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Yao, H.; , . Plasmid-Mediated Transfer of Antibiotic Resistance Genes in Soil. Encyclopedia. Available online: https://encyclopedia.pub/entry/22245 (accessed on 27 July 2024).
Yao H,  . Plasmid-Mediated Transfer of Antibiotic Resistance Genes in Soil. Encyclopedia. Available at: https://encyclopedia.pub/entry/22245. Accessed July 27, 2024.
Yao, Huaiying, . "Plasmid-Mediated Transfer of Antibiotic Resistance Genes in Soil" Encyclopedia, https://encyclopedia.pub/entry/22245 (accessed July 27, 2024).
Yao, H., & , . (2022, April 25). Plasmid-Mediated Transfer of Antibiotic Resistance Genes in Soil. In Encyclopedia. https://encyclopedia.pub/entry/22245
Yao, Huaiying and . "Plasmid-Mediated Transfer of Antibiotic Resistance Genes in Soil." Encyclopedia. Web. 25 April, 2022.
Plasmid-Mediated Transfer of Antibiotic Resistance Genes in Soil
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This entry is adapted from the peer-reviewed paper 10.3390/antibiotics11040525

Due to selective pressure from the widespread use of antibiotics, antibiotic resistance genes (ARGs) are found in human hosts, plants, and animals and virtually all natural environments. Their migration and transmission in different environmental media are often more harmful than antibiotics themselves. ARGs mainly move between different microorganisms through a variety of mobile genetic elements (MGEs), such as plasmids and phages. The soil environment is regarded as the most microbially active biosphere on the Earth’s surface and is closely related to human activities. With the increase in human activity, soils are becoming increasingly contaminated with antibiotics and ARGs. Soil plasmids play an important role in this process.

plasmid antibiotic resistance genes gene transfer soil

1. Introduction

Antibiotics promote healthcare and animal husbandry by inhibiting the growth and reproduction of microorganisms and by treating and preventing bacterial infections. However, the chronic use of large amounts of antibiotics can create selection pressures that cause resistant bacteria to develop resistance genes (ARGs). ARGs are widespread in clinical settings, human hosts, plants, animals, and in virtually all natural environments [1][2][3][4].

2. Plasmid-Mediated Transfer of Antibiotic Resistance Genes

An MGE identified in a bacterial strain in 2003 was one of the first indicators of the existence of antibiotic resistance [5]. Since then, bacterial strains with resistance to ampicillin, chloramphenicol, erythromycin, streptomycin and tetracycline have been found in frozen soil samples [6][7]. Antibiotic resistance genes are widely present in a variety of environments, whether natural without human intervention or heavily contaminated with antibiotics. The well-known dominant phyla in soil are Proteobacteria, Acidobacteria, Actinobacteria, Verrucomicrobia, Bacteroidetes, Chloroflexi, Gemmatimonadetes and Firmicutes [8]. A recent study has found that drug-resistant bacteria such as Actinobacterium, Bacillus, Xanthobacteraceae and Geobacter species, are common latent hosts for multidrug resistance genes (MRGs) [9]. Polymyxins have therefore been repurposed for infections caused by multidrug-resistant Gram-negative bacteria [10]. Colistin possesses antibacterial activity against members of the Enterobacteriaceae family, including Klebsiella species, Escherichia coli (E. coli), Shigella species, Enterobacter species, and Salmonella species [11]. The main pathway through which bacteria obtain external ARGs and develop resistance is HGT. HGT mainly occurs through transformation, splicing and transduction [12]. The horizontal transmission of ARGs among bacteria is primarily driven by bacterial plasmids, which facilitate the transfer of resistance genes. ARGs such as those encoding broad-spectrum β-lactamases (ESBLs) (e.g., CTX-M), carbapenemases (e.g., KPC, NDM, and OXA-58) [13], and mucilage resistance (e.g., MCR-1) [14], are prevalent in Gram-negative bacteria. Several Gram-negative bacteria, such as Pseudomonas, Acinetobacter and Stenotrophomonas species isolated by Kudinova et al. [15] have simultaneously developed resistance to multiple antibiotics. Plasmids were also detected in some dominant Gram-positive bacteria, such as Bacillus, Microbacteriaceae, and Methanobacterium species, suggesting that ARGs are highly likely to be transferred in both G− and G+ bacteria [16].

2.1. Presence of ARGs in the Natural Environment

ARGs are ubiquitous in the natural environment. On the one hand, they originate from the production of antibiotics or their derivatives by microorganisms in the soil. On the other hand, biological interactions between bacteria and other microorganisms, such as antagonistic interactions between fungi and bacteria, affect bacterial community composition and the abundance of ARGs directly [17].
ARGs have been found to be present in most terrestrial ecosystems on Earth with no or limited anthropogenic disturbance, including seabed, primeval forests, and even polar regions. Inka et al. [18] identified three sulfonamide-resistant synthases in beech and pine forest soils with different taxonomic origins. This suggests that sulfonamide antibiotic resistance occurs naturally in bacterial communities in forest soil. Song et al. [19] detected a large number of ARGs resistant to modern antibiotics in soils of primary forests in China with very low levels of antibiotics in the soil, indicating that forest soils are highly likely to be a source of potential resistance traits. The low abundance of MGEs in forest soils and their nonpositive association with ARGs reflect the minimal likelihood of HGT in forest soil environments. Kim et al. [20] detected a total of 70 independent ARGs related to 18 antibiotics in the Arctic permafrost zone using a macrogenomic approach. The genomes of permafrost and clinical strains contain similar mobile elements and prophages [21], suggesting that strains in the natural environment exhibit an extremely strong horizontal transfer of genetic material. Permafrost strains, although related to various clinical isolates, do not form separate clusters in the phylogenetic tree. Belov et al. [22] analysed the macrogenomes of perennial permafrost and sediments; Proteobacteria, Firmicutes, Chloroflexi, Acidobacteria, Actinobacteria and Bacteroidetes were the most common taxa, and the bacterial abundance was high in the microbial communities of the Canadian Arctic. Paun et al. [23] obtained and identified the first strains of bacteria from 13,000-year-old ice cores that accumulated in caves over many years since the Late Ice Age. Among the isolated bacteria, Gram-negative bacteria were more resistant than Gram-positive bacteria. Over 50% of the strains showed high resistance to 17 antibiotics. Some of these strains can inhibit the growth of typically clinically resistant strains, revealing a metabolic profile with potential applications. Mootapally et al. [24] evaluated antibiotic resistance groups in pelagic sediments and found that the dominant genes carA, macB, bcrA, taeA, srmB, tetA, oleC and sav1866 were mainly resistant to macrolides, glycopeptides, and tetracyclines. Nathani et al. [25] studied a pelagic sediment microbiome for marine resistance groups and their corresponding bacterial communities. A total of 2354 unique resistance genes were identified in a comparison with samples from the open Arabian Sea, showing the presence of tlrC genes in addition to carA, macB, bcrA, taeA, srmB, tetA, sav1866 and oleC. Moreover, Proteobacteria, Actinobacteria and Bacteroidetes were the predominant phyla in the deep-sea sediments.

2.2. Prevalence and Spread of ARGs under Antibiotic Selection Pressure

2.2.1. Transfer of ARGs from Severely Contaminated Sites

Antibiotics have been extensively used in healthcare and farm animal husbandry to treat or prevent bacterial infections and promote animal husbandry. However, the overuse of antibiotics has led to antibiotic residues in clinical settings and in soil on farms, sewage treatment plants, and other sites. These residues are potentially toxic to organisms, resulting in the enrichment of ARGs, making it an emerging and persistent environmental pollutant [26]. Hospitals consume large amounts of antibiotics, especially β-lactams, quinolones and methotrexate [27]. However, their residues in hospital wastewater are unknown. The efficiency of antibiotic removal from hospital wastewater treatment processes was reported to be 74–81% [28]. Among various types of antibiotics, the removal efficiency for β-lactam antibiotics was high (84.4–99.5%) [29], while ofloxacin was more difficult to remove, and these residues were detected in wastewater at a higher rate than other types of antibiotics [30]. The improper disposal of antibiotics and medical waste in hospitals can contribute to the introduction of antibiotic residues in soil and underground water.
Most of the antibiotics administered to people in hospitals are used in homes and end up in domestic wastewater. Thus, municipal wastewater treatment plants (WWTPs) are one of the major sources of antibiotic-resistant bacteria (ARB) and ARGs released into the environment and have become a hotspot for HGT. Osinska et al. [31] showed a high potential for bacterially mediated HGT in wastewater environments. Single ARB are consistently associated with multiple ARGs. Once ARB successfully enter a WWTP, ARGs can be transmitted between the bacteria in the endogenous microbial community and the bacteria passing through the WWTP. Guo et al. [32] found that MGEs, including plasmids, transposons, integrons (intI1) and insertion sequences (e.g., ISSsp4, ISMsa21 and ISMba16) were abundant in sludge samples. Additionally, a network analysis indicated that some environmental bacteria might be potential hosts for multiple ARGs. Isolates resistant to β-lactams most frequently carried the blaTEM and blaOXA genes. The genomes that encode resistance to tetracyclines were most commonly tetA, tetB and tetK, while the qnrS gene was found in isolates resistant to fluoroquinolones [33]. Munir et al. [34] showed that the concentration of ARB decreased by several orders of magnitude compared to that in the original influent water, but the concentration of ARGs remained quite similar in pre- and post-disinfection effluents. There was no significant reduction in the abundance of MGEs in the effluent water either [35]. Compared with those in the original influent, most of the ARGs were effectively removed after wastewater treatment [36][37]. The specific environmental conditions in WWTPs offer a selective advantage for HGT of ARGs and ARB in bacterial communities.
The plasmid-mediated transfer of ARGs poses a grave danger to global public health. The use of amoxicillin on farms has made the poultry farm environment an essential reservoir of blaNDM-carrying bacteria [38][39]. Additionally, blaNDM contamination was also detected in the farm environment (soil, sewage, feed, dust) in commercial goose farms [40]. Moreover, IncX3- and pM2-1-type plasmids contribute to the prevalence and spread of ARGs in different bacteria. Mohsin et al. [41] detected IncFII- and IncQ-type plasmids carrying the tet (X4) gene in four different sources of E. coli (poultry, chicken, wild birds and slaughterhouse wastewater). In another study, all mcr-1-positive E. coli strains isolated from poultry were multidrug resistant, with up to 88.24% of the isolates containing blaTEM genes and tetracycline (tetA and tetB) and sulfonamide (sulI, sulII and sulIII) resistance genes [42]. The antibiotics commonly used in aquaculture are aminoglycosides, β-lactams, sulfonamides and tetracyclines [43]. Residual antibiotics leached from fish feed are often present in effluents. The levels of ARGs in fish farm effluents were found to be significantly higher than those in the surrounding water environment, and most of the ARGs were present on plasmids [44].

2.2.2. Human Activities Affect the Transfer of ARGs in the Environment

The major dominant groups in agricultural sediments are Actinobacteria, Chlamydomonas and Firmicutes [45]. Wendi et al. [46] detected no antibiotic-associated resistance genes in aquaculture farm sediments used for farming, suggesting that natural resistance bodies may be present in farm sediments. However, the application of organic fertilizers to agricultural soils greatly contributes to resistance gene contamination. ARGs carried by bacteria in organic fertilizers and in antibiotics themselves have caused a significant increase in the abundance of resistance genes in fertilized soils [47][48]. Pu et al. [49] isolated two transferable amino-glycoside resistance plasmids from pig or chicken manure, namely, pRKZ3 and pKANJ7. As is known, pRKZ3 is a nonconjugated IncQ plasmid with arr-3 and aacA resistance-conferring genes that encode plasmid replication and stabilization (repA, repB and repC) and mobilization (mob) functions. Furthermore, pKANJ7 is a conjugated IncQ plasmid encoding the T4SS-type IncX plasmid. Wang et al. [50] analysed the contamination of soil with ARGs in agricultural soils with long-term application of organic fertilizers. There is a high abundance of macrolide- and quinolone-resistant bacteria and drug resistance genes in fertilized soils in contrast to unfertilized soils. In addition, the abundances of intI and intII were significantly correlated with the abundances of qnrS and ermB, respectively. In general, intI is located on the Tn21 transposon, and intII is located on the Tn7 transposon, which has certain ramifications. Thus, this gene can be transmitted among bacteria via transposons. The intl1 and intl2 genes are frequently found in manure-treated agricultural soils and greenhouse soils. The broad availability of integrase genes can facilitate gene transfer, thereby increasing the persistence and accumulation of ARGs [51][52]. Zhao et al. [53] also found that the total relative abundance of the intI gene in manure-amended soil positively correlated with those of tetW, tetO, sulI and sulII. However, it has also been shown that the production of drug-resistant bacteria is negatively correlated with the dose of antibiotic exposure. This may be due to high antibiotic concentrations affecting the community structure and function of soil microorganisms. Some developed countries have applied sludge to agricultural production to reduce production costs [54]. The direct application of sludge also leads to the introduction of ARGs in agricultural systems. Markowicz [55] isolated 16 resistance genes and four integrator classes in sewage sludge containing plasmids with extreme resistance to β-lactams as well as tetracyclines. Iwu et al. [56] isolated multidrug-resistant E. coli containing plasmids harbouring AmpC and ESBLS in irrigation water and agricultural soil samples, as well as a plasmid-harbouring multigene sequence.
Talukder et al. [57] isolated multidrug-resistant P. aeruginosa from soils from industrial areas, and 60% of MARs carried 1000–2000 bp double plasmids, which suggests the occurrence of plasmid-mediated transfer of ARGs in industrial soils. This is most likely due to the targeted selection of resistant bacteria by certain concentrations of antibiotic residues. The horizontal transfer of ARGs in sediments is rarely reported compared to that in agricultural soils, but sediments are considered to be the main vector for the multiplication and translocation of antibiotics and ARGs [58]. Chen et al. [59] found that in the Pearl River basin, the intI and sul genes were dynamically transported between water and sediment, and intI was closely associated with some specific genes in the sediment [60]. Yang et al. [58] detected a higher variety and relative abundance of genes in the sediments of East Dongting Lake than in Hong Lake. Another study found that the most common ARGs in the coastal sediments of the East China Sea in China were sulfonamide resistance genes [61].

2.3. Transfer of ARGs under Other Selection Pressures

The co-selection of ARGs by heavy metals and antibiotics also increases ARG contamination in soil [62][63]. Xu et al. [64] reported correlations between heavy metals and some ARG subtypes and observed positive correlations between Zn and the intI gene, with Cu and Zn having stronger positive correlations with ARGs than antibiotics. This implies that metals may play an important role in increasing the integration frequency of ARGs in various bacteria in agricultural soils. Both copper oxide nanoparticles and copper ions (Cu2+) can facilitate the conjugative transfer of multiple resistance genes [65]. Heavy metal exposure accelerates the plasmid-mediated conjugative transfer of ARGs. Although nanomaterials can remove heavy metals by adsorption, Cd2+ and high concentrations of Fe2O3 nanoparticles significantly increase the frequency of the conjugative transfer of RP4 plasmids [66]. High concentrations of metals in soil affect the composition and function of soil bacterial communities. Klumper et al. [67] demonstrated for the first time that metal stress can modulate the tolerance of different soil bacteria to IncP plasmids. Soil minerals also affect the rate of the conjugative transfer of plasmids carrying ARGs, and the effect of different types of soil minerals on the rate of conjugative transfer varies [68]. Herbicides can cause changes in the susceptibility of certain strains to antibiotics and can also accelerate the HGT of ARGs in soil bacteria [69]. It has been shown that herbicide-use has a weak effect on the abundance and composition of soil microbial communities but can increase the abundance of corresponding ARGs and MGEs as well as the coupling frequency of plasmids [70].

3. Phage-Mediated Transfer of Antibiotic Resistance Genes

Phages can transfer genes by specific or universal transduction. Specific transduction involves the transfer of only a few specific genes, whereas universal transduction can move any segment of the bacterial genome. Another mechanism that is similar to transduction but different in nature is lysogenic conversion. When a mild phage infects a host bacterium, the phage DNA integrates with the host chromosome, causing the host to become lysogenic and leading it to acquire certain characteristic traits. Certain phenotypes of the host can also be altered by lysogenic transformation, leading to the acquisition or loss of a trait. Among several mechanisms of DNA transfer, lysogenic transformation caused by phage is more dominant and efficient [71]. Once phage-transferred ARGs reach the recipient bacteria by either mechanism, the survival of ARGs depends on the ability of the sequence to integrate into the bacterial genome. If ARGs are specifically transduced by phage transfer, an intact phage genome including the integrase gene will increase the chances of successful integration. If the gene is transduced by universal transduction, then the successful transfer of ARGs requires the recombination of the exogenous gene into the host chromosome. Thus, the genes encoding recombinase and integrase will determine the efficiency of the acquisition of ARGs by the recipient bacterium [72]. The presence of phages in aqueous environments and their potential for the HGT of ARGs have been widely demonstrated [73], but has been less studied in soil environments. Blance [74] et al. isolated phage particles carrying five ARGs (blaTEM, blaCTX-M-1, blaCTX-M-9, sul1 and tetW) from seawater. Another study found that fluoroquinolone exposure of multidrug-resistant Salmonella induced its phage-mediated gene transfer [75]. However, several studies have found phages carrying ARGs in the faces of poultry, cattle, pigs and even humans [76][77]. In manure-amened agricultural soils, this undoubtedly gives rise to a significant risk of phage-mediated transfer of ARGs.

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HuaiYing Yao
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