List of the contaminants/substances identified in this review, the agroecological practice involved, the behavior in the soil and ecotoxicological impact of the contaminant/substance on soil microorganisms.
| Contaminant/substance . | Agroecological practice involved . | Behavior of the contaminant/substance in the soil . | Ecotoxicological impact on soil microorganisms . |
|---|---|---|---|
| Heavy metals1 | |||
| As, Cd, Cr, Hg, Ni, Pb, Se | Organic fertilization (SS, MSW, composts and digestates) | Mobility, bioavailability and toxicity differ according to the chemical speciation (free ionic, complexed, precipitated, oxidation state). | Above a certain threshold, HM are toxic for microorganisms. HM toxicity act primarily at a cellular level, due to the following characteristics: |
| Cu, Zn | Organic fertilization (livestock manure, SS, MSW, composts and digestates) | No degradation possible. Regular application leads to an accumulation in the long term (often significant for Cu and Zn). A part of the total metal concentration in soil is irreversibly linked to or sequestered by the soil matrix.Low solubility (for consequent low lixiviation). HM concentration in a soil solution is influenced mainly by the soil pH, but also by redox potential, clay content and presence of soil organic matter (SOM). Only a fraction of HMs in solution are bioavailable (plants and other biota). It is generally assumed that the free ion is the chemical species which is taken up and causes toxicity when present in excess. Other chemical forms or forms chelated by organic molecules cannot be taken up directly. | • high affinity for negatively charged cellular groups, such as sulfhydryls, phosphates and hydroxyls;• generation of reactive oxygen species, causing oxidative stress;• competition with essential ions acquisition;• disturbance of cellular ion balance and osmotic regulation. A summary of the literature on metal toxicity to soil microbial processes and populations reveal an enormous variability in the data. Two factors contribute to the discrepancies between studies: (1) factors which modify the toxicity/bioavailability of the metals and (2) differences in sensitivity of the microorganism(s) or microbial process(es). Heavy metal concentrations in soils at around current European Union limits have been shown to decrease total microbial biomass, diversity and activity. While most studies focus on the total community, more subtle changes in microbial community structure can also be observed, such as alterations in relative abundance of particular microbial groups or species of agronomical importance. For example, nitrogen-fixing rhizobia are sensitive to metal toxicity. Long-term heavy metal contamination in soil is a selection pressure which can promote bacterial species able to develop HM resistance. |
| Biological contaminants2 | |||
| Human and animal pathogens (prions, viruses, bacteria, protozoa, helminths) | Organic fertilization (SS, livestock manure, slaughterhouse waste) | Survival times variable, from a few days to multiple years (e.g. <35 to 231 days for Salmonella; from <2 weeks to >6 months for enteroviruses). Persistence in the soil is favored by low temperature, high humidity, low light intensity and neutral pH; and by a deep application of OWP. | Interaction with other organisms (predation, competition, antagonism). Poorly characterized. |
| Antibiotic-resistant bacteria (ARB) and Antibiotic resistance genes (ARG) | Organic fertilization (SS, livestock manure, digestates) | The fate of ARBs and ARGs from OWP in soil and their contribution to the overall problem of antibiotic resistance are poorly characterized. Soil bacteria inherently contain ARGs, which makes studies very difficult. Environmental microorganisms are hypothesized to be the main source of antibiotics as well as the concomitant antibiotic resistance.The large numbers of resistant bacteria entering the soil through OWP are likely to compete with other bacteria or survive in the soil environment. | OWP application can increase antibiotic resistance in the soil microflora through several effects:● horizontal gene transfer (HGT) of fecal-derived ARGs to native soil microorganisms. HGT mainly includes three pathways mediated by mobile genetic elements, namely extracellular DNA-mediated transformation, plasmid-mediated conjugation, and phage-mediated transduction. |
| ● mutation in the native soil microorganisms through the selection pressure exerted by the residues of antibiotics, metals, PAHs and biocides, causing the appearance of new resistant microorganisms (see section on antibiotics).Although several studies supporting the two concepts have been published, available data are still inconclusive and do not provide direct evidence that links specific factors to individual ARGs. | |||
| Trace organic contaminants | |||
| 1. Persistent organic pollutants (POP)3 | |||
| Organochlorine pesticides:aldrin, chlordane, DDT, dieldrin, endrin, heptachlor, hexachlorobenzene, mirex, toxaphene | Organic fertilization (SS, green manure, crop residues, food residues, MSW,composts, digestates) | ● Persistent, risk of long-term accumulation in soils. Half-life: years or decades in soil/sediment.Fates of the pollutants:● Dissipation from soils by biodegradation and photodegradation (low degradability). | Hydrophobic and highly lipid-soluble chemicals. They accumulate in the membrane bilayer between the acyl chains of fatty acids and increase membrane fluidity. Few studies on the impact of POP on soil microorganisms, even less data on the impact of degradation metabolites. |
| Industrial chemicals:Hexachlorobenzene, polychlorinated biphenyls (PCBs), Polybrominated diphenyl ethers (PBDE), perfluorinated compound (PFC) | Biological decomposition is the most important and effective way to remove these compounds from the environment.● Binding to soil solid phases, mainly to SOM but also to the mineral fraction. Pollutant bioavailability decreases with increasing soil-pollutant contact time (= ageing process). ● Transfer to water (leaching to groundwater and surface water). | POP exposure might alter the microbial community structure and the metabolic pathways/activities (shown for gut microbiome and pelagic bacterial communities). It has been shown to:● Induce profound changes in bacterial lipid profiles ● Disturb bacterial energy metabolism pathways | |
| By-products:hexachlorobenzene (HCB), polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans (PCDD/PCDF), Polycyclic aromatic hydrocarbons (PAHs) | ● Because they are semi-volatile, POPs are transported over long distances in the atmosphere.● Transfer to plants and Bioaccumulation. | ● Disruption in protein export● Induction of bacterial membrane biogenesis● Induction of stress response pathways● Induction of defense of DNA damage | |
| 2. Low to medium persistence organic products4 | |||
| Polydiméthylsiloxane (PDMS),Linear alkylbenzene sulphonates (LAS), phtalates and bisphenols | Organic fertilization (SS, MSW, composts digestates) | Limited data available on the fate and occurrence of low to medium persistence organic products.Half-life: few days to few years (variable according to the chemical). | Variable ecotoxicological impacts on soil organisms, according to the chemical. Limited data available.For antibiotics: exert a selection pressure on soil microorganisms, conferring antibiotic resistance. Co-exposure to metals, PAHs and biocides increase the appearance of new resistant microorganisms. Antibiotic residues can adversely affect microbial processes in the environment (e.g. nutrient cycling and pollutant degradation). |
| Pharmaceuticals and personal care products (antibiotics,antidepressants, endocrine disruptors, fragrances, amongst others) | Organic fertilization (SS, livestock manure, composts, digestates) | ● Transformation/degradation through biodegradation, photodegradation and hydrolysis (principally driven by enzymatic transformations conducted by microorganisms)● Soil adsorption: main physicochemical mechanism that prevents leaching or runoff to some extent. Adsorption depends on the | |
| Some pesticides | Organic fertilization (SS, green manure and crop residues,MSW, composts, digestates) | chemical, soil properties (including pH, organic matter content, and the concentration and type of divalent cations present), influence of temperature and humidity● Transport to surface and groundwaters (leaching and runoff). Dissolved organic matter increase their mobility.● Transfer to plants | |
| “Eco-friendly” herbicides5 | |||
| β-triketone herbicides: sulcotrione, mesotrione and tembotrione | Crop protection: weed management | Low mobility in soils. Half-life time of 4 to 144 days depending on soil properties. | No effects on soil microbial diversity and abundance at agronomical dose but some molecule-, dose- and strain-dependent effects at the population level. |
| Pelargonic acid | Very high to low mobility in soil. Half-life time of 1.6 days. | Ecotoxicological effects on soil microbial communities have not been studied yet. | |
| Simple organic acids: acetic acid | Very high mobility in soil. Half-life time of 0.85 to 1.23 days. | No significant effects on the structure and the diversity of soil microbial communities. | |
| Biopesticides6 | |||
| Bacillus thuringiensis | Crop protection: microbial pesticides | Efficient degradation of Bt proteins in soil. Lack of data concerning the toxicity of the accumulation of some Bt endotoxins in soils. | Limited impact on microbial community structure and microbial diversity in soil. |
| Trichoderma | No information available. | Some studies show an impact of volatiles, toxins and antibiotics produced by Trichoderma on soil microbiome. | |
| Pseudomonas | No information available. | Various effects observed, from no prominent alteration of bacterial communities to substantial shift within microbial communities (sometimes suggested as an indirect mode of action). | |
| Spinosad (Saccharopolyspora spinosa) | Relatively fast dissipation of spinosad in soil—Half-life between 1.11 and 2.21 days7 | Effects on soil enzymatic activities are recorded at high doses or in the short term after application but no negative effects in the long term at the recommended doses of application. | |
| Entomopathogenic fungi | No information available. | No or limited adverse effects recorded on soil microbial communities. | |
| Entomopathogenic viruses | No information available. | The little studies available tend to show low ecotoxicological risk. | |
| Azadirachtin | Crop protection: Botanical pesticides | Low mobility in soil due to its oily composition. No consensus in the literature on its half-life (from a few hours to 8–10 days). Formulated products can have a half-life up to 26 days.8 | Studies report a toxicity on certain soil microbial groups, somewhat comparable to that observed under the effect of chemical pesticides. |
| Pyrethroids | Soil bacterial and fungal strains are able to degrade pyrethroids into non-toxic compounds through hydrolysis of ester bond by enzyme esterase/carboxyl esterase. | No observed negative impact to soil microbial community. | |
| Essential oils | Essential oils are known to be easily degraded (mainly by oxidation). | Effects mostly unknown and poorly described. | |
| Elicitors, pheromones, allelochemicals, double stranded RNA (dsRNA)-based pesticides and pesticidal substances containing added genetic material | Crop protection: Biochemical pesticides, semiochemi-cals and plant incorporated protectants | No information available | Effects mostly unknown and poorly described but mode of action suggest limited off-target toxicity effects. |
| Nanopesticides | Crop protection: Nanopesticides | Few studies available on the behavior in soils. Behavior is depending on the nature of the nanoparticles and of the inorganic nanocarriers. | Some studies tend to show a microbial toxicity of the inorganic nanocarriers. |
| Mineral pesticides | |||
| Copper | Crop protection: mineral pesticide | Mobility, bioavailability and toxicity differ according to the chemical speciation (free ionic, complexed, precipitated, oxidation state).No degradation possible. Regular application leads to an accumulation in the long term. Please also refer to the heavy metal section. | Negative effects on soil microbial biomass and biodiversity. Please also refer to the heavy metal section. |
| Microplastics9 | |||
| Coming from the breakdown of biodegradable plastics: starch-based, polylactide-based or polyhydroxyalkanoate-based | Crop protection: weed management (mulching) | Few studies available: slight degradation of polylactide-based plastics after 12 months in field conditions10 | Mainly studied in aquatic environments. Soil studies focus on their biodegradation, not on their ecotoxicological impact. |
| Contaminant/substance . | Agroecological practice involved . | Behavior of the contaminant/substance in the soil . | Ecotoxicological impact on soil microorganisms . |
|---|---|---|---|
| Heavy metals1 | |||
| As, Cd, Cr, Hg, Ni, Pb, Se | Organic fertilization (SS, MSW, composts and digestates) | Mobility, bioavailability and toxicity differ according to the chemical speciation (free ionic, complexed, precipitated, oxidation state). | Above a certain threshold, HM are toxic for microorganisms. HM toxicity act primarily at a cellular level, due to the following characteristics: |
| Cu, Zn | Organic fertilization (livestock manure, SS, MSW, composts and digestates) | No degradation possible. Regular application leads to an accumulation in the long term (often significant for Cu and Zn). A part of the total metal concentration in soil is irreversibly linked to or sequestered by the soil matrix.Low solubility (for consequent low lixiviation). HM concentration in a soil solution is influenced mainly by the soil pH, but also by redox potential, clay content and presence of soil organic matter (SOM). Only a fraction of HMs in solution are bioavailable (plants and other biota). It is generally assumed that the free ion is the chemical species which is taken up and causes toxicity when present in excess. Other chemical forms or forms chelated by organic molecules cannot be taken up directly. | • high affinity for negatively charged cellular groups, such as sulfhydryls, phosphates and hydroxyls;• generation of reactive oxygen species, causing oxidative stress;• competition with essential ions acquisition;• disturbance of cellular ion balance and osmotic regulation. A summary of the literature on metal toxicity to soil microbial processes and populations reveal an enormous variability in the data. Two factors contribute to the discrepancies between studies: (1) factors which modify the toxicity/bioavailability of the metals and (2) differences in sensitivity of the microorganism(s) or microbial process(es). Heavy metal concentrations in soils at around current European Union limits have been shown to decrease total microbial biomass, diversity and activity. While most studies focus on the total community, more subtle changes in microbial community structure can also be observed, such as alterations in relative abundance of particular microbial groups or species of agronomical importance. For example, nitrogen-fixing rhizobia are sensitive to metal toxicity. Long-term heavy metal contamination in soil is a selection pressure which can promote bacterial species able to develop HM resistance. |
| Biological contaminants2 | |||
| Human and animal pathogens (prions, viruses, bacteria, protozoa, helminths) | Organic fertilization (SS, livestock manure, slaughterhouse waste) | Survival times variable, from a few days to multiple years (e.g. <35 to 231 days for Salmonella; from <2 weeks to >6 months for enteroviruses). Persistence in the soil is favored by low temperature, high humidity, low light intensity and neutral pH; and by a deep application of OWP. | Interaction with other organisms (predation, competition, antagonism). Poorly characterized. |
| Antibiotic-resistant bacteria (ARB) and Antibiotic resistance genes (ARG) | Organic fertilization (SS, livestock manure, digestates) | The fate of ARBs and ARGs from OWP in soil and their contribution to the overall problem of antibiotic resistance are poorly characterized. Soil bacteria inherently contain ARGs, which makes studies very difficult. Environmental microorganisms are hypothesized to be the main source of antibiotics as well as the concomitant antibiotic resistance.The large numbers of resistant bacteria entering the soil through OWP are likely to compete with other bacteria or survive in the soil environment. | OWP application can increase antibiotic resistance in the soil microflora through several effects:● horizontal gene transfer (HGT) of fecal-derived ARGs to native soil microorganisms. HGT mainly includes three pathways mediated by mobile genetic elements, namely extracellular DNA-mediated transformation, plasmid-mediated conjugation, and phage-mediated transduction. |
| ● mutation in the native soil microorganisms through the selection pressure exerted by the residues of antibiotics, metals, PAHs and biocides, causing the appearance of new resistant microorganisms (see section on antibiotics).Although several studies supporting the two concepts have been published, available data are still inconclusive and do not provide direct evidence that links specific factors to individual ARGs. | |||
| Trace organic contaminants | |||
| 1. Persistent organic pollutants (POP)3 | |||
| Organochlorine pesticides:aldrin, chlordane, DDT, dieldrin, endrin, heptachlor, hexachlorobenzene, mirex, toxaphene | Organic fertilization (SS, green manure, crop residues, food residues, MSW,composts, digestates) | ● Persistent, risk of long-term accumulation in soils. Half-life: years or decades in soil/sediment.Fates of the pollutants:● Dissipation from soils by biodegradation and photodegradation (low degradability). | Hydrophobic and highly lipid-soluble chemicals. They accumulate in the membrane bilayer between the acyl chains of fatty acids and increase membrane fluidity. Few studies on the impact of POP on soil microorganisms, even less data on the impact of degradation metabolites. |
| Industrial chemicals:Hexachlorobenzene, polychlorinated biphenyls (PCBs), Polybrominated diphenyl ethers (PBDE), perfluorinated compound (PFC) | Biological decomposition is the most important and effective way to remove these compounds from the environment.● Binding to soil solid phases, mainly to SOM but also to the mineral fraction. Pollutant bioavailability decreases with increasing soil-pollutant contact time (= ageing process). ● Transfer to water (leaching to groundwater and surface water). | POP exposure might alter the microbial community structure and the metabolic pathways/activities (shown for gut microbiome and pelagic bacterial communities). It has been shown to:● Induce profound changes in bacterial lipid profiles ● Disturb bacterial energy metabolism pathways | |
| By-products:hexachlorobenzene (HCB), polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans (PCDD/PCDF), Polycyclic aromatic hydrocarbons (PAHs) | ● Because they are semi-volatile, POPs are transported over long distances in the atmosphere.● Transfer to plants and Bioaccumulation. | ● Disruption in protein export● Induction of bacterial membrane biogenesis● Induction of stress response pathways● Induction of defense of DNA damage | |
| 2. Low to medium persistence organic products4 | |||
| Polydiméthylsiloxane (PDMS),Linear alkylbenzene sulphonates (LAS), phtalates and bisphenols | Organic fertilization (SS, MSW, composts digestates) | Limited data available on the fate and occurrence of low to medium persistence organic products.Half-life: few days to few years (variable according to the chemical). | Variable ecotoxicological impacts on soil organisms, according to the chemical. Limited data available.For antibiotics: exert a selection pressure on soil microorganisms, conferring antibiotic resistance. Co-exposure to metals, PAHs and biocides increase the appearance of new resistant microorganisms. Antibiotic residues can adversely affect microbial processes in the environment (e.g. nutrient cycling and pollutant degradation). |
| Pharmaceuticals and personal care products (antibiotics,antidepressants, endocrine disruptors, fragrances, amongst others) | Organic fertilization (SS, livestock manure, composts, digestates) | ● Transformation/degradation through biodegradation, photodegradation and hydrolysis (principally driven by enzymatic transformations conducted by microorganisms)● Soil adsorption: main physicochemical mechanism that prevents leaching or runoff to some extent. Adsorption depends on the | |
| Some pesticides | Organic fertilization (SS, green manure and crop residues,MSW, composts, digestates) | chemical, soil properties (including pH, organic matter content, and the concentration and type of divalent cations present), influence of temperature and humidity● Transport to surface and groundwaters (leaching and runoff). Dissolved organic matter increase their mobility.● Transfer to plants | |
| “Eco-friendly” herbicides5 | |||
| β-triketone herbicides: sulcotrione, mesotrione and tembotrione | Crop protection: weed management | Low mobility in soils. Half-life time of 4 to 144 days depending on soil properties. | No effects on soil microbial diversity and abundance at agronomical dose but some molecule-, dose- and strain-dependent effects at the population level. |
| Pelargonic acid | Very high to low mobility in soil. Half-life time of 1.6 days. | Ecotoxicological effects on soil microbial communities have not been studied yet. | |
| Simple organic acids: acetic acid | Very high mobility in soil. Half-life time of 0.85 to 1.23 days. | No significant effects on the structure and the diversity of soil microbial communities. | |
| Biopesticides6 | |||
| Bacillus thuringiensis | Crop protection: microbial pesticides | Efficient degradation of Bt proteins in soil. Lack of data concerning the toxicity of the accumulation of some Bt endotoxins in soils. | Limited impact on microbial community structure and microbial diversity in soil. |
| Trichoderma | No information available. | Some studies show an impact of volatiles, toxins and antibiotics produced by Trichoderma on soil microbiome. | |
| Pseudomonas | No information available. | Various effects observed, from no prominent alteration of bacterial communities to substantial shift within microbial communities (sometimes suggested as an indirect mode of action). | |
| Spinosad (Saccharopolyspora spinosa) | Relatively fast dissipation of spinosad in soil—Half-life between 1.11 and 2.21 days7 | Effects on soil enzymatic activities are recorded at high doses or in the short term after application but no negative effects in the long term at the recommended doses of application. | |
| Entomopathogenic fungi | No information available. | No or limited adverse effects recorded on soil microbial communities. | |
| Entomopathogenic viruses | No information available. | The little studies available tend to show low ecotoxicological risk. | |
| Azadirachtin | Crop protection: Botanical pesticides | Low mobility in soil due to its oily composition. No consensus in the literature on its half-life (from a few hours to 8–10 days). Formulated products can have a half-life up to 26 days.8 | Studies report a toxicity on certain soil microbial groups, somewhat comparable to that observed under the effect of chemical pesticides. |
| Pyrethroids | Soil bacterial and fungal strains are able to degrade pyrethroids into non-toxic compounds through hydrolysis of ester bond by enzyme esterase/carboxyl esterase. | No observed negative impact to soil microbial community. | |
| Essential oils | Essential oils are known to be easily degraded (mainly by oxidation). | Effects mostly unknown and poorly described. | |
| Elicitors, pheromones, allelochemicals, double stranded RNA (dsRNA)-based pesticides and pesticidal substances containing added genetic material | Crop protection: Biochemical pesticides, semiochemi-cals and plant incorporated protectants | No information available | Effects mostly unknown and poorly described but mode of action suggest limited off-target toxicity effects. |
| Nanopesticides | Crop protection: Nanopesticides | Few studies available on the behavior in soils. Behavior is depending on the nature of the nanoparticles and of the inorganic nanocarriers. | Some studies tend to show a microbial toxicity of the inorganic nanocarriers. |
| Mineral pesticides | |||
| Copper | Crop protection: mineral pesticide | Mobility, bioavailability and toxicity differ according to the chemical speciation (free ionic, complexed, precipitated, oxidation state).No degradation possible. Regular application leads to an accumulation in the long term. Please also refer to the heavy metal section. | Negative effects on soil microbial biomass and biodiversity. Please also refer to the heavy metal section. |
| Microplastics9 | |||
| Coming from the breakdown of biodegradable plastics: starch-based, polylactide-based or polyhydroxyalkanoate-based | Crop protection: weed management (mulching) | Few studies available: slight degradation of polylactide-based plastics after 12 months in field conditions10 | Mainly studied in aquatic environments. Soil studies focus on their biodegradation, not on their ecotoxicological impact. |
Acronyms: OWP—organic waste product; SS—sewage sludge; MSW—municipal solid waste; SOM—soil organic matter; HM—heavy metal; ARB—Antibiotic-resistant bacteria; ARG—antibiotic resistance genes; HGT—horizontal gene transfer; MGEs—mobile genetic elements; PAHs—poly-aromatic hydrocarbons; POP—persistent organic pollutants; DDT –; PCB—polychlorinated biphenyls; PBDE—Polybrominated diphenyl ethers; PFC—perfluorinated compound; HCB—hexachlorobenzene; PCDD/PCDF—polychlorinated dibenzo-p-dioxins and furans; PAHs—Polycyclic aromatic hydrocarbons; PDMS—Polydiméthylsiloxane; LAS—Linear alkylbenzene sulphonates.
List of the contaminants/substances identified in this review, the agroecological practice involved, the behavior in the soil and ecotoxicological impact of the contaminant/substance on soil microorganisms.
| Contaminant/substance . | Agroecological practice involved . | Behavior of the contaminant/substance in the soil . | Ecotoxicological impact on soil microorganisms . |
|---|---|---|---|
| Heavy metals1 | |||
| As, Cd, Cr, Hg, Ni, Pb, Se | Organic fertilization (SS, MSW, composts and digestates) | Mobility, bioavailability and toxicity differ according to the chemical speciation (free ionic, complexed, precipitated, oxidation state). | Above a certain threshold, HM are toxic for microorganisms. HM toxicity act primarily at a cellular level, due to the following characteristics: |
| Cu, Zn | Organic fertilization (livestock manure, SS, MSW, composts and digestates) | No degradation possible. Regular application leads to an accumulation in the long term (often significant for Cu and Zn). A part of the total metal concentration in soil is irreversibly linked to or sequestered by the soil matrix.Low solubility (for consequent low lixiviation). HM concentration in a soil solution is influenced mainly by the soil pH, but also by redox potential, clay content and presence of soil organic matter (SOM). Only a fraction of HMs in solution are bioavailable (plants and other biota). It is generally assumed that the free ion is the chemical species which is taken up and causes toxicity when present in excess. Other chemical forms or forms chelated by organic molecules cannot be taken up directly. | • high affinity for negatively charged cellular groups, such as sulfhydryls, phosphates and hydroxyls;• generation of reactive oxygen species, causing oxidative stress;• competition with essential ions acquisition;• disturbance of cellular ion balance and osmotic regulation. A summary of the literature on metal toxicity to soil microbial processes and populations reveal an enormous variability in the data. Two factors contribute to the discrepancies between studies: (1) factors which modify the toxicity/bioavailability of the metals and (2) differences in sensitivity of the microorganism(s) or microbial process(es). Heavy metal concentrations in soils at around current European Union limits have been shown to decrease total microbial biomass, diversity and activity. While most studies focus on the total community, more subtle changes in microbial community structure can also be observed, such as alterations in relative abundance of particular microbial groups or species of agronomical importance. For example, nitrogen-fixing rhizobia are sensitive to metal toxicity. Long-term heavy metal contamination in soil is a selection pressure which can promote bacterial species able to develop HM resistance. |
| Biological contaminants2 | |||
| Human and animal pathogens (prions, viruses, bacteria, protozoa, helminths) | Organic fertilization (SS, livestock manure, slaughterhouse waste) | Survival times variable, from a few days to multiple years (e.g. <35 to 231 days for Salmonella; from <2 weeks to >6 months for enteroviruses). Persistence in the soil is favored by low temperature, high humidity, low light intensity and neutral pH; and by a deep application of OWP. | Interaction with other organisms (predation, competition, antagonism). Poorly characterized. |
| Antibiotic-resistant bacteria (ARB) and Antibiotic resistance genes (ARG) | Organic fertilization (SS, livestock manure, digestates) | The fate of ARBs and ARGs from OWP in soil and their contribution to the overall problem of antibiotic resistance are poorly characterized. Soil bacteria inherently contain ARGs, which makes studies very difficult. Environmental microorganisms are hypothesized to be the main source of antibiotics as well as the concomitant antibiotic resistance.The large numbers of resistant bacteria entering the soil through OWP are likely to compete with other bacteria or survive in the soil environment. | OWP application can increase antibiotic resistance in the soil microflora through several effects:● horizontal gene transfer (HGT) of fecal-derived ARGs to native soil microorganisms. HGT mainly includes three pathways mediated by mobile genetic elements, namely extracellular DNA-mediated transformation, plasmid-mediated conjugation, and phage-mediated transduction. |
| ● mutation in the native soil microorganisms through the selection pressure exerted by the residues of antibiotics, metals, PAHs and biocides, causing the appearance of new resistant microorganisms (see section on antibiotics).Although several studies supporting the two concepts have been published, available data are still inconclusive and do not provide direct evidence that links specific factors to individual ARGs. | |||
| Trace organic contaminants | |||
| 1. Persistent organic pollutants (POP)3 | |||
| Organochlorine pesticides:aldrin, chlordane, DDT, dieldrin, endrin, heptachlor, hexachlorobenzene, mirex, toxaphene | Organic fertilization (SS, green manure, crop residues, food residues, MSW,composts, digestates) | ● Persistent, risk of long-term accumulation in soils. Half-life: years or decades in soil/sediment.Fates of the pollutants:● Dissipation from soils by biodegradation and photodegradation (low degradability). | Hydrophobic and highly lipid-soluble chemicals. They accumulate in the membrane bilayer between the acyl chains of fatty acids and increase membrane fluidity. Few studies on the impact of POP on soil microorganisms, even less data on the impact of degradation metabolites. |
| Industrial chemicals:Hexachlorobenzene, polychlorinated biphenyls (PCBs), Polybrominated diphenyl ethers (PBDE), perfluorinated compound (PFC) | Biological decomposition is the most important and effective way to remove these compounds from the environment.● Binding to soil solid phases, mainly to SOM but also to the mineral fraction. Pollutant bioavailability decreases with increasing soil-pollutant contact time (= ageing process). ● Transfer to water (leaching to groundwater and surface water). | POP exposure might alter the microbial community structure and the metabolic pathways/activities (shown for gut microbiome and pelagic bacterial communities). It has been shown to:● Induce profound changes in bacterial lipid profiles ● Disturb bacterial energy metabolism pathways | |
| By-products:hexachlorobenzene (HCB), polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans (PCDD/PCDF), Polycyclic aromatic hydrocarbons (PAHs) | ● Because they are semi-volatile, POPs are transported over long distances in the atmosphere.● Transfer to plants and Bioaccumulation. | ● Disruption in protein export● Induction of bacterial membrane biogenesis● Induction of stress response pathways● Induction of defense of DNA damage | |
| 2. Low to medium persistence organic products4 | |||
| Polydiméthylsiloxane (PDMS),Linear alkylbenzene sulphonates (LAS), phtalates and bisphenols | Organic fertilization (SS, MSW, composts digestates) | Limited data available on the fate and occurrence of low to medium persistence organic products.Half-life: few days to few years (variable according to the chemical). | Variable ecotoxicological impacts on soil organisms, according to the chemical. Limited data available.For antibiotics: exert a selection pressure on soil microorganisms, conferring antibiotic resistance. Co-exposure to metals, PAHs and biocides increase the appearance of new resistant microorganisms. Antibiotic residues can adversely affect microbial processes in the environment (e.g. nutrient cycling and pollutant degradation). |
| Pharmaceuticals and personal care products (antibiotics,antidepressants, endocrine disruptors, fragrances, amongst others) | Organic fertilization (SS, livestock manure, composts, digestates) | ● Transformation/degradation through biodegradation, photodegradation and hydrolysis (principally driven by enzymatic transformations conducted by microorganisms)● Soil adsorption: main physicochemical mechanism that prevents leaching or runoff to some extent. Adsorption depends on the | |
| Some pesticides | Organic fertilization (SS, green manure and crop residues,MSW, composts, digestates) | chemical, soil properties (including pH, organic matter content, and the concentration and type of divalent cations present), influence of temperature and humidity● Transport to surface and groundwaters (leaching and runoff). Dissolved organic matter increase their mobility.● Transfer to plants | |
| “Eco-friendly” herbicides5 | |||
| β-triketone herbicides: sulcotrione, mesotrione and tembotrione | Crop protection: weed management | Low mobility in soils. Half-life time of 4 to 144 days depending on soil properties. | No effects on soil microbial diversity and abundance at agronomical dose but some molecule-, dose- and strain-dependent effects at the population level. |
| Pelargonic acid | Very high to low mobility in soil. Half-life time of 1.6 days. | Ecotoxicological effects on soil microbial communities have not been studied yet. | |
| Simple organic acids: acetic acid | Very high mobility in soil. Half-life time of 0.85 to 1.23 days. | No significant effects on the structure and the diversity of soil microbial communities. | |
| Biopesticides6 | |||
| Bacillus thuringiensis | Crop protection: microbial pesticides | Efficient degradation of Bt proteins in soil. Lack of data concerning the toxicity of the accumulation of some Bt endotoxins in soils. | Limited impact on microbial community structure and microbial diversity in soil. |
| Trichoderma | No information available. | Some studies show an impact of volatiles, toxins and antibiotics produced by Trichoderma on soil microbiome. | |
| Pseudomonas | No information available. | Various effects observed, from no prominent alteration of bacterial communities to substantial shift within microbial communities (sometimes suggested as an indirect mode of action). | |
| Spinosad (Saccharopolyspora spinosa) | Relatively fast dissipation of spinosad in soil—Half-life between 1.11 and 2.21 days7 | Effects on soil enzymatic activities are recorded at high doses or in the short term after application but no negative effects in the long term at the recommended doses of application. | |
| Entomopathogenic fungi | No information available. | No or limited adverse effects recorded on soil microbial communities. | |
| Entomopathogenic viruses | No information available. | The little studies available tend to show low ecotoxicological risk. | |
| Azadirachtin | Crop protection: Botanical pesticides | Low mobility in soil due to its oily composition. No consensus in the literature on its half-life (from a few hours to 8–10 days). Formulated products can have a half-life up to 26 days.8 | Studies report a toxicity on certain soil microbial groups, somewhat comparable to that observed under the effect of chemical pesticides. |
| Pyrethroids | Soil bacterial and fungal strains are able to degrade pyrethroids into non-toxic compounds through hydrolysis of ester bond by enzyme esterase/carboxyl esterase. | No observed negative impact to soil microbial community. | |
| Essential oils | Essential oils are known to be easily degraded (mainly by oxidation). | Effects mostly unknown and poorly described. | |
| Elicitors, pheromones, allelochemicals, double stranded RNA (dsRNA)-based pesticides and pesticidal substances containing added genetic material | Crop protection: Biochemical pesticides, semiochemi-cals and plant incorporated protectants | No information available | Effects mostly unknown and poorly described but mode of action suggest limited off-target toxicity effects. |
| Nanopesticides | Crop protection: Nanopesticides | Few studies available on the behavior in soils. Behavior is depending on the nature of the nanoparticles and of the inorganic nanocarriers. | Some studies tend to show a microbial toxicity of the inorganic nanocarriers. |
| Mineral pesticides | |||
| Copper | Crop protection: mineral pesticide | Mobility, bioavailability and toxicity differ according to the chemical speciation (free ionic, complexed, precipitated, oxidation state).No degradation possible. Regular application leads to an accumulation in the long term. Please also refer to the heavy metal section. | Negative effects on soil microbial biomass and biodiversity. Please also refer to the heavy metal section. |
| Microplastics9 | |||
| Coming from the breakdown of biodegradable plastics: starch-based, polylactide-based or polyhydroxyalkanoate-based | Crop protection: weed management (mulching) | Few studies available: slight degradation of polylactide-based plastics after 12 months in field conditions10 | Mainly studied in aquatic environments. Soil studies focus on their biodegradation, not on their ecotoxicological impact. |
| Contaminant/substance . | Agroecological practice involved . | Behavior of the contaminant/substance in the soil . | Ecotoxicological impact on soil microorganisms . |
|---|---|---|---|
| Heavy metals1 | |||
| As, Cd, Cr, Hg, Ni, Pb, Se | Organic fertilization (SS, MSW, composts and digestates) | Mobility, bioavailability and toxicity differ according to the chemical speciation (free ionic, complexed, precipitated, oxidation state). | Above a certain threshold, HM are toxic for microorganisms. HM toxicity act primarily at a cellular level, due to the following characteristics: |
| Cu, Zn | Organic fertilization (livestock manure, SS, MSW, composts and digestates) | No degradation possible. Regular application leads to an accumulation in the long term (often significant for Cu and Zn). A part of the total metal concentration in soil is irreversibly linked to or sequestered by the soil matrix.Low solubility (for consequent low lixiviation). HM concentration in a soil solution is influenced mainly by the soil pH, but also by redox potential, clay content and presence of soil organic matter (SOM). Only a fraction of HMs in solution are bioavailable (plants and other biota). It is generally assumed that the free ion is the chemical species which is taken up and causes toxicity when present in excess. Other chemical forms or forms chelated by organic molecules cannot be taken up directly. | • high affinity for negatively charged cellular groups, such as sulfhydryls, phosphates and hydroxyls;• generation of reactive oxygen species, causing oxidative stress;• competition with essential ions acquisition;• disturbance of cellular ion balance and osmotic regulation. A summary of the literature on metal toxicity to soil microbial processes and populations reveal an enormous variability in the data. Two factors contribute to the discrepancies between studies: (1) factors which modify the toxicity/bioavailability of the metals and (2) differences in sensitivity of the microorganism(s) or microbial process(es). Heavy metal concentrations in soils at around current European Union limits have been shown to decrease total microbial biomass, diversity and activity. While most studies focus on the total community, more subtle changes in microbial community structure can also be observed, such as alterations in relative abundance of particular microbial groups or species of agronomical importance. For example, nitrogen-fixing rhizobia are sensitive to metal toxicity. Long-term heavy metal contamination in soil is a selection pressure which can promote bacterial species able to develop HM resistance. |
| Biological contaminants2 | |||
| Human and animal pathogens (prions, viruses, bacteria, protozoa, helminths) | Organic fertilization (SS, livestock manure, slaughterhouse waste) | Survival times variable, from a few days to multiple years (e.g. <35 to 231 days for Salmonella; from <2 weeks to >6 months for enteroviruses). Persistence in the soil is favored by low temperature, high humidity, low light intensity and neutral pH; and by a deep application of OWP. | Interaction with other organisms (predation, competition, antagonism). Poorly characterized. |
| Antibiotic-resistant bacteria (ARB) and Antibiotic resistance genes (ARG) | Organic fertilization (SS, livestock manure, digestates) | The fate of ARBs and ARGs from OWP in soil and their contribution to the overall problem of antibiotic resistance are poorly characterized. Soil bacteria inherently contain ARGs, which makes studies very difficult. Environmental microorganisms are hypothesized to be the main source of antibiotics as well as the concomitant antibiotic resistance.The large numbers of resistant bacteria entering the soil through OWP are likely to compete with other bacteria or survive in the soil environment. | OWP application can increase antibiotic resistance in the soil microflora through several effects:● horizontal gene transfer (HGT) of fecal-derived ARGs to native soil microorganisms. HGT mainly includes three pathways mediated by mobile genetic elements, namely extracellular DNA-mediated transformation, plasmid-mediated conjugation, and phage-mediated transduction. |
| ● mutation in the native soil microorganisms through the selection pressure exerted by the residues of antibiotics, metals, PAHs and biocides, causing the appearance of new resistant microorganisms (see section on antibiotics).Although several studies supporting the two concepts have been published, available data are still inconclusive and do not provide direct evidence that links specific factors to individual ARGs. | |||
| Trace organic contaminants | |||
| 1. Persistent organic pollutants (POP)3 | |||
| Organochlorine pesticides:aldrin, chlordane, DDT, dieldrin, endrin, heptachlor, hexachlorobenzene, mirex, toxaphene | Organic fertilization (SS, green manure, crop residues, food residues, MSW,composts, digestates) | ● Persistent, risk of long-term accumulation in soils. Half-life: years or decades in soil/sediment.Fates of the pollutants:● Dissipation from soils by biodegradation and photodegradation (low degradability). | Hydrophobic and highly lipid-soluble chemicals. They accumulate in the membrane bilayer between the acyl chains of fatty acids and increase membrane fluidity. Few studies on the impact of POP on soil microorganisms, even less data on the impact of degradation metabolites. |
| Industrial chemicals:Hexachlorobenzene, polychlorinated biphenyls (PCBs), Polybrominated diphenyl ethers (PBDE), perfluorinated compound (PFC) | Biological decomposition is the most important and effective way to remove these compounds from the environment.● Binding to soil solid phases, mainly to SOM but also to the mineral fraction. Pollutant bioavailability decreases with increasing soil-pollutant contact time (= ageing process). ● Transfer to water (leaching to groundwater and surface water). | POP exposure might alter the microbial community structure and the metabolic pathways/activities (shown for gut microbiome and pelagic bacterial communities). It has been shown to:● Induce profound changes in bacterial lipid profiles ● Disturb bacterial energy metabolism pathways | |
| By-products:hexachlorobenzene (HCB), polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans (PCDD/PCDF), Polycyclic aromatic hydrocarbons (PAHs) | ● Because they are semi-volatile, POPs are transported over long distances in the atmosphere.● Transfer to plants and Bioaccumulation. | ● Disruption in protein export● Induction of bacterial membrane biogenesis● Induction of stress response pathways● Induction of defense of DNA damage | |
| 2. Low to medium persistence organic products4 | |||
| Polydiméthylsiloxane (PDMS),Linear alkylbenzene sulphonates (LAS), phtalates and bisphenols | Organic fertilization (SS, MSW, composts digestates) | Limited data available on the fate and occurrence of low to medium persistence organic products.Half-life: few days to few years (variable according to the chemical). | Variable ecotoxicological impacts on soil organisms, according to the chemical. Limited data available.For antibiotics: exert a selection pressure on soil microorganisms, conferring antibiotic resistance. Co-exposure to metals, PAHs and biocides increase the appearance of new resistant microorganisms. Antibiotic residues can adversely affect microbial processes in the environment (e.g. nutrient cycling and pollutant degradation). |
| Pharmaceuticals and personal care products (antibiotics,antidepressants, endocrine disruptors, fragrances, amongst others) | Organic fertilization (SS, livestock manure, composts, digestates) | ● Transformation/degradation through biodegradation, photodegradation and hydrolysis (principally driven by enzymatic transformations conducted by microorganisms)● Soil adsorption: main physicochemical mechanism that prevents leaching or runoff to some extent. Adsorption depends on the | |
| Some pesticides | Organic fertilization (SS, green manure and crop residues,MSW, composts, digestates) | chemical, soil properties (including pH, organic matter content, and the concentration and type of divalent cations present), influence of temperature and humidity● Transport to surface and groundwaters (leaching and runoff). Dissolved organic matter increase their mobility.● Transfer to plants | |
| “Eco-friendly” herbicides5 | |||
| β-triketone herbicides: sulcotrione, mesotrione and tembotrione | Crop protection: weed management | Low mobility in soils. Half-life time of 4 to 144 days depending on soil properties. | No effects on soil microbial diversity and abundance at agronomical dose but some molecule-, dose- and strain-dependent effects at the population level. |
| Pelargonic acid | Very high to low mobility in soil. Half-life time of 1.6 days. | Ecotoxicological effects on soil microbial communities have not been studied yet. | |
| Simple organic acids: acetic acid | Very high mobility in soil. Half-life time of 0.85 to 1.23 days. | No significant effects on the structure and the diversity of soil microbial communities. | |
| Biopesticides6 | |||
| Bacillus thuringiensis | Crop protection: microbial pesticides | Efficient degradation of Bt proteins in soil. Lack of data concerning the toxicity of the accumulation of some Bt endotoxins in soils. | Limited impact on microbial community structure and microbial diversity in soil. |
| Trichoderma | No information available. | Some studies show an impact of volatiles, toxins and antibiotics produced by Trichoderma on soil microbiome. | |
| Pseudomonas | No information available. | Various effects observed, from no prominent alteration of bacterial communities to substantial shift within microbial communities (sometimes suggested as an indirect mode of action). | |
| Spinosad (Saccharopolyspora spinosa) | Relatively fast dissipation of spinosad in soil—Half-life between 1.11 and 2.21 days7 | Effects on soil enzymatic activities are recorded at high doses or in the short term after application but no negative effects in the long term at the recommended doses of application. | |
| Entomopathogenic fungi | No information available. | No or limited adverse effects recorded on soil microbial communities. | |
| Entomopathogenic viruses | No information available. | The little studies available tend to show low ecotoxicological risk. | |
| Azadirachtin | Crop protection: Botanical pesticides | Low mobility in soil due to its oily composition. No consensus in the literature on its half-life (from a few hours to 8–10 days). Formulated products can have a half-life up to 26 days.8 | Studies report a toxicity on certain soil microbial groups, somewhat comparable to that observed under the effect of chemical pesticides. |
| Pyrethroids | Soil bacterial and fungal strains are able to degrade pyrethroids into non-toxic compounds through hydrolysis of ester bond by enzyme esterase/carboxyl esterase. | No observed negative impact to soil microbial community. | |
| Essential oils | Essential oils are known to be easily degraded (mainly by oxidation). | Effects mostly unknown and poorly described. | |
| Elicitors, pheromones, allelochemicals, double stranded RNA (dsRNA)-based pesticides and pesticidal substances containing added genetic material | Crop protection: Biochemical pesticides, semiochemi-cals and plant incorporated protectants | No information available | Effects mostly unknown and poorly described but mode of action suggest limited off-target toxicity effects. |
| Nanopesticides | Crop protection: Nanopesticides | Few studies available on the behavior in soils. Behavior is depending on the nature of the nanoparticles and of the inorganic nanocarriers. | Some studies tend to show a microbial toxicity of the inorganic nanocarriers. |
| Mineral pesticides | |||
| Copper | Crop protection: mineral pesticide | Mobility, bioavailability and toxicity differ according to the chemical speciation (free ionic, complexed, precipitated, oxidation state).No degradation possible. Regular application leads to an accumulation in the long term. Please also refer to the heavy metal section. | Negative effects on soil microbial biomass and biodiversity. Please also refer to the heavy metal section. |
| Microplastics9 | |||
| Coming from the breakdown of biodegradable plastics: starch-based, polylactide-based or polyhydroxyalkanoate-based | Crop protection: weed management (mulching) | Few studies available: slight degradation of polylactide-based plastics after 12 months in field conditions10 | Mainly studied in aquatic environments. Soil studies focus on their biodegradation, not on their ecotoxicological impact. |
Acronyms: OWP—organic waste product; SS—sewage sludge; MSW—municipal solid waste; SOM—soil organic matter; HM—heavy metal; ARB—Antibiotic-resistant bacteria; ARG—antibiotic resistance genes; HGT—horizontal gene transfer; MGEs—mobile genetic elements; PAHs—poly-aromatic hydrocarbons; POP—persistent organic pollutants; DDT –; PCB—polychlorinated biphenyls; PBDE—Polybrominated diphenyl ethers; PFC—perfluorinated compound; HCB—hexachlorobenzene; PCDD/PCDF—polychlorinated dibenzo-p-dioxins and furans; PAHs—Polycyclic aromatic hydrocarbons; PDMS—Polydiméthylsiloxane; LAS—Linear alkylbenzene sulphonates.
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