Review Overview of Approaches to Improve Rhizoremediation of Petroleum Hydrocarbon-Contaminated Soils Fahad Alotaibi 1,2, Mohamed Hijri 1,3 and Marc St-Arnaud 1,* 1 Biodiversity Centre, Institut de Recherche en Biologie Végétale, Université de Montréal and Jardin Botanique de Montréal, Montréal, QC 22001, Canada; [email protected] (F.A.); [email protected] (M.H.) 2 Department of Soil Science, King Saud University, Riyadh 11564, Saudi Arabia 3 African Genome Center, Mohammed VI Polytechnic University (UM6P), Ben Guerir 43150, Morocco * Correspondence: [email protected] Abstract: Soil contamination with petroleum hydrocarbons (PHCs) has become a global concern and has resulted from the intensification of industrial activities. This has created a serious environmental issue; therefore, there is a need to find solutions, including application of efficient remediation technologies or improvement of current techniques. Rhizoremediation is a green technology that has received global attention as a cost-effective and possibly efficient remediation technique for PHC- polluted soil. Rhizoremediation refers to the use of plants and their associated microbiota to clean up contaminated soils, where plant roots stimulate soil microbes to mineralize organic contaminants to H2O and CO2. However, this multipartite interaction is complicated because many biotic and abiotic factors can influence microbial processes in the soil, making the efficiency of rhizoremediation unpredictable. This review reports the current knowledge of rhizoremediation approaches that can Citation: Alotaibi, F.; Hijri, M.; accelerate the remediation of PHC-contaminated soil. Recent approaches discussed in this review St-Arnaud, M. Overview of include (1) selecting plants with desired characteristics suitable for rhizoremediation; (2) exploiting Approaches to Improve and manipulating the plant microbiome by using inoculants containing plant growth-promoting rhi- Rhizoremediation of Petroleum zobacteria (PGPR) or hydrocarbon-degrading microbes, or a combination of both types of organisms; Hydrocarbon-Contaminated Soils. (3) enhancing the understanding of how the host–plant assembles a beneficial microbiome, and how Appl. Microbiol. 2021, 1, 329–351. it functions, under pollutant stress. A better understanding of plant–microbiome interactions could https://doi.org/10.3390/ lead to successful use of rhizoremediation for PHC-contaminated soil in the future. applmicrobiol1020023 Keywords: phytoremediation; PGPR; hydrocarbon-degrading bacteria; Salix; contaminated soils; Academic Editor: Katarzyna Turnau alkanes; PAHs Received: 26 May 2021 Accepted: 6 August 2021 Published: 10 August 2021 1. Introduction Publisher’s Note: MDPI stays neutral Industrial activities, including mining and extraction of oil and gas, as well as chemical with regard to jurisdictional claims in inputs into agricultural production systems, have led to different degrees of environmental published maps and institutional affil- contamination worldwide. Petroleum hydrocarbons (PHCs) are among the major pollu- iations. tants that can pose a serious environmental threat. PHC products have adversely affected various ecosystems, causing disturbing damage to natural habitats with serious economic consequences [1]. PHCs are heterogeneous organic mixtures composed of carbon and hydrogen atoms arranged in varying structural configurations and have different physical and chemical Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. properties [2]. These compounds consist mainly of hydrocarbons and fewer numbers of This article is an open access article other non-hydrocarbon constituents, such as nitrogen, oxygen, and sulfur [3,4]. They are distributed under the terms and broadly classified into two major fractions: aliphatic hydrocarbons and aromatic hydrocar- conditions of the Creative Commons bons (Figure1). Prior to processing, PHCs are composed, on average, of ~57% aliphatic Attribution (CC BY) license (https:// hydrocarbons, ~29% aromatic hydrocarbons, and ~14% asphaltenes and other polar com- creativecommons.org/licenses/by/ pounds containing nitrogen, oxygen, and sulfur [5]. Aliphatic hydrocarbons include both 4.0/). linear or branched-chain hydrocarbons, which may be unsaturated (alkenes and alkynes) or Appl. Microbiol. 2021, 1, 329–351. https://doi.org/10.3390/applmicrobiol1020023 https://www.mdpi.com/journal/applmicrobiol Appl. Microbiol. 2021, 1, FOR PEER REVIEW 2 hydrocarbons, ~29% aromatic hydrocarbons, and ~14% asphaltenes and other polar com- Appl. Microbiol. 2021, 1 330 pounds containing nitrogen, oxygen, and sulfur [5]. Aliphatic hydrocarbons include both linear or branched-chain hydrocarbons, which may be unsaturated (alkenes and alkynes) or saturated (alkanes) [6]. Aromatic hydrocarbons include monocyclic (i.e., benzene, tol- uene,saturated phenol, (alkanes) etc.) and [6]. polycyclic Aromatic hydrocarbonsaromatic hydrocarbons include monocyclic (PAHs) (Figure (i.e., benzene, 1). PHCs toluene, are the mostphenol, common etc.) and pollutants polycyclic in soil aromatic and ground hydrocarbons water worldwide. (PAHs) (Figure The ever-1) . PHCsincreasing are the depend- most encycommon of modern pollutants society inon soilfuel andfor energy ground genera watertion worldwide. in many vital The sectors, ever- suchincreasing as electricity dependency, heat, industry,of modern and society transportation on fuel for energyhas resulted generation in the in manyextensive vital exploitation sectors, such of as PHCs electricity [2]., heatAlt-, houghindustry, environmental and transportation transitionhas actions resulted have in thebeen extensive taken in exploitationmany countries, of PHCs dependency [2]. Al- onthough petroleum environmental will last for transition some decades, actions havecontributing been taken to organic in many pollution countries, risks. dependency on petroleum will last for some decades, contributing to organic pollution risks. Figure 1. Schematic diagram showing the classification of PHCs. Figure 1. Schematic diagram showing the classification of PHCs. Soil contamination with PHCs is an international issue, and the magnitude of soil Soil contamination with PHCs is an international issue, and the magnitude of soil pollution is hard to quantify. For example, in Australia, around 80,000 sites are estimated pollution is hard to quantify. For example, in Australia, around 80,000 sites are estimated to be contaminated by PHCs [7], whereas in Canada around 22,000 federal-owned sites are toidentified be contaminated as being contaminated by PHCs [7], by whereas PHCs [8 in]. InCanada Europe, around PHC contamination 22,000 federal-owned was observed sites arein at identified least 342,000 as being sites [contaminated9]. These organic by PHCs contaminants [8]. In Europe, also pose PHC serious contamination health risks was to observedhumans andin at other least organisms342,000 sites in [9]. addition These toorganic their adversecontaminants impact also on pose the soil serious microflora, health risksleading to humans to environmental and other qualityorganisms degradation. in addition For to instance,their adverse some impact aromatic on the substances, soil mi- croflora,such as BTEX leading and to PAHs, environmental are notorious quality mutagens degradation. and carcinogens For instance, that some can enteraromatic our foodsub- stances,chain together such as with BTEX lipophilic and PAHs, compounds are notorious [10], andmutagens they have and beencarcinogens linked withthat can probable enter ourcauses food of chain bladder, together kidney, with liver, lipophilic lung, and compou skin cancers.nds [10], This and explains they have the been growing linked concern with probablewith these causes contaminants of bladder, and kidney, the urgent liver, lu needng, and to use skin all cancers. possible This means explains to protect the grow- the ingenvironment concern with and tothese find contaminants the appropriate and techniques the urgent to need remediate to use polluted all possible soils. means to protectVarious the environment chemical, physical, and to andfind thermalthe appropriate conventional techniques techniques to remediate have been polluted used to soils.remediate soils contaminated with PHCs. These conventional methods, which can contain, destroy,Various or separate chemical, the physical, pollutants, and include thermal a wide conv rangeentional of both techniques in situ andhave ex been situ cleanupused to remediatetechnologies, soils such contaminated as asphalt batching, with PHCs. biopiles, These chemical conventional oxidation, methods, excavation, which hydrolysis, can con- tain,incineration, destroy, photolysis, or separate pump the pollutants, and treat, multi-phasedinclude a wide slurry range reactors, of both soil in vaporsitu and extraction, ex situ cleanupsoil washing, technologies, and thermal such desorption. as asphalt However,batching, thesebiopiles, methods chemical have oxidation, particular excavation, limitations. hydrolysis,First, their cost incineration, is often prohibitive; photolysis, for pump example, and treat, it can multi-phas cost betweened USD slurry 480 reactors, and 813 soil per va- m3 porfor extractionextraction, [ 11soil]. Second,washing, chemical and thermal procedures desorption. only work However, for specific these organicmethods compounds, have par- ticularand they limitations. most often First, destroy their soilcost microbialis often prohibitive; communities. for example, Third, these it can methods