Plant-and microbe-assisted biochar amendment technology for petroleum hydrocarbon remediation in saline-sodic soils:A review

Kudakwashe MEKI,Qiang LIU,Shuai WU and Yanfei YUAN

Institute of Coastal Environmental PollutionControl,KeyLaboratoryof Marine Environment and Ecology,Ministryof Education,Institute for Advanced OceanStudy,OceanUniversityof China,Qingdao 266100(China)

ABSTRACT Soil degradation through salinization and pollution by toxic compounds such as petroleum hydrocarbons(PHCs)in the coastal wetlands has become a significant threat to ecosystem health,biodiversity,and food security.However,traditional remediation technologies can generate secondary pollutants,incur high operating costs,and consume significant quantities of energy.Bioremediation,using plants,biochar,and microbes,is an innovative and cost-effective option to remediate contaminated soils.Biochar,as a plant/microbe growth enhancer,is a promising green approach for the sustainable phytoremediation of PHCs in salinized soils.This review therefore summarizes the effect of plant-and microbe-assisted biochar amendment technology for the remediation of PHCs and salinization.Plant-microbe interactions mediated rhizodegradation despite increasing hydrocarbon sorption.Overall,microbial respiration is more active in biochar amendments,due to faster biodegradation of PHCs and improved soil properties.The use of biochar,plants,and microbes is recommended,as it offers a practical and sustainable option,both ecologically and economically,for the remediation of PHCs and excess salinity.Further development of new green technologies is to be encouraged.

KeyWords:bioremediation,microbial community,petrochemical pollution,phytoremediation,salinity

INTRODUCTION

Food security continues to be a priority,due to the growing global population and shifting of diets(Ecksteinet al.,2020).Soil degradation,such as erosion,desertification,acidification,salinization,and pollution,is a significant challenge to the sustainability of agricultural production and food security(Ellebyet al.,2020).The persistent imbalance between the world population and the need for a more sustainable food supply has increased the urgency of food security management(González-Balderaset al.,2020;Koyandeet al.,2020).The current world population is around 7.8 billion,and it is projected to reach 9.9 billion by 2050,an increase of more than 25%(Ecksteinet al.,2020).However,soil degradation constitutes the major challenge of our time and,in turn,threatens the long-term sustainability of agricultural production and thus food security(Kramer and Mau,2020;Sarkaraet al.,2020).The presence of petroleum hydrocarbons(PHCs)in soils,especially wetland ecosystems,has an adverse impact on human health as well as plant growth and development.The PHCs in natural gas,crude oil,tars,and asphalts are composed of various alkanes,aromatics,and polycyclic aromatic hydrocarbons(Zhanget al.,2010;Moubasheret al.,2015).The hydrocarbons enter the environment from leaking storage tanks,pipelines,and land disposal of waste petroleum and oil(Sam and Zabbey,2018;Zhuet al.,2018).

The deterioration of soil quality and fertility resulting from salinization and PHC pollution has become a critical limitation in restoring these degraded soils(Zhanget al.,2010;Moubasheret al.,2015).The influence of salts and PHCs decreases soil productivity,restricts plant growth,and adversely affects the soil microbial community structure(Penget al.,2009).The harmful effects of PHCs include inhibition of seed germination,reduction of photosynthetic pigments,slowdown of nutrient assimilation,and shortening of roots and aerial organs.It is also expected that some petroleum fractions can dissolve biological membranes and,consequently,disrupt plant root architecture(Huanget al.,2019;Shiet al.,2019;Zhuet al.,2020).To date,various approaches have been developed for the remediation of contaminated areas.The removal of pollutants has been done through different techniques,such as chemical oxidation,photocatalytic oxidation,volatilization,sedimentation,and fertilization(compost manure,ammonium sulfate,and microbial fertilizer).Fertilization has been used in soils unsuitable for agricultural production.However,many problems have been encountered,including high costs and secondary pollution(El-Naggaret al.,2018;Yanget al.,2018).Manure and compost contain pathogens,heavy metals,and pharmaceuticals,which may cause long-term contamination of farmland(Zhuet al.,2020).Therefore,developing environment-friendly technologies and sustainable strategies for remediation of excess salinity and PHC contamination in soils is essential to restoring soil ecosystem function and service,alleviating adverse effects on global climate change,and protecting biodiversity(Varjani,2017).

Since the turn of the century,the development of innovative technologies for removing PHCs and excess salinity has been the topic of much debate(Dzioneket al.,2016).Among these technologies,phytoremediation is the most eco-friendly,economically sustainable,and cost-effective technology,offering ecological and esthetic benefits.The use of plants associated with rhizospheric microbial populations to degrade organic pollutants is becoming a promising method for the remediation of polluted soil(Zhanget al.,2010;Moubasheret al.,2015).Plants used in phytoremediation can promote the dissipation of PHCs in soils through phytostabilization,phytoextraction,phytovolatilization,and phytodegradation.The enhancement of microbial activities and diversity through the improvement of physical and chemical conditions in rhizospheric soil and the phytoremediation process significantly reduce the toxicity of highmolecular-weight PHCs(Wenzel,2009;Moubasheret al.,2015).Several plant species have produced positive results when used in the phytoremediation of soils contaminated with organic and inorganic pollutants(Khanet al.,2013).Of significant concern are the improvement of efficiency and the optimization of phytoremediation conditions.Studies have revealed that soil physicochemical properties and microbial activities substantially impact the effectiveness of phytoremediation(Zhenet al.,2019).In addition,the microbial biomass and activity might be stimulated in the rhizosphere,because roots excrete significant amounts of sugars,amino acids,organic acids,hormones,vitamins,mucilage,and other substances,as well as sloughing offroot cap material.

Recently,scientists have proposed using biochar as a material with the capacity to adsorb pollutants(Anyikaet al.,2015).In recent years,biochar application as a soil amendment has received increased attention(Xiaoet al.,2018;Lenget al.,2019;Xiaoet al.,2020).Biochar is a stable,solid,and highly aromatized C-rich material formed by the low-temperature pyrolysis(＜700°C)of biomass under oxygen-limited conditions,with large specific surface area,developed pore structure,rich surface functional groups,and other excellent characteristics(Xiaoet al.,2018),and widely used in multiple fields including C sequestration.The addition of biochar to contaminated soils results in improved soil fertility,nutrient retention,water-holding capacity,and oxygen supply and remediates contamination by surface adsorption,precipitation,partitioning,and sequestration.Microbial growth and biomass can be promoted by the addition of biochar,as it also provides shelter for microbes in the soil(Chagantiet al.,2015;Lashariet al.,2015;Mahmoudet al.,2019).For instance,biochar is applied as a novel carbonaceous material for adsorbing metals in soil and water(Kwoczynski andČmelík,2021).It was reported that biochar can decrease the toxicity and mobility of many metal pollutants(Yaashikaaet al.,2020).Its characteristics,such as high surface area and microporosity,have also proven to be efficient in adsorbing organic contaminants in water(Suman and Gautam,2017).Although there have been studies evaluating the effectiveness of plant-and microbe-assisted biochar amendment technology,this research has been inadequately reported.Several studies have focused on using biochar to directly bind organic pollutants,or to induce their microbial degradation(Qinet al.,2013).Relevant critical reviews have been published,encompassing the working mechanisms and factors influencing the degradation of PHCs.To our knowledge,there are limited studies that evaluate plantand microbe-assisted biochar amendment technology for promoting the rate and efficiency of PHC degradation under saline conditions.This review therefore provided a comprehensive summary of the plant-and microbe-assisted biochar amendment technology for the remediation of PHCs and salinization.The specific objectives included:1)evaluation of the effectiveness of plants-and microbe-assisted biochar amendment technology and 2)identification of gaps and future considerations for PHC and salinity remediation.

PROBLEMS OFSALINE-SODIC SOILS

The relative significant soil problems include key soil structural devastations from physical,chemical,and biological properties(Verheijenet al.,2019;El-Mageedet al.,2020).The physical properties become bad with increasing exchangeable sodium levels,high swell-shrink potential,poor hydraulic properties due to aggregate breakdown,and poor drainage(Wonget al.,2010;Wuet al.,2014a;Sunet al.,2018).These effects result in poor plant growth(Abou-Shady,2016),reduced water availability,increased runoff,and soil erosion.Studies further noted that saline soil became dense,cloudy,and structureless due to natural aggregation loss(Dayet al.,2019).Furthermore,saline soil is associated with high bulk density and poor porosity as the permeability of soil to water and air is restricted due to its poor porous structure(Wanget al.,2019;Mehdizadehet al.,2020)and very low hydraulic conductivity.The saline soil then reforms and solidifies into almost cement-like soil with little or no structure(Aminiet al.,2015).The problems caused by sodium result in reduced infiltration,hydraulic conductivity,and surface crusting(Lashariet al.,2015),as well as the increased runoffand soil erosion previously mentioned.On the other hand,the saline soil is also compromised by its high electrical conductivity and increased osmotic pressure in soil solutions(El-Naggaret al.,2019).The soil has a low cation exchange capacity(CEC)due to the immobilization of cations such as K,Ca,and Mg.It has been noted that anions are bound very poorly by soils,especially those affected by salt.The salts in soil limit the uptake of essential plant nutrients(K,Ca,Mg,and P),resulting in nutrition disorders and eventually in poor crop yields(Akhtaret al.,2015;Aminiet al.,2015,Abou-Shady,2016).The characteristic reduction in soil organic C is also an essential resource owing to positive effects on the nutrient supply,detoxification of harmful soil constituents,moisture and nutrient retention,and soil formation(Chávez-García and Siebe,2019).

Furthermore,the increase in salinity results in a decrease in total N and organic C mineralization(Dugduget al.,2018;Sadegh-Zadehet al.,2018).High salt concentrations in soils cause osmotic stress and dehydration of microbial cells.Though having discovered the problems mentioned earlier on,more new emerging challenges are found in salt-affected soils,which require urgent attention.For example,the wetlands also face PHC pollution issues,which critically require attention to enable sustainable agriculture(Wenzel,2009;Moubasheret al.,2015).In general,deterioration of soil physical and chemical properties causes limited oxygen supply.This results in poor growth of seedlings and roots,and even seedling death.All these limiting factors work simultaneously,harming the rhizosphere environment,including microbial communities,and thereby reducing crop yields.Therefore,repairing and maintaining the sustainability of these soils have become a top priority.

POLLUTANT IMPACTS ON TERRESTRIAL BIODIVERSITY

Pollutants are a major source of degenerative diseases that affect human life,such as cancer,Alzheimer’s disease,atherosclerosis,Parkinson’s disease,and so on(Al-Baldawiet al.,2015).The degree of toxicity of each pollutant depends on the exposure and dose absorbed by organism.Plants are strongly affected by the toxicity of pollutants,because their normal physiological activities are severely hindered(Dayet al.,2019).It can be seen that the processes of respiration,photosynthesis,electron transport,and cell division are adversely affected by increased heavy metal content,as demonstrated by laboratory experiments.In addition,severe metal toxicity can inhibit cytoplasmic enzymes in plant cells and damage the cell structure due to oxidative stress(Karppinenet al.,2017a),thereby affecting plant growth and metabolism.Human exposure to such pollutants can cause serious health risks,such as lack of coordination and paralysis.

Severe exposure to Cd can damage the internal organs of the human body,such as kidney,liver,and heart tissue.Hydrocarbons are the most common cause of acute heavy metal poisoning in adults and children(Renet al.,2014;Zhenet al.,2019).The central nervous system is affected by mercury,a neurotoxin that can damage speech and hearing and cause muscle weakness(Sarmaet al.,2019).It accumulates in the microbial cells of aquatic organisms and is converted into methylmercury in the microbes,which is harmful to marine organisms.Human consumption of fish and other aquatic animals can lead to the transfer of toxic methylmercury to humans.Currently,there are limited data concerning the degree to which PHCs negatively affect the environment and sustainable measures to reduce its existence.However,due to the harmful effects of these pollutants,collaborative efforts must aim to eliminate them from the environment and support ecosystem stabilization.

METHODS OFSOIL REMEDIATION

Continuous efforts have been directed toward reclaiming degraded soils with a long history(Qadir and Oster,2002;Sastre-Condeet al.,2015;Seenivasanet al.,2015;Aroraet al.,2017).Traditional approaches have been employed to remediate soil pollution by PHCs and excess salinity,including physical engineering(e.g.,underground drainage and physical barrier),the application of chemical agents(e.g.,gypsum)(Hafezet al.,2015;Zhuet al.,2020),and bioremediation methods(e.g.,phytoremediation and microbia)(Yuet al.,2019).Nevertheless,these methods require significant investment,owing to high costs.In addition,manures and composts contain pathogens,heavy metals,and pharmaceuticals,which may cause long-term contamination of farmland(El-Naggaret al.,2018;Yanget al.,2018).Consequently,there is an imperative need to establish low-cost,environmentally friendly,and sustainable technologies for the remediation of salt-affected soil.The most appropriate method is decisive in minimizing environmental impact,while reducing salinity,the concentration of PHCs,or the toxicity of pollutants(Al-Baldawiet al.,2015).Some contaminants,such as agricultural chemicals,are applied to the soil surface.By means of leakage from buried storage tanks,sewage pipes,or landfills,other pollutants are released below the surface(Qinet al.,2013).Atmospheric pollutants containing harmful substances can also cause problems.Furthermore,pollution is not always limited to specific locations but can penetrate groundwater through the soil or be brought to nearby land and waterways in rainwater or dust.

Chemical decontamination methods usually focus on chemical oxidation.Reactive chemical oxidants are injected into the soil and groundwater quickly and then destroy pollutants.In-situ chemical oxidation is a universal solution,especially when remediating contaminants in areas that are difficult to access,such as deep soil or soil under buildings(Hussain Iet al.,2018).Chemical oxidation has a wide range of applications and can be used to treat various organic pollutants.By effectively locking PHC pollutants in the soil,the risk of pollution is reduced.It can be achieved in two ways:firstly,by modifying the contaminants in the ground to less dangerous forms;and secondly,by curing,i.e.,reducing the migration rate of the pollutants and combining them in an appropriate location,making it impossible to reach any receptor(Sanusiet al.,2016;Varjani,2017).Although chemical treatments effectively reduce pollutants in contaminated areas,they are not highly recommended,as they bring secondary pollutants and simultaneously cause underground water pollution.In addition,manures and composts contain pathogens,heavy metals,and pharmaceuticals,which may cause long-term contamination of farmland.Moreover,manures and composts have the potential to lead to ammonia and methane releases,which can aggravate global warming,and severe groundwater and stream nutrient pollution(Hussain Iet al.,2018).

Soil stability depends on the addition of fixatives,which reduce the leaching capacity and bioavailability of pollutants.Due to the higher resistance and lower permeability,the technology can also improve the geotechnical engineering capacity of the ground,making it more suitable for construction projects compared with other technologies.Soil washing with a liquid solution can eliminate harmful pollutants.In this process,the fine-grained soil(such as silt and clay)will be washed away along with contaminants,and the pollutants are more likely to combine with fine soil.Therefore,the contaminated fine powder is thus separated from the clean coarse-grained soil(such as sand and gravel),which can then be safely reused.Due to the health risks posed by soil pollution to humans,animals,and plants,soil remediation is essential in many cases(Alessandrelloet al.,2017).

Bioremediation uses biological processes to degrade,transform,or substantially remove soil pollutants(Chen Met al.,2015).The process relies on microorganisms,including bacteria and/or fungi,which use contaminants as food sources(Chen Met al.,2015;Hilberet al.,2017).Composting is a technology that utilizes microbes to clean up or stabilize pollutants(Zhanget al.,2010).Multiple studies have shown that many kinds of microbes are very effective in the degradation of various organic pollutants and the passivation of heavy metals(Yuet al.,2011;Chen Met al.,2015;Piet al.,2017).Bacteria and fungi,the main pollutant-degrading microbes in composts,have been widely considered the most crucial factors governing the remediation of contaminated soils.Remediation of contaminated soils by composting or compost addition mainly relies on two mechanisms(Hussain Fet al.,2018):i)adsorption by organic matter and ii)degradation by microorganisms.The decomposition of organic pollutants in a soil/compost mixture relies mostly on microbial activity(Chen Met al.,2015).Hence,more research needs to be undertaken to discover mechanisms that come with plant species.Care must also be taken when introducing genetically engineered microbes into the environment for bioremediation.Horizontal gene transfer can occur between the engineered and indigenous microbes in the environment.Environmentalists are concerned about such horizontal gene transfer,because the microbes are capable of spreading rapidly in the environment and transfer-resistant genes from one microbe to anotherviaplasmids enable them to adapt to new ecological environments.

The adverse effects associated with traditional methods for rehabilitating degraded soil mean that an alternative technological approach is required for better environmental purification.Moreover,alternative technologies are considered less harmful to the environment,easier to apply in any contaminated environment,and more cost-effective than traditional technologies.In general,using plant-and microbe-assisted biochar amendment technology stimulates contaminant degradation,as they complement each other’s weaknesses for sustainable recovery.

RECOVERY OFPHC AND SALINIZATION

Environmental problems such as PHC accumulation,salinization,groundwater quality deterioration,soil degradation,and various threats to human,animal,and ecosystem health are closely related to the presence of high concentrations of pollutants in the environment.Employing the appropriate technologies to remediate contaminated soils is crucial due to the site-specificity of most remediation methods(Yavariet al.,2015;Harindintwaliet al.,2020),given the nature of the pollutants and the diversity of the biosphere.Soil degradation,due to salinization and contamination,has led to failures of food security(Harindintwaliet al.,2020).However,the limitations of conventional remediation technologies include low environmental compatibility,high implementation costs,and inadequate public acceptability.This creates a need to employ biological remediation methods.Plant-and microbe-assisted biochar amendment technology offers many ecological and cost-associated benefits(Goudaet al.,2018).The plants,biochar,and microorganisms that can tolerate and grow in the presence of contaminants are commonly used.

Effects of biochar onPHC degradation

In recent years,biochar has been used as a soil improver.It has become a subject with increased scientific attention owing to its capability for soil remediation(Wuet al.,2014b;Sunet al.,2016;Sunet al.,2018).Many studies reported that biochar can change soil physical and chemical properties(Tanget al.,2010;Mukherjee and Lal,2013).For instance,it can increase soil pH(Abitet al.,2012),strengthen water retention capacity(Sunet al.,2017),improve soil fertility(Liuet al.,2019),reduce the leaching of soluble micronutrients(Aminiet al.,2015),and enhance C sequestration(Baratiet al.,2017).Moreover,it is potentially beneficial to crop productivity and growth,mitigating climate change by reducing greenhouse gas emissions(Jiet al.,2020).At the same time,biochar is a promising material in environmental restoration.The application of biochar is reported to immobilize heavy metals in the environment and reduce heavy metal toxicity to organisms(Gonget al.,2019;Zhanget al.,2019).For instance,Xuet al.(2013)demonstrated that bamboo biochar can immobilize Cd and Pb in soil and reduce their bioavailability,which were ascribed to the adsorption of metals onto the surface of biochar by complexation and ion exchange.

The benefits of biochar in soil remediation generally depend on its properties,including physical and chemical properties.It exhibits high biodegradability and high levels of total and organic C,as well as optimal concentrations of macro-and microelements(K,Na,Mn,Ca,Cu,Zn,etc.)(Hanet al.,2016;Gonget al.,2019).The application of biochar increases cation charges that contribute to the increase in soil CEC.For instance,Mehdizadehet al.(2020)reported an 8.2% increase in CEC after applying 2%(weight/weight)woody branch biochar produced at 530°C.Similarly,Mahmoudet al.(2019)used maize stalk-and wood sawdust-derived biochar made at 500°C at application rates of 5,10,and 19 t ha−1,respectively,and the soil CEC increased by 44.1%—142.4%.The mechanisms for the improvement of soil CEC following biochar application are as follows.Firstly,biochar has a high specific surface area,negative surface charge,and oxygen-containing functional groups,which can directly increase the replacement of Na at exchange sites through the provision of Ca and Mg in the soil colloids(Lashariet al.,2015).Secondly,the high adsorption capacity of biochar can reduce the Na+content in the soil solution,thereby increasing the exchange site of soil colloids by holding cations such as Ca2+,Mg2+,and Fe3+,which eventually precipitate with negatively charged elements(Luoet al.,2016;Zhenget al.,2018).Thirdly,biochar promotes the increase of soil organic matter content and then increases the value of CEC.Biochar is crucial because nutrients are low in PHC-contaminated soils;thus,plants and microbes compete for this limited resource.Therefore,the use of biochar alongside phytoremediation method is essential because biochar improves soil nutrient content.

Moreover,biochar,as a soil conditioner,creates more avenues for generating favorable soil conditions and thereby enhancing plant and microbial growth.When bacteria are applied to the soil for PHC degradation,biochar could function as a habitat for microbes as well as providing nutrients.To date,insufficient data are available on the implications of using the trio of plant,microbe,and biochar together in bioremediation technologies;hence,there is a need for further studies on this subject.

Mechanisms of biochar applicationinPHC removal

Studies have demonstrated that biochar can reduce contaminant bioavailability and biodegradation in soil(Anyikaet al.,2015;Hanet al.,2016;Zhenet al.,2019).In these studies,pollutant concentrations in soil were generally relatively low(＜500 mg kg−1),and apparent sequestering effects occurred,leading to a reduction in pollutant mobility and bioavailability.When incorporated into contaminated soil by thorough mixing,biochar promptly interacts with organic contaminants and soil microorganisms.Organic pollutants are stabilized on the biochar surface and in pores and may be further decomposed by microbes,which are stimulated by biochar amendment.The porous biochar surface,with abundant functional groups and condensed aromatic C,can adsorb various organic compounds through different mechanisms.As organic pollutants are adsorbed by biochar,their concentrations in soil water decrease,and their bioaccessibility to soil organisms,including plant roots,is reduced.

Biochar amendment enhances overall soil health by improving soil physical,chemical,and biological properties.Furthermore,microbial growth and biomass can be promoted by the addition of biochar,as it also provides shelter for microbes in the soil(Tanget al.,2010).Denyeset al.(2013)reported that biochar in the soil improved plant growth and physiological development(chlorophyll content and shoot and root biomass).Similarly,the augmentation of microbial consortia(selected microbial strains)is also well documented to promote plant vigor and growth and hydrocarbon degradation,thereby improving phytoremediation(Zhenet al.,2019).

Biochar has been used to remediate a variety of inorganic and organic contaminants in soils.In addition to providing mineral nutrients such as N,P,K,Ca,Mg,and S,the biochar modifier also introduces a large quantity of biodegradable organic C as a soil microbial substrate(Zhanget al.,2017).After the initial disturbance period,the modified soil typically shows an improved microbial community structure.Biochar promotes microbial activity,as indicated by soil respiration rate,soil enzyme activity,and soil microbial biomass.The mechanism for organic pollutant remediation,including that of PHCs,is increased sorption by means of adsorption,partitioning,and sequestration(Beesleyet al.,2011).The remediation of PHCs and polycyclic aromatic hydrocarbons by biochar has been widely reported,and the sorption of recalcitrant molecules is considered the primary mechanism(Bushnafet al.,2011;Zhenet al.,2019).In some studies,biochar was used as a stimulating agent(Qinet al.,2013;Sarmaet al.,2019)and a carrier for selected microbial strains during remediation trials(Zhanget al.,2017).In addition,biochar contains more or less multivalent metal elements such as Fe,Al,Ca,and Mg on the surface,and ionized organic compounds may form complexes with the metal ions and be deposited on the biochar surface or precipitated in soil(Songet al.,2017).

Therefore,besides abiotic factors,biochar addition may change the microbial community structure,enzyme activity,decomposition of C substrates,and cycling of other soil elements(Lehmannet al.,2011;Kuzyakov and Razavi,2019).It has been suggested that biochar absorbs organic and inorganic compounds onto its surface.According to previous studies,this is an advantage as sorption decreases the lability and availability of toxicants in soils,leading to decreased phytotoxicity(Beesleyet al.,2011;Luet al.,2015).Thus,biochar absorption ability is used for the bioremediation of soils polluted by PHCs such as alkanes,polycyclic aromatic hydrocarbons,and asphaltenes(Beesleyet al.,2011).The influence of biochar on oil-polluted soils varies,depending on the dose and timing of use,type of biochar(initial substrate and method of preparation),and soil quality(Lehmannet al.,2011).In a more recent study,a novel biochar-plant tandem approach was used to understand the rhizoremediation stimulation mechanism by biochar addition(Harindintwaliet al.,2020).They concluded that the first recalcitrant organic molecules were adsorbed onto the biochar.Root exudates may help in desorption of these adsorbed organic compounds that will subsequently be available to the degenerative microbial community in the rhizosphere.

Biochar has also been used as an adsorbent owing to its surface area and aromatic and aliphatic structures(Zhanget al.,2015).Moreover,due to its inflexibility,pore structure,and nutrient characteristics,it can affect the microbial degradation of PHCs in the soil.For instance,Baratiet al.(2017)compared granular biochar(GBC)and powdered biochar(PBC)produced at low temperatures and found a positive effect of pore size on microbial habitat.However,it is not clear whether this response is the result caused by soil acid conditions.The potentials of biochar to serve as a shelter for microbes and to decrease the proportion of de-functional microbes in soil result in greater bacterial biomass(Galitskayaet al.,2016).Fungal biomass,however,remains unchanged as a result of decreased fungal mobility due to their hyphal arrangement(Gonget al.,2019).This also favors microbes that rely on their extracellular enzymes to degrade PHCs in soils into compounds that can be absorbed by their cells and consumed during metabolic activity.However,it has been reported that microbes prefer to remain closer to surfaces,where they release extracellular enzymes into their surroundings(Rillig,2009).The presence of plants following biochar amendment increases the microbial respiration rate and then the PHC degradation rate,because there will be good conditions in the plant rhizosphere(Renet al.,2014;Galitskayaet al.,2016).The prevention of nutrient leaching by plants enables biochar amendment to provide sufficient nutrients(Hussain Fet al.,2018).However,there are insufficient data concerning the use of biochar for the immobilization of hydrocarbon-degrading microbes.

The surface properties of biochar,particularly surface area,pore size,pore volume,polarity,aromaticity,and hydrophobicity,are predominant among the factors affecting biochar-organic compound interactions.In general,biochar produced at higher pyrolysis temperatures has greater surface area,aromaticity,and hydrophobicity,and lower surface polarity due to the loss of O-and H-containing functional groups(Baratiet al.,2017;Karppinenet al.,2017b).Additionally,it has been reported that the surface of biochar exhibits hydrophobic or electrostatic attraction(Lehmannet al.,2011),thus enhancing its adsorption capacity.However,biochar has a low isoelectric point,i.e.,it is electrically neutral at pH＜4(Chenget al.,2019).The presence of minerals can promote electrostatic attraction or bio-oil on the surface of biochar.For example,Galitskayaet al.(2016)claimed that the biochar surface could absorb nutrients and cations from the soil solution,resulting in sufficient nutrients for microbial metabolism.

Zhanget al.(2015)found that adding biochar helped to overcome polychlorinated biphenyl toxicity to microorganisms.It is noted that biochar addition can lead to reduction in the mobility and bioaccessibility of soil contaminants.Karppinenet al.(2017b)reported that the biochar produced at lower temperatures might absorb contaminantsviaa partitioning mechanism that is relatively more accessible to microbes than the dominant adsorption process,which appears in the biochar produced at higher temperatures(600—800°C).The biochar produced at low temperature contains abundant nutrients with good adsorption performance,making it an excellent candidate in practice for remediation of PHC in soil.Admittedly,owing to the complexity and dynamics of PHCs in field conditions,the effectiveness of biochar may vary widely.The effect of biochar on pollutant stabilization in field soils may also diminish over time.Field studies at larger scales are needed to examine the long-term impact of biochar amendment on the mitigation of soil contamination under field conditions(Penget al.,2009;Beheraet al.,2019).Based on these potential changes in soil properties,biochar could stimulate PHC degradation while utilizing waste products from local industries.However,its success and practicality under field conditions have not been well studied,especially in wetland ecosystems.

Remediationof PHC and salinitybyplants and microbes

Phytoremediation includes a set of technologies that use plants and their associated microorganisms to remove pollutants from the environment or make them harmless.In addition,plant microbiology can promote the removal of organic pollutants(Maqboolet al.,2012).In particular,some studies have conducted on the purpose of combining plants and biodegradable bacteria to remove petroleum products(Penget al.,2009;Beheraet al.,2019),which seems to be a promising approach.Phytoremediation is the most beneficial repair technology because it is both economical and environmentally friendly(Fig.1).

Fig.1 Phytoremediation of pollutants by plant species including different processes such as phytodegradation and phytoextraction.

The planted soils harbor more oil-utilizing bacteria than the non-planted soils(Sorkhohet al.,2010).Several plants,such as ryegrass(LoliumLinn.)and alfalfa(Medicago sativaLinn.),have been used in phytoremediation,and the additional use of bacteria such as Proteobacteria,Firmicutes,Chloroflexi,and Acidobacteria is included to reconstruct the bacteria community(Kirket al.,2005;Gansbergeret al.,2015),which enhances PHC degradation in the contaminated soils(Chen Z Met al.,2015;Varjani,2017).Therefore,reconstruction of contaminated soil texture before phytoremediation is an excellent solution to nutrient-deficient soils(Maqboolet al.,2012).

Although many plants can absorb,degrade,and accumulate large quantities of pollutants,their growth is inhibited by these toxic contaminants(Chenet al.,2017).This reduction in plant growth ultimately reduces the plant’s capacity to remediate contaminated soil.Additionally,there is inadequate research on the application of plants for remediation of PHCs in soil.However,some studies indicate that applying bacteria that promote plant growth and degradation of pollutants feasibly is the first step in improving plant growth and plant remediation activity(Beheraet al.,2019).The inoculated bacteria must survive and colonize the rhizosphere and plant tissues such as roots(Bleicher,2016).

Microbe-assisted phytoremediation is an ecologically sound technology that uses microorganisms(bacteria,yeast,algae,protozoa,fungi,etc.)with distinctive features of metabolic potential and their products such as enzymes and biosurfactants to assist plants for the decontamination of pollutants.Phytoremediation of varying types can benefit from the use of intrinsic or extrinsic microorganisms to promote pollutant remediation.

Bacteria known as plant growth-promoting bacteria have been described as the top performers in the phytoremediation of agricultural soils because of their fast growth,diversity,ubiquity,adaptability,versatility,and ability to promote plant growth and health by fixing N,solubilizing phosphate,and K and producing phytohormones,antibiotics,and siderophores(Sarmaet al.,2019).Within bacterial groups,members of the phylum Actinobacteria,notably theStreptomycesgenus,have the most useful physiological and metabolic properties for PHC bioremediation(Zhenet al.,2019).

Studies have found that the expected changes in pH in the rhizosphere soil are often caused by acid and alkaline cations present in the soil.The number of hydrocarbon-degrading bacteria in the rhizosphere varies greatly in response to plant species and PHC concentration.High plant-to-plant variations in the number of PHC degraders and the microbial community structure and diversity among treatments with different PHC concentrations were detected(Chenget al.,2017;Hussain Fet al.,2018)and found to be caused by the accumulation of acidic metabolites(e.g.,aliphatic acids)produced by microbes during hydrocarbon degradation.

It is well known that bioavailability is one of the most important limiting factors in the bioremediation of persistent organic pollutants in soils(Gaoet al.,2010;Hilberet al.,2017).Nevertheless,there is a need to combine the technology of plant-and microbe-assisted remediation with biochar amendment in contaminated soil;thus,biochar will assist in obtaining effective plant growth and microbe functionality.

BIOCHAR,MICROBIAL,AND PLANT-BASED METHODS OFREMEDIATING DEGRADED SOILS

There are limited studies that focuse on assisted bioremediation(biochar,phytoremediation,and microbes)of PHCs in saline-sodic soil(Hanet al.,2016).However,several studies have shown that biochar can reduce the bioavailability of organic pollutants(Baratiet al.,2017;Hussain Fet al.,2018)by improving soil chemical properties(Fig.2).In general,plant-and microbe-assisted biochar amendment technology improves soil nutrient status and ameliorate potentially toxic environments for plants and microorganisms to colonize.Nonetheless,it has been noted that the use of various plant species results in the biodegradation of hydrocarbons(Al-Baldawiet al.,2015;Chenget al.,2017);thus,some plant-associated bacteria can produce biosurfactants that can boost the bioavailability of hydrocarbons and may be useful for bioremediation(Dos Santos and Maranho,2018).The use of assisted bioremediation results in a significant effect in reducing salinity and degrading PHC.Recent studies have indicated that biochar can stimulate plant growth by facilitating beneficial microorganism growth,making the combination methods environmentally friendly and sustainable.Microorganisms can secrete plant hormones and promote the absorption of nutrients in the soil,which not only directly enhances plant growth,but also improves adaptation to drought,salinity,toxicity,and organic pollutants.Comparative analyses of biochar and phytoremediation are yet to be conducted,and further research is needed.In particular,elucidation of the mechanism by which biochar assists in the degradation of PHCs and identification of the effective species that enhance microorganism survival require further in-depth studies.

Fig.2 Application of biochar improving soil chemical properties through several mechanisms for the reduction of petroleum hydrocarbon(PHC)in soil.EC=electrical conductivity;ESP=exchangeable sodium percentage;SAR=sodium adsorption ratio;CEC=cation exchange capacity.

FURTHER RESEARCH AND DEVELOPMENT NEEDS

The following lines of research are proposed,reflecting the potential attributes of bioremediation strategies.Firstly,the phytoremediation of PHCs through phytodegradation,specifically using microbe-enhanced systems,is encouraged.Secondly,future efforts should focus mainly on publishing field trials and their associated costs,enabling bioremediation by means of plants,microbes,and biochar to become a common choice for sites impacted by PHCs.There have been cost concerns about bioremediation,particularly for inorganic contaminants.

Biochar reduces pollution by ensuring rapid sorption and reducing the risks of split PHCs reaching crops and leaching into groundwater or surface runoff.Biochar rehabilitates soil physicochemical properties,supporting greater microbial stimulation and thereby enhancing the biodegradation of PHCs.Due to the heterogeneous nature of biochar resulting from production temperatures and feedstocks used,there is a need to determine the optimal type before making biochar recommendations that can absorb pollutants.

Good experimental design is essential for evaluating the efficiency of biochar amendment compared to non-amended treatments.We recommend that experiments of biochar use for sorption and biodegradation of PHCs should be designed,so that the concentration of biodegraded pollutant can be determined through comparison analysis on each method,and hence sterile soil is needed to use to validate results.This review has outlined the existing evidence for the concept,forming a basis for future work.

CONCLUSIONS

The plant-and microbe-assisted biochar amendment technology offers an emerging trend in remediation technologies for several persistent organic pollutants,especially PHCs.The usefulness of bioremediation makes it to be a better substitute for removing heavy metals from contaminated sites compared to the physiochemical techniques,which are less efficient and more expensive due to the amount of energy expended.Microorganisms and plants possess inherent biological mechanisms that enable them to survive under heavy metal stress and remove metals from the environment.Microbes use several processes,such as precipitation,biosorption,enzymatic transformation of metals,and complexation;among phytoremediation techniques,phytoextraction and phytostabilization have been very useful.Existing findings indicate that plant-based bioremediation approaches for petroleum-contaminated soils are more efficient than those for non-amended soils.The combined application of plants,microbes,and biochar has been found to affect the rhizosphere.Individually,each of these amendments can significantly improve the selected plant’s tolerance and increase the pollutant dissipation rate;the combined method,using organic modification and synergistic augmentation of microbial consortia,is more advantageous for accelerating widespread use of bioremediation for PHCs in saline-sodic soils.We recommend focusing on long-term field studies,discovering suitable removal methods,and treating potentially toxic biomass.Furthermore,we suggest that other studies should be undertaken to fill the knowledge gaps and determine the best biomass valorization options.

ACKNOWLEDGEMENT

This research was supported by the Shandong Provincial Key Research and Development Program of China—Major Science and Technology Innovation Project(No.2018CXGC0304),the Shandong Provincial Natural Science Foundation of China(No.ZR2019MD017),and the Chinese Government Scholarship(CSC).