Science of the Total Environment 610–611 (2018) 1154–1163 Contents lists available at ScienceDirect Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv Review Sorption, transport and biodegradation – An insight into bioavailability of persistent organic pollutants in soil Xiaoya Ren, Guangming Zeng ⁎, Lin Tang, Jingjing Wang, Jia Wan, Yani Liu, Jiangfang Yu, Huan Yi, Shujing Ye, Rui Deng a College of Environmental Science and Engineering, Hunan University, Changsha 410082, China b Key Laboratory of Environmental Biology and Pollution Control, Hunan University, Ministry of Education, Changsha 410082, China HIGHLIGHTS GRAPHICAL ABSTRACT • Microbial degradation of persistent or- ganic pollutants (POPs) is limited by their low bioavailability. • Sorption, transport and physiological aspects of POPs bioavailability are reviewed. • Surfactants and compost amendments affect the bioavailability of POPs. • Further researches should focus on the influence of various bioremediation strategies on the bioavailability of POPs. article info abstract Article history: Contamination of soils with persistent organic pollutants (POPs), such as organochlorine pesticide, Received 10 June 2017 polybrominated diphenyl ethers, halohydrocarbon, polycyclic aromatic hydrocarbons (PAHs) is of increasing Received in revised form 9 August 2017 concern. Microbial degradation is potential mechanism for the removal of POPs, but it is often restricted by Accepted 9 August 2017 low bioavailability of POPs. Thus, it is important to enhance bioavailability of POPs in soil bioremediation. A series Available online 30 August 2017 of reviews on bioavailability of POPs has been published in the past few years. However, bioavailability of POPs in Editor: Jay Gan relation to soil organic matter, minerals and soil microbes has been little studied. To fully understand POPs bio- availability in soil, research on interactions of POPs with soil components and microbial responses in bioavailabil- Keywords: ity limitation conditions are needed. This review focuses on bioavailability mechanisms of POPs in terms of POPs sorption, transport and microbial adaptation, which is particularly novel. In consideration of the significance of Soil organic matter bioavailability, further studies should investigate the influence of various bioremediation strategies on POPs Mineral bioavailability. Microbial adaptation © 2017 Elsevier B.V. All rights reserved. Soil amendments Contents 1. Introduction............................................................. 1155 2. SorptionofPOPsinsoil........................................................ 1155 ⁎ Corresponding author at: College of Environmental Science and Engineering, Hunan University, Changsha 410082, China. E-mail address: [email protected] (G. Zeng). http://dx.doi.org/10.1016/j.scitotenv.2017.08.089 0048-9697/© 2017 Elsevier B.V. All rights reserved. X. Ren et al. / Science of the Total Environment 610–611 (2018) 1154–1163 1155 2.1. Impactsofsoilorganicmatter................................................... 1155 2.1.1. StructurecharacteristicsofSOM.............................................. 1156 2.1.2. SpatialarrangementofSOM............................................... 1156 2.1.3. PhysicalconformationofSOM............................................... 1156 2.1.4. PolarityofSOM..................................................... 1156 2.2. Impactsofsoilminerals...................................................... 1156 2.2.1. Pureminerals...................................................... 1157 2.2.2. Mineral-SOMcomplexes................................................. 1158 3. TransportofPOPsinsoil......................................................... 1158 4. Microbialadaptationstoenhancebioavailability.............................................. 1159 4.1. Morphologicaladaptationofmicroorganisms............................................ 1159 4.2. Physiologicaladaptationofmicroorganisms............................................ 1159 4.3. Behavioraladaptationofmicroorganisms.............................................. 1160 4.4. MicrobialaccesstoadsorbedPOPs................................................. 1160 5. Conclusionsandfutureperspectives................................................... 1160 Acknowledgements............................................................. 1161 References................................................................. 1161 1. Introduction matter (SOM) and minerals to POPs; (ii) transport ways of POPs in soil; and (iii) microbial adaptations to increase bioavailability of POPs Contamination of soils with persistent organic pollutants (POPs) has under bioavailability restriction conditions. By giving a particular analy- achieved high concerns in recent years. The POPs of particular concern sis about bioavailability mechanisms of POPs, we want to provide a good include organochlorine pesticide, polybrominated diphenyl ethers research idea of bioavailability in soil bioremediation. (PBDEs), halohydrocarbon, polycyclic aromatic hydrocarbons (PAHs) (Wang et al., 2011b; Zeng et al., 2013a; Zhang et al., 2007; Zhou et al., 2014). Most of those compounds are toxic to human health even at 2. Sorption of POPs in soil low concentrations (Deng et al., 2017b; Tang et al., 2016; Tang et al., 2014; Tang et al., 2008). Microbial degradation, as an important mech- It has been reported that bioavailability of POPs was decreased after anism for the removal of POPs, is restricted by the low bioavailability adsorption by soil. With time increasing, soils form stronger binding (Chen and Ding, 2012). Therefore, increasing the bioavailability of with POPs, consequently causing a decline in bioavailability, a process POPs to degrader is important in soil bioremediation. termed as aging. Aging results in three contaminant desorption man- The National Research Council report defines “bioavailability pro- ners: the ‘rapid’, ‘slow’ and ‘very-slow domains. The rapid desorption cesses” as the individual physical, chemical, and biological interactions fractions are surface-adsorbed and interchangeable with the pore- that determine the exposure of organisms to chemicals associated water, thus readily bioavailable. However, ‘slow’ and ‘very-slow frac- with soils and sediments (Ehlers and Luthy, 2003). From the soil to tions are strongly bounded or micropore-adsorbed, making it unavail- the microorganism, bioavailability of contaminants involves a full pro- able by microorganisms (Semple et al., 2007). Slow or irreversible cess of adsorption and desorption, transport, and uptake by microor- desorption of POPs is the main factors restricting their bioavailability. ganisms (Rončević et al., 2016). Sorption process limit the substrate Although microorganisms can attack adsorbed contaminants, they pre- supplement and mass transfer of pollutants to microorganisms fer dissolved fractions (Megharaj et al., 2011). Therefore, sorption and (Kickham et al., 2012; Wang et al., 2015; Wang et al., 2013c). Therefore, desorption in soil are fundamental processes in controlling susceptibil- contaminants that adsorb strongly on soil are recalcitrant to degrada- ity of POPs to microbial degradation. Sorption of POPs is mostly affected tion, and remain in soil for a long term (Riding et al., 2013; Semple by the content and properties of SOM. Meanwhile, soil minerals also et al., 2013; Wang et al., 2013b; Wu et al., 2014). As for POPs that are play a role in sorption of POPs, especially when organic matter content bound on the inner domain of soil aggregate or micropore-adsorbed, is lower than 1% (Cheng et al., 2012). Consequently, both the properties only by the way of transport can they be accessed by microorganisms, of SOM and minerals should be considered in sorption of POPs. either POPs transfer out or microorganisms transfer in. Hence, transport of POPs should also be considered (Hu et al., 2011; Liu et al., 2012). In addition to physicochemical process, understanding the mechanisms 2.1. Impacts of soil organic matter of microorganisms to attack POPs is required in bioavailability process. Microorganisms with some special characteristics could increase the It has been well demonstrated that the sequestration capacity of soil bioavailability of POPs under physical limitation conditions. For exam- to POPs is strongly connected to the proportion of SOM (Lima et al., ple, micropore-adsorbed POPs are unable to be attached by microorgan- 2012). However, soils with the same organic matter content may have isms. In this case, secretion of biosurfactant or hypha structure is different sorption potentials for POPs. SOM is a heterogeneous mixture important (Fester et al., 2014; Pacwa-Płociniczak et al., 2011). To deal including newly deposited biopolymers (e.g., proteins, polysaccharides, with the problem of deficient solubility of POPs, formation of biofilm, se- and lipids), moderately aged humic substances (HSs), well matured cretion of biosurfactant or change of cell wall properties are possible mi- kerogen and black carbon, each of which are potential sorbents for crobial response (Johnsen and Karlson, 2004; Pacwa-Płociniczak et al., POPs (Mechlińska et al., 2009). In the study of Liu et al. (2010), sorption 2011; Wick et al., 2002b). coefficient (KOC) of phenanthrene followed the descending order of Several reviews have reported biodegradation mechanisms of POPs humin (HM), humic acid (HA) and fulvic acid (FA). Zhu et al. (2016) re- during bioremediation (Johnsen et al., 2005; Ortega-Calvo et al.,