the highest formaldehyde removal efficiency of 0.07 ~ 0.16 m3/h and soil performed better for air purification. Vermiculite, which is rich in organic matter, can be used as a growing medium for plants and assist them in the effective removal of VOCs (Citation151]. (2) Plant Green Wall. Deposition of VOCs was most effective when the composite media was applied in a 50:50 ratio of activated carbon to coconut shell substrate to a green wall consisting of vertically aligned plants [Citation152]. Citation151,in their study suggested that the combination of vermiculite, perlite and coconut shell enriched growing media with plants would form a sustainable indoor green wall. Citation153,designed an active plant biofilter with 54.5% removal of PM2.5, 65.42% removal of PM10, and 46% removal of VOC. Currently, the efficacy and safety of active plant biofiltration technology needs to be considered [Citation58]. [3) Nanomaterial implantation. Citation66,suggested that plant-implanted nanomaterials could act as catalysts to enhance the interaction with rhizobial microorganisms and the protein content of the plant itself. Certain nanomaterials act as nutrient carriers to promote plant growth, phosphorus and nitrogen fixation, and soil fertility. [Citation154], found that multi-walled carbon nanotubes greatly increased the accumulation of cadmium (Cd] and arsenic (As) in Solanum nigrum L. by promoting plant growth and stimulating the activity of antioxidant enzymes.

In summary, phytoremediation is an effective way to combat air pollution. Phytotechnologies make a positive impact on phytoremediation ecosystems, but the deposition efficiency is high when the growth medium affects the growth of plants and the implantation of excessive nanomaterials causing damage and pollution to plants and the environment are also should be considered. Only by taking into account these complex interactions can sustainable phytoremediation be obtained.

5. Conclusion

Air pollution brings harm to humans and ecosystems. Plants are an effective way to mitigate air pollution converting these into substances needed for growth. The presence of microorganisms helps to improve phytoremediation efficiency by producing nutrients that plants need to help them cope with stress. However, there is a wide range of air pollutants and the removal of other air pollutants needs to be studied. Far from enough is still known about phyllosphere microbes, many of which cannot be cultured, and it is not clear whether microbes can remediate PM and O3. Targeted selection of the most effective plant species for air pollution removal and enrichment of microorganisms with high capacity in degradation, transformation, sequestration, detoxification and plant growth promoting ability to obtain the best plant microbial system is the goal. The use of phytoremediation can achieve green, environmental protection to ensure ecological and human health, and phytotechnologies should become an important way to achieve sustainable development.

Highlights

● Here we review phytoremediation and air pollution

● This show the importancy of plant-microbe interactions

● We provide a list of the efficiency of plants to remove air pollution

● Summarizes future studies for phytotechnologies

Authors’ contributions

Yue Li: Writing – review & editing, Software, Data curation. Xiangmeng Chen: Writing – review & editing, Software, Data curation. Christian Sonne: Writing – review & editing, Software, Data curation. Su Shiung Lam: Writing – review & editing, Software, Data curation.Yafeng Yang: Writing – review & editing. Nyuk Ling Ma: Writing – review & editing, Writing – original draft, Data curation. Wanxi Peng: Project administration, Conceptualization, Methodology, Funding acquisition, Writing – original draft, Writing – review & editing, Data curation. All authors read and approved the final manuscript.

Disclosure statement

No potential conflict of interest was reported by the author(s)

Additional information

Funding

This work was supported by Program for Innovative Research Team (in Science and Technology) in University of Henan Province (No. 21IRTSTHN020) and Central Plain Scholar Funding Project of Henan Province (No. 212101510005).

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