Heavy Metal Contamination and the Rise of Antibiotic Resistance

Overview

Antibiotic resistance has escalated into a global health crisis, traditionally attributed to the selective pressure of antibiotic misuse. However, mounting evidence indicates that environmental pollution – particularly heavy metal contamination – is also propelling the proliferation of antimicrobial resistance (AMR).^[1][2] Heavy metals such as lead (Pb), mercury (Hg), arsenic (As), chromium (Cr), cadmium (Cd), and nickel (Ni) are non-degradable toxic elements that persist in soils and waters, exerting long-term selective pressure on microbial communities.^[3][4] Unlike antibiotics (which can degrade over time), heavy metals can accumulate at concentrations orders of magnitude higher than typical antibiotic levels, creating hotspots for resistance development.^[5] Bacteria exposed to heavy metals often develop metal resistance genes (MRGs), and these may be genetically or mechanistically linked to antibiotic resistance genes (ARGs). This phenomenon of co-selection means heavy metals can enrich bacterial populations that are multi-drug resistant, even in the absence of antibiotic exposure.^[6][7]

From a One Health perspective, heavy metal-induced antibiotic resistance spans environmental, agricultural, industrial, and clinical domains. Environmental reservoirs (soil, sediments, water) contaminated with metals show higher ARG abundance.^[8] In agriculture, metal-laden fertilizers and animal feed supplements (e.g. copper and zinc) select for resistant microbiota in soil and livestock gut.^[9][10] Industrial activities and wastewater release metals that enrich multidrug-resistant bacteria in effluents and downstream ecosystems.^[11] Even clinical and urban settings are not exempt: for example, wartime environmental damage disperses metals (from shrapnel, infrastructure) that co-select for drug-resistant pathogens in wounds.^[12] Heavy metal resistance is an ancient trait – predating modern antibiotics – and may have set the stage for contemporary ARG evolution.^[13] Notably, nickel (Ni) contamination has drawn special attention for its co-selective effects, and certain bacteria exhibit glyoxalase-positive phenotypes that enhance survival under metal stress. Glyoxalases are enzymes that detoxify methylglyoxal, a toxic metabolic byproduct; their activity (often Ni-dependent) may fortify bacteria against both metal toxicity and other stresses. In this review, we integrate recent findings on how heavy metals drive antibiotic resistance across multiple contexts, emphasizing mechanistic insights – from efflux pumps and co-resistance plasmids to stress responses (e.g. glyoxalase-mediated) and horizontal gene transfer. Key molecular mechanisms and case studies are summarized in tables for clarity.

Environmental and Industrial Perspectives on Metal-Driven AMR

Sources and Scope of Contamination: Heavy metals enter the environment through natural processes (geothermal activity, mineral weathering) and myriad anthropogenic sources.^[14] Industrial mining and smelting, energy production, metal plating, and improper waste disposal have led to widespread contamination of soils, sediments, and waterways with metals like As, Cd, Cr, Cu, Pb, Hg, Ni, and Zn.[15]^[x] Agricultural runoff and sewage sludge can further introduce metals (e.g., from fertilizers, manure, or wastewater) into ecosystems.^[16] Unlike organic pollutants, metals do not biodegrade; they persist and accumulate, maintaining continuous pressure on local microbes.^[17][18] This sustained exposure has selected for metal-tolerant bacteria that frequently also harbor antibiotic resistance. Indeed, a global survey found that many heavy-metal-polluted environments contain higher levels of ARGs than unpolluted sites, even in the absence of elevated antibiotics.^[19][20] Heavy metals thereby act as chronic selectors of multidrug resistance in the environment.

Evidence from Polluted Environments: Numerous empirical studies link metal pollution to antibiotic resistance. For example, river sediments impacted by historic mining and industry (e.g., in the UK’s River Tyne catchment) showed significantly elevated ARG abundances correlating with high sediment concentrations of Pb, Zn, Ni, and other metals.^[21] In these sediments, genes conferring metal and antibiotic resistance co-occurred, and bacterial communities were dominated by metal-tolerant groups (Firmicutes, Bacteroidota) known to carry integron-based gene cassettes with both MRGs and ARGs.^[22] A comparative study of polluted Indian rivers similarly found that sites with higher heavy metal levels had markedly more ARGs, underscoring metal pollution as a driver of AMR on a global scale.^[23] Intriguingly, certain metal combinations have synergistic effects: one study noted that cobalt plus nickel together, or a trio of Co, Zn, and Cd, produced the strongest enrichment of antibiotic-resistant bacteria in sediments.^[24] This suggests mixed-metal contamination can amplify co-selection pressures beyond what single metals do.

Industrial waste streams and wastewater treatment plants (WWTPs) are important nodes where heavy metals and antibiotics converge. Wastewater effluents often contain a cocktail of metals (e.g., Cu, Zn, Mn, Cd from industrial discharges) along with antibiotic residues.^[25] Even at sub-inhibitory concentrations, these metals can alter bacterial physiology in ways that promote drug resistance. Notably, heavy metals can upregulate bacterial efflux pump systems, leading to cross-resistance against antibiotics.^[26] A study of WWTP bacterial isolates showed that exposure to low-level Cu or Zn triggered increased expression of multi-drug efflux pumps, resulting in decreased susceptibility to multiple antibiotics.^[27] Similarly, metal-rich industrial effluents can select for plasmids and integrons bearing both MRGs and ARGs, which are then disseminated in downstream environments. Long-term field investigations have confirmed that metal pollution creates a reservoir of mobile resistance elements: for instance, soil chronically contaminated with heavy metals near smelters or in mining areas harbors a higher abundance of class 1 integrons (intI1) and resistance plasmids than uncontaminated soil. ^[28] These integrons facilitate the capture and spread of ARGs under heavy metal selection. In summary, environmental and industrial contamination with heavy metals establishes an ideal breeding ground for antibiotic resistance by continuously selecting co-resistant organisms and enriching gene exchange platforms (see Table 1 for examples).

Agricultural Perspective: Metals in Farming and Food Production

Heavy Metals in Agriculture: Agricultural practices have inadvertently introduced substantial heavy metal loads into the biosphere. Common examples include the supplementation of animal feed with trace metals (notably copper and zinc in swine and poultry diets to promote growth or prevent disease), the use of arsenical compounds in pastured animals (historically, e.g., roxarsone in poultry), and the presence of metals in phosphate fertilizers and pesticides.[29] Manures and slurries from intensive livestock operations often contain elevated Cu, Zn, and other metals, which are subsequently applied to fields as fertilizer. Over time, this leads to metal accumulation in agricultural soils. These metals can co-select for antibiotic resistance in both the commensal flora of animals and environmental bacteria in soil and water runoff.

Co-selection in Livestock: There is compelling evidence that in-feed metals select for multidrug-resistant bacteria in farm animals. A well-documented case is the rise of livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) in pig farms. In swine, high zinc diets have been linked to increased MRSA carriage. The genetic basis is a zinc resistance gene (czrC, conferring Zn/Cd efflux) that is co-located with the methicillin resistance determinant (mecA) on the SCCmec element of LA-MRSA.^[30] Studies in Denmark demonstrated that supplementing weanling pigs’ feed with zinc oxide significantly increased nasal MRSA colonization in the herd.^[31] All MRSA isolates from zinc-fed pigs were czrC-positive and zinc-resistant, indicating that Zn exposure had co-selected the MRSA strains.^[32] Likewise, copper supplementation in pig diets has been implicated in selecting for enterococci carrying coupled resistances. Enterococcus faecium isolates from copper-fed swine often harbor the tcrB gene (for Cu tolerance) on the same conjugative plasmid as vanA (vancomycin resistance) and erm(B) (erythromycin resistance).^[33] Thus, a single plasmid endows these strains with both heavy metal and antibiotic resistance – a textbook example of co-resistance in an agricultural setting. These plasmid-bearing enterococci can disseminate from farms to humans via the food chain or environmental pathways, raising concern that on-farm metal use contributes to clinical AMR.

Manure, Soil, and Crop Impacts: Heavy metals in animal manure also influence the resistome of agricultural soils. Land application of manure or sewage sludge containing metals has been shown to enrich soil bacteria carrying ARGs. For instance, long-term field trials in China revealed that soils amended with metal-rich swine manure had higher ARG diversity and abundance than control soils, with strong correlations between soil copper/zinc levels and tetracycline and sulfonamide resistance gene prevalence ^[34]. Even soil in the vicinity of pig farms (exposed via runoff and aerosolized dust) can acquire a co-selected resistome: one survey found co-occurrence of multiple ARGs with Zn, Cu, and Cd resistance genes in pig farm soils and hypothesized that common feed metals were a driving factor.^[35] Aquaculture is another agricultural domain of concern, heavy metal-containing antifouling agents (like copper compounds on fish farm nets) and dietary supplements can select for metal- and antibiotic-resistant Aeromonas, Vibrio, and other aquacultural pathogens, though research here is ongoing. Overall, the agricultural use of heavy metals creates a continual background selection for resistance in microbial communities associated with food production. This not only complicates efforts to reduce AMR through prudent antibiotic use but also exemplifies how environmental management (e.g., feed composition, waste handling) is integral to combating resistance.

Clinical and Public Health Perspectives

In clinical settings, direct heavy metal exposure is less common today than in the past, but heavy metal resistance still plays a role in nosocomial pathogens and public health. Historically, metals like mercury, arsenic, and silver were used as antimicrobials (e.g., mercurial skin antiseptics, arsenical therapeutics, silver nitrate in wound care). Pathogens evolved mechanisms to detoxify these metals; for example, the plasmid-encoded mer operon for mercury resistance became widespread in the mid-20th century due to mercurial disinfectant use^[36]. Even though antibiotics replaced most metal-based therapies, the legacy of those metal resistance elements persists, often now co-existing with ARGs on the same mobile elements. Modern healthcare still employs metals in limited ways, such as copper alloy surfaces (used in hospitals for their antimicrobial properties) and silver-coated medical devices. These measures can reduce overall microbial load, but paradoxically, they may favor any bacteria that carry metal resistance genes. For instance, vancomycin-resistant Enterococcus faecium (VRE) isolates from hospitals frequently also exhibit high-level copper resistance, attributed to the tcrYAZ locus on a plasmid that is often linked with the vanA gene.^[37] This suggests that VRE originating in farms (where copper is used) can survive on copper-infused hospital surfaces, complicating infection control.

Another clinical dimension is heavy metal contamination in human-impacted environments such as drinking water and urban soils. Lead pipes or copper plumbing can leach metals into water supplies; chronic exposure of gut or skin flora to such metals could maintain selection for resistance in the population. Hospital wastewater is a particularly concentrated mixture of antibiotics, biocides, and metals (e.g., from radiology contrast agents or lab reagents) that enters municipal sewage. Bacteria in hospital effluent and sewage treatment plants are thus bombarded with both antibiotics and metals, promoting gene exchange. Mitigating this combined pollution is important for public health.

A striking example linking heavy metals to clinical AMR emerged from war zones. Combat injuries with embedded shrapnel or soil introduce metals (lead, antimony, copper from bullets and explosives) directly into wounds.^[38] Researchers noted that during the Iraq war, multidrug-resistant Acinetobacter baumannii (“Iraqibacter”) infections surged, and these isolates often carried genes for heavy metal efflux and detoxification.^[39] It is hypothesized that battlefield heavy metal contamination co-selected for A. baumannii strains that were also antibiotic-resistant, helping them outcompete susceptible bacteria in wounds laced with metal fragments.^[40] This wartime scenario underscores how environmental metal exposure can have a direct clinical impact by selecting hardier, drug-resistant opportunists. More broadly, heavy metal-driven AMR represents a pathway of resistance emergence that is independent of antibiotic use.^[41] Improved antibiotic stewardship alone cannot address this, so public health efforts must also target environmental contaminants. In summary, while antibiotics are the proximal cause of most clinical resistance, heavy metals form an often overlooked background pressure that primes bacteria to be multi-resistant before they ever encounter a human patient.

Mechanistic Insights into Metal-Driven Co-selection

Heavy metal exposure and antibiotic resistance are mechanistically intertwined through several non-mutually exclusive routes. These include co-resistance (different resistance genes linked together), cross-resistance (one mechanism providing dual resistance), co-regulatory responses, metal-induced stress physiology, and horizontal gene transfer facilitation. The subsections below detail each mechanism, highlighting known molecular players and examples (also summarized in Table 2).

Co-resistance: Linked Genes on Mobile Elements

Co-resistance refers to the genetic linkage of resistance determinants so that a single bacterial strain (or plasmid) carries resistance to both metals and antibiotics. In this scenario, the use of either selective agent (metal or drug) can enrich bacteria that incidentally carry resistance to the other agent, since the genes are inherited together.^[42] Co-resistance most commonly arises from mobile genetic elements–plasmids, transposons, integrons – that accumulate multiple resistance genes. A classic example is the pIGRJ conjugative plasmid in Enterococcus faecium from swine, which harbors tcrB (teicoplanin/copper resistance gene) alongside erm(B) (erythromycin resistance) and vanA (vancomycin resistance). All these genes are transmitted as a unit during plasmid transfer. ^[43] Under copper exposure (e.g., in pig intestines or on copper surfaces), bacteria carrying this plasmid are selected, thereby also propagating vancomycin and macrolide resistance. Another example is a plasmid in Serratia marcescens that was found to carry an array of metal resistance genes (to arsenic, copper, mercury, and silver) physically linked with multiple antibiotic resistance genes (conferring chloramphenicol, tetracycline, and kanamycin resistance).^[44] Isolates with this plasmid could survive heavy metal shock and were concurrently multi-drug-resistant. Salmonella enterica serovars have likewise been reported to possess integron-borne Hg resistance operons adjacent to genes for ampicillin, chloramphenicol, sulfonamide, and trimethoprim resistance.^[45] In these cases, a single acquisition (of a plasmid or transposon) endows the bacterium with a suite of resistances, so any one pressure (e.g., mercury from the environment) co-selects all the traits. Co-resistance explains why environments containing no antibiotics can still breed pathogens resistant to multiple drugs.^[46] It also means efforts to remove one type of pressure (say, reducing antibiotic use) may not fully succeed if another pressure (metals, biocides) maintains the resistant strains.

Cross-resistance: Shared Mechanisms and Efflux Pumps

Cross-resistance occurs when a single molecular mechanism confers protection against both heavy metals and antibiotics.^[47][48] Unlike co-resistance (which involves separate genes hitchhiking together), cross-resistance often involves broad-spectrum resistance factors, the most prominent being multidrug efflux pumps. Many bacterial efflux systems can extrude a range of structurally dissimilar toxicants, including multiple antibiotic classes as well as certain metal ions thereby reducing intracellular concentrations of both. Heavy metals can act as inducers or substrates of these pumps. For instance, the MdrL pump in Listeria monocytogenes transports Zn, Co, and CrO out of the cell, and the same pump also exports macrolide antibiotics like erythromycin and clindamycin.^[49] Exposure to any one of those agents can activate pump expression, leading to cross-protection. Similarly, the CmeABC efflux pump of Campylobacter jejuni, originally characterized for antibiotic resistance, has been shown to mediate resistance to cobalt and copper ions alongside fluoroquinolones, tetracycline, and ethidium bromide. A striking case is the RND-family efflux system (DsbA-DsbB) in Burkholderia cepacia, which, when overexpressed, yields resistance to β-lactams, aminoglycosides, and fluoroquinolones and to zinc and cadmium ions.^[50][51] These pumps typically have low specificity and can bind/export diverse compounds. Heavy metal exposure can select for mutations or regulatory changes that upregulate efflux pumps, thereby concomitantly raising antibiotic MICs. Indeed, laboratory studies demonstrate that sub-lethal concentrations of Cu or Zn can select for mutants overproducing efflux pumps, resulting in antibiotic cross-resistance (e.g., increased tolerance to quinolones and β-lactams).^[52] Even without genetic mutation, many efflux operons (like acrAB-TolC in Gram-negatives) are controlled by global stress regulators that respond to metal stress signals, leading to transient pump overexpression. One WWTP study reported that very low levels of several metals altered efflux gene expression and promoted multidrug resistance in resident bacteria.^[53]

Thus, cross-resistance via efflux is a pervasive and insidious mechanism: heavy metals essentially “teach” bacteria to ramp up defenses that also work against antibiotics. Beyond efflux, other cross-resistance mechanisms include enzymatic detoxification (e.g., some oxidoreductases can neutralize both metallic ions and certain antibiotics) and target modification (if a metal and an antibiotic act on the same cellular target, a protective mutation could confer resistance to both). However, such cases are less common than efflux-based cross-resistance. In summary, cross-resistance means a single biochemical shield is doing double duty, which is a key reason why heavy metal presence in an environment can directly increase the frequency of multi-drug-resistant phenotypes.^[54]

Co-regulation of Metal and Antibiotic Resistance

While co-resistance and cross-resistance involve structural genes, co-regulatory resistance refers to shared regulatory circuits that control disparate resistance determinants in response to one stimulus. This is a comparatively rarer phenomenon but provides elegant examples of the cell’s regulatory network linking metal and antibiotic responses.^[55] In co-regulation, a single regulator (often a transcription factor or two-component system) modulates the expression of both metal resistance genes and antibiotic resistance genes. A well-characterized case is the CzcRS two-component system in Pseudomonas aeruginosa. CzcRS is a heavy-metal-sensing regulatory pair: CzcS (sensor kinase) detects external Zn, Cd, or Co and phosphorylates CzcR (response regulator). Phospho-CzcR then activates the czcCBA efflux pump operon, which expels Co, Zn, Cd, and simultaneously represses the oprD porin gene.^[56] OprD is a channel that allows uptake of carbapenem antibiotics; by down-regulating OprD, the bacterium reduces imipenem entry, thereby increasing carbapenem resistance as a side-effect of heavy metal response.[x] In essence, P. aeruginosa in a zinc-rich environment will turn on metal efflux and incidentally become more antibiotic-resistant (to imipenem) through co-regulation. Another potential example is the BaeSR two-component system in Escherichia coli, which responds to envelope stressors, including heavy metals, and triggers expression of the MdtABC multidrug efflux pump linking metal sensing to antibiotic efflux, although the full scope of BaeSR’s role in co-selection is still under investigation. Overall, co-regulation underscores that bacteria’s stress responses are highly interconnected: a single regulatory switch can reconfigure the cell to withstand multiple threats. Though fewer cases are known compared to co- or cross-resistance, co-regulatory mechanisms are important as they can rapidly induce multidrug resistance in response to environmental metals without requiring new mutations or gene acquisitions.

Horizontal Gene Transfer Facilitated by Heavy Metals

Heavy metals not only select for existing resistance genes but can also facilitate the spread of ARGs by enhancing horizontal gene transfer (HGT) processes. There are several ways this occurs. Firstly, metal stress can enrich mobile genetic elements, as discussed (plasmids, integrons, transposons carrying MRGs/ARGs). But beyond enrichment, sub-toxic levels of metals can physiologically stimulate HGT. Studies have shown that sub-inhibitory concentrations of Cu, Zn, Ag, and Cr can increase the conjugation frequency of plasmids between bacteria.^[57]

For example, exposure of a donor and recipient to a low dose of copper might induce membrane changes or the SOS response, resulting in a higher likelihood that a conjugative plasmid successfully transfers. One report demonstrated that heavy metal co-exposure (e.g., a mix of Cd with an antibiotic) led to up-regulation of conjugation machinery genes on plasmid RP4 and an elevated transfer rate of that plasmid in a freshwater microcosm.^[58] Mechanistically, metals can generate oxidative stress and DNA damage, activating the SOS response in bacteria; in class 1 integron-bearing cells, the SOS response induces the integrase enzyme IntI1, promoting the rearrangement and capture of gene cassettes (often ARGs).^[59] Thus, metal-stressed cells may have heightened integron activity, shuffling resistance genes more readily. Metals can also select for conjugative plasmids indirectly by killing or inhibiting plasmid-free competitors. For instance, long-term nickel exposure in soils was found to significantly increase not just ARG abundance but also the prevalence of integrons and other MGEs, suggesting Ni favors bacteria that carry transferable resistance elements.^[60] Additionally, in biofilm communities, heavy metals often promote biofilm formation (as a protective response), which creates dense cell aggregates ideal for HGT. Biofilms allow close cell-to-cell contact and can concentrate plasmid transfer events; one study noted that metal pollutants in river biofilms led to enrichment of both MRGs and ARGs and provided optimal conditions for gene exchange.^[61] In summary, heavy metals can act as HGT catalysts – by inducing the cellular stress pathways that control gene transfer, by selecting for mobile element carriers, and by fostering communal states (biofilms) that ease DNA exchange. This acceleration of resistance gene dissemination under metal pressure is especially problematic in mixed pollution scenarios (e.g., metals + antibiotics + microplastics), where all factors together create a “perfect storm” for ARG spread.^[62]

Metal-Induced Stress Responses and Mutation

Beyond specific resistance mechanisms, heavy metals impose a general stress on bacteria that can lead to adaptive mutagenesis and enhanced survival traits. Many heavy metals participate in Fenton-like reactions or disrupt redox balance, causing the generation of reactive oxygen species (ROS).^[63] ROS inflict DNA damage, protein misfolding, and membrane lipid peroxidation. Bacteria respond by activating global stress response regulons (e.g., SoxRS, OxyR, RecA/LexA for SOS). A side effect of this is an increased mutation rate – error-prone DNA polymerases get deployed to rescue heavily damaged DNA, potentially introducing mutations that confer antibiotic resistance (for example, a gyrA mutation conferring quinolone resistance might arise under metal-induced SOS activation). Indeed, some research has observed that metal exposure selects for rifampicin- or quinolone-resistant mutants in E. coli and Mycobacterium populations, presumably via ROS-mediated mutagenesis (though direct evidence is still emerging). Moreover, heavy metal stress can select for generally stress-tolerant phenotypes that incidentally weather antibiotic attacks better. One such phenotype involves the glyoxalase system. Methylglyoxal (MG) is a reactive cytotoxin that is overproduced in cells under stress (due to imbalances in glycolysis). Heavy metals have been shown to impair the glyoxalase pathway, causing MG accumulation as part of their toxicity.^[64] Bacteria that can upregulate glyoxalase enzymes (principally glyoxalase I and II) can detoxify MG into harmless metabolites, thereby surviving metal stress more effectively. These “glyoxalase-positive” bacteria not only cope with metals but also resist MG-dependent toxicity mechanisms. This has implications for antibiotic resistance: methylglyoxal is known to have bactericidal activity and is actually employed by the immune system (e.g. human neutrophils generate MG to kill bacteria).^[65] Pathogens with robust glyoxalase activity can neutralize host-derived MG, thus contributing to virulence and survival during infection. For example, Streptococcus agalactiae (Group B strep) requires a functional glyoxalase I (gloA) to withstand MG stress and survive in blood; gloA mutants are attenuated in infection models.^[66] Notably, glyoxalase I in many bacteria is a Ni metalloenzyme.^[67] In E. coli and others, Ni+ is the preferred cofactor for glyoxalase I activity, although Zn can substitute in some species. This means nickel availability can enhance glyoxalase-mediated stress tolerance. If a bacterium is in a Ni-contaminated environment, it might activate Ni-dependent enzymes like glyoxalase I to counteract MG buildup, gaining a survival edge. Over time, communities exposed to Ni could become enriched in glyoxalase-positive, Ni-requiring bacteria that also happen to be hardy against other stresses. While research directly linking glyoxalase to antibiotic resistance is nascent, the correlation is plausible: glyoxalase reduces endogenous toxin stress and potentially frees up resources for bacteria to invest in defense against antibiotics. At minimum, glyoxalase illustrates how metal-induced physiological adaptations (managing oxidative and metabolic stress) can broadly increase bacterial robustness, indirectly facilitating antibiotic resistance.

In summary, heavy metal contamination pressures bacteria in multiple ways – genetic, biochemical, and physiological that all tilt the evolutionary balance towards antibiotic resistance. Table 2 distills the key co-selection mechanisms and their molecular bases, and Table 3 lists several bacteria and plasmids exemplifying these mechanisms.

Case Studies and Evidence from Recent Research

To concretely link these concepts to real-world scenarios, we highlight a few representative case studies spanning environmental, agricultural, and clinical contexts:

Nickel-Contaminated Agricultural Soils: Hang-Wei Hu et al. (2017) conducted a long-term field experiment in which agricultural plots were amended with nickel sulfate (up to 400 mg Ni/kg soil) for 4–5 years.^[68] Metagenomic and qPCR analyses revealed a significant increase in the diversity and abundance of ARGs in Ni-treated soils compared to controls.^[69] Over 149 unique ARGs were detected, with Ni exposure selecting especially for multidrug and β-lactam resistance genes.^[70] Importantly, Ni-amended soils showed elevated levels of class 1 integron integrase (intI1) and other mobile element markers, indicating enhanced horizontal gene transfer potential.^[71] Network analysis in the study showed intI1 was centrally connected to many co-occurring ARGs, suggesting Ni was selected for integron-bearing bacteria that can collect resistance genes.^[72] This provides direct evidence that a heavy metal (Ni) can drive ARG proliferation in soil over time.

Pig Farms – Zinc and MRSA: In Danish pig farms, zinc oxide is often added to piglet feed at high doses. A study by A. Moodley et al. found that this practice correlated with increased nasal carriage of MRSA in pigs. Molecular typing showed the MRSA strains were of the livestock-associated ST398 lineage and carried the czrC gene for zinc resistance on the SCCmec element.^[73] All MRSA isolates from zinc-fed pigs were zinc-resistant, whereas MRSA from farms not using Zn feed had lower zinc tolerance.^[74] This indicates zinc use was selecting for MRSA specifically equipped with zinc efflux machinery. Subsequent work demonstrated that the czrC and mecA genes are physically linked. This case confirms that a heavy metal in the absence of any antibiotic can enrich a dangerous antibiotic-resistant pathogen in livestock, exemplifying co-selection in agriculture.

War Wound Infections – Heavy Metals and A. baumannii: Military physicians observed an unusual prevalence of MDR Acinetobacter baumannii infections in soldiers wounded by improvised explosive devices (IEDs) in Iraq and Afghanistan.^[75] Environmental analysis of wound debris and soil from war zones showed high concentrations of metals like lead, antimony, copper, and tungsten from munitions.^[76] Bazzi et al. (2020) reviewed evidence that these heavy metals could be selecting for A. baumannii strains with co-resistance. Many war-zone A. baumannii isolates carried genes for Cu efflux, arsenic resistance, and mercury reductases in addition to β-lactamases and other ARGs.^[77] Copper resistance in particular (via cop and cue gene clusters) was enriched. The timing and geography of outbreaks suggest that battlefield metal contamination created a niche for metal-tolerant, MDR A. baumannii (“Iraqibacter”). This case underscores the One Health principle: environmental destruction (through war) had clinical repercussions in the form of difficult-to-treat wound infections.^[78]

River Systems – Mixed Industrial Pollution: A 2022 study (Newcastle Univ. & IIT Delhi) examined sediments from the Ganges and Yamuna rivers in India and the River Tyne in the UK.^[79] These sites receive industrial effluents rich in heavy metals. The researchers found a positive correlation between metal concentrations and both MRG and ARG abundances in sediments.^[80] Notably, sections of the Tyne with legacy mine pollution had among the highest ARG levels despite no local antibiotic sources.^[81] They also observed that certain metal pairs (Co + Ni) and combinations (Co + Zn + Cd) produced the greatest increase in ARGs, hinting at synergistic co-selection by metal mixtures.^[82] The bacterial community shifted towards metal-tolerant taxa carrying integrons, explaining mechanistically how metal exposure translated to ARG enrichment.^[83] This study provides a clear environmental parallel to clinical AMR hotspots: contaminated rivers can act as reservoirs and mixing bowls for resistance genes, potentially transmitting them to human pathogens downstream.

Wastewater Treatment Plants (WWTPs): Several investigations have looked at how heavy metals in wastewater impact microbial resistance. In one WWTP study, trace amounts of metals (particularly Cu and Zn) were shown to select for multi-drug efflux pump overexpression in E. coli isolates.^[84] Another experimental study by Wang et al. (2020) found that exposing a model bacterial community to a low level of Cr(VI) or Ag(I) significantly increased the conjugative transfer frequency of a multidrug resistance plasmid (RP4) among the bacteria.^[85] Genome sequencing of transconjugants revealed no new resistance mutations, implying the effect was due to metal-stimulated transfer rather than selection of mutants.^[86] These WWTP findings reinforce that even in modern engineered systems, heavy metals can bolster the persistence and spread of ARGs, complicating efforts to eliminate resistance in effluent discharges.

Together, such case studies affirm that heavy metal contamination is a tangible contributor to the rise of antibiotic resistance across diverse settings. They also highlight the mechanistic themes discussed earlier: in each case, either co-resistance (linked genes) or cross-resistance (shared mechanisms like efflux) or HGT promotion was evident. By integrating these perspectives, we gain a more holistic understanding of AMR’s environmental dimensions. The following tables summarize key findings, mechanisms, and notable co-resistant microbes from the literature:

Table 1. Selected Studies Linking Heavy Metal Contamination to Antibiotic Resistance (environmental, agricultural, industrial examples with key findings):

Context / Study	Heavy Metal(s)	Key Findings on Antibiotic Resistance	Source
Agricultural soil (China) – Long-term field trial with Ni supplementation for 5 years.[87]	Nickel (Ni)	ARG diversity and abundance increased along Ni gradient; highest at 400 mg/kg Ni. Enrichment of class 1 integrons (intI1) and mobile elements, indicating enhanced HGT . Ni exposure drove co-selection of multiple ARG classes (β-lactams, multidrug, etc.)	Hu et al., 2017 [88] (Environ. Sci. Technol.)
Pig farm manure & soil (Europe) – Surveys of pig slurry and farm soil microbiomes.	Zinc (Zn), Copper (Cu), Cadmium (Cd)	High co-occurrence of ARGs with metal resistance genes in pig manure and nearby soils. [89][90] Zn/Cu administered in feed selected for bacteria harboring both metal- and antibiotic resistance (e.g. Enterococcus with Cu and vancomycin genes). Indicates manure-borne metals maintain ARG pools in the environment.	Wu et al., 2016 (BMC Genomics) ; Anton et al., 2022 (Vet. Res.)
Livestock-associated MRSA in pigs (Denmark) – Effect of high-Zn feed on MRSA carriage.[91]	Zinc (Zn)	Zn supplementation in feed selected for MRSA carrying czrC (Zn/Cd efflux gene). All MRSA from Zn-treated pigs were Zn-resistant. czrC is co-located with mecA (methicillin resistance); thus Zn use co-selects MRSA. [92] MRSA prevalence and persistence increased under ZnO therapy.[93]	Moodley et al., 2008; Slifierz et al., 2015.[94]
River sediments near mines/industry (UK, India) – Newcastle University study	Mixed metals (Pb, Ni, Zn, Cd, Co, etc.)	Sediments with high metal concentrations had high ARG levels.[95] Positive correlations between metal pollution indices and ARG/MRG abundances. Firmicutes and Bacteroidota dominated contaminated sites, carrying integron-borne ARG-MRG cassettes. Metal combinations (Co+Ni, Co+Zn+Cd) showed the strongest ARG proliferation.[96]	Pal et al., 2017 (Environ. Pollut.);
Battlefield wound infections (Iraq/ Afghanistan) – MDR “Iraqibacter” outbreaks.[97]	Lead (Pb), Copper (Cu), Antimony (Sb), others in shrapnel	War injuries contaminated with metal fragments led to the selection of MDR A. baumannii. Isolates from war wounds carried heavy metal resistance genes (Cu-export, arsenic, and mercury operons) along with antibiotic genes.[x] Heavy metal debris in wounds hypothesized to drive co-resistance, explaining the high incidence of carbapenem-resistant A. baumannii in conflict zones.[98]	Bazzi et al., 2020 11 36 (Front. Microbiol.)
Wastewater treatment plant bacteria – Lab exposure studies.	Copper (Cu), Zinc (Zn), Chromium (Cr), Silver (Ag)	Sub-inhibitory Cu and Zn in WWTP cultures caused overexpression of efflux pumps and increased tolerance to multiple antibiotics.[99] Exposure to low-dose Cr or Ag significantly increased conjugative plasmid transfer rates of ARG-bearing plasmids.[100] Suggests WWTP metals enhance cross-resistance and HGT in situ.	Knapp et al., 2011; Wang et al., 2020. [101]

Table 1: Case studies illustrating heavy metal-induced co-selection of antibiotic resistance. Each example shows how a particular metal contamination scenario led to increased antibiotic resistance in microbes, via co-resistance, cross-resistance, or enhanced gene transfer. ARG = antibiotic resistance gene; MRG = metal resistance gene; HGT = horizontal gene transfer.

Table 2. Mechanisms of Co-selection by Heavy Metals – Summary of Molecular Pathways: ^[102]

Co-selection	Description	Mechanism, Molecular Basis, and Examples
Co-resistance (physical linkage)	Selection for one resistance trait (metal or antibiotic) co-selects another due to genetic linkage on the same mobile element.[103] Inherited together.	Heavy metals enhance the horizontal transfer of ARGs and maintenance of resistance plasmids/ integrons.
Cross-resistance (shared mechanism)	One biochemical mechanism imparts resistance to both metal and antibiotics.[104] A single adaptive change protects against both stressors.	Basis: Typically, multidrug efflux pumps or common target modification. Examples: MdrL pump in Listeria exports Zn, CrO, and macrolide antibiotics; CmeABC pump in Campylobacter extrudes Cu, Co, and fluoroquinolones; DsbA-DsbB efflux in B. cepacia -> resistance to β-lactams, aminoglycosides, and Zn, Cd.[105] Result: Metal exposure induces pump expression, reduces intracellular antibiotic levels (elevating MIC).
Co-regulation (regulatory linkage)	A shared regulator or signaling pathway controls both metal resistance and antibiotic resistance genes.[106] Metal triggers a regulatory response that affects antibiotic susceptibility.	Basis: Multiple resistance genes on plasmids, integrons, and transposons. Examples: Plasmid pRUM in E. faecium carries tcrB (Cu resistance) with vanA (vancomycin)[107] Integron In2 in Serratia – carries arsenic, mercury, silver genes with antibiotic (chloramphenicol, tetracycline, etc.) resistances.[108] Result: Heavy metal presence retains multi-ARG plasmid in population.
Metal-induced HGT (gene transfer)	Heavy metals enhance horizontal transfer of ARGs and maintenance of resistance plasmids/ integrons.	Basis: Metals induce SOS response and stress, stimulating integrase activity and conjugation machinery. [109] Biofilm formation under metals fosters cell contact. Examples: intI1 integrase frequency is higher in metal-polluted microbiomes (integrons capture ARGs) [110]. Sub-lethal Cu/Zn increases F-plasmid conjugation rates; Cd antibiotic co-exposure upregulates plasmid transfer genes (in P. putida experiment), leading to more frequent ARG transmission.[111]
Stress responses & mutagenesis	Metals cause oxidative and metabolic stress, promoting error-prone DNA repair and selection of stress-tolerant mutants	Basis: ROS generation by metals → DNA damage → SOS mutagenesis → possible emergence of resistance mutations. Metals also trigger global stress regulons (e.g., oxidative stress defenses) that can cross-protect against certain antibiotics (those that induce ROS). Examples: E. coli exposed to sub-lethal Cr(VI) showed increased mutation rates to rifampicin resistance (via ROS damage, reported in lab studies). Glyoxalase system upregulation under metal stress detoxifies methylglyoxal (toxin); glyoxalase-positive bacteria better survive both metal and host immune stresses.[112] Strep. with active GloA (Ni-dependent glyoxalase I) tolerated MG was more virulent.[113]

Table 2: Major mechanisms by which heavy metals co-select for antibiotic resistance. Each mechanism is defined, with its molecular basis and an example. Co-resistance = physical linkage of genes; Cross-resistance = one mechanism, two resistances; Co-regulation = one regulator controls multiple resistance genes; HGT = horizontal gene transfer processes; Stress responses = indirect selection via general stress and mutation. References illustrate specific cases.

Table 3. Examples of Bacterial Taxa and Elements with Co- or Cross-Resistance to Metals and Antibiotics:^[114]

Bacterium/ Plasmid	Implicated Metal(s)	Antibiotic Resistance Trait(s)	Mechanism	Reference
Enterococcus faecium (pig isolate)	Copper (Cu) via tcrB operon	Vancomycin (VanA), erythromycin (ErmB) on the same plasmid	Co-resistance (plasmid-borne gene linkage)	Hasman & Aarestrup 2002; Silveira et al. 2014 [115]
Staphylococcus aureus ST398 (LA-MRSA)	Zinc (Zn), Cadmium (Cd) via czrC efflux.[116]	Methicillin (mecA on SCCmec); also tetracycline often co-selected	Co-resistance (genetic linkage on SCCmec element)	Cavaco et al., 2010; Moodley et al., 2008. [117][118]
Pseudomonas aeruginosa	Cobalt (Co), Zinc (Zn), Cadmium (Cd) sensed by CzcRS.	Carbapenems (imipenem) via loss of OprD porin; multidrug efflux (Mex pumps) also contribute	Co-regulation (two-component system CzcRS controlling metal efflux & antibiotic uptake)	Perron et al., 2004. [119]
Burkholderia cepacia	Zinc (Zn), Cadmium (Cd)	β-lactams, aminoglycosides, fluoroquinolones	Cross-resistance (broad-spectrum DsbA-DsbB efflux pump)	Hayashi et al., 2000; Bazzi et al., 2020. [120]
Campylobacter jejuni	Cobalt (Co), Copper (Cu)	Fluoroquinolones (e.g. ciprofloxacin), macrolides (erythromycin)	Fluoroquinolones (e.g., ciprofloxacin), macrolides (erythromycin)	Lin et al., 2002.[121]
Listeria monocytogenes	Zinc (Zn), Cobalt (Co), Chromium (Cr)	Macrolides (erythromycin, clindamycin)	Cross-resistance (MdrL efflux pump for metal & drugs)	Mata et al., 2000. [122]
Serratia marcescens plasmid	Arsenic (As), Copper (Cu), Mercury (Hg), Silver (Ag)	Chloramphenicol, Tetracycline, Kanamycin (all encoded on the same plasmid).[123]	Co-resistance (multiple resistance genes colocated)	Gilmour et al., 2004[124]
Salmonella enterica (Typhi and others)	Mercury (Hg) via mer operon	Multi-drug: e.g., Chloramphenicol (cat), β-lactams (bla_TEM), Sulfonamides (sul1), Trimethoprim (dfr)	Co-resistance (transposon with mer and ARGs)	Wireman et al., 1997 ; Boyd et al., 1996. [125]
Integrative Conjugative Element ICEpMER (Klebsiella pneumoniae)	Mercury (Hg), Tellurite (Te)	Extended-spectrum β-lactamases (CTXM), quinolone resistance (qnr)	Co-resistance (ICE with metal + drug genes)	Rowswell et al., 2019 (example of co-resistant ICE in Enterobacteriaceae)
Escherichia coli (lab strain with plasmid pRP4)	Chromium (Cr), Silver (Ag) experimentally	Ampicillin, Tetracycline, Kanamycin (on RP4 plasmid)	HGT facilitation (metal-induced higher conjugation frequency)	Wang et al., 2020 (Env. Int.)[126]

Table 3: Representative bacteria and genetic elements exhibiting linked heavy metal and antibiotic resistance. These examples illustrate the range of taxa (Gram-positive and Gram-negative) and mechanisms (plasmid co-resistance, efflux-mediated cross-resistance, co-regulatory systems) involved in metal-driven antibiotic resistance. LA-MRSA = livestock-associated MRSA. (Note: This is not exhaustive; many other examples exist in literature.)

Conclusion

Heavy metal contamination has emerged as a significant and underappreciated force driving the global rise of antibiotic resistance. Through long-term persistence in the environment, heavy metals impose a selective pressure that enriches bacterial populations for metal resistance, and by various co-selection mechanisms, this often means enriching for antibiotic resistance as well.^[127][128] Environmental, agricultural, industrial, and clinical data all converge on this point. In the environment, non-antibiotic pollutants like metals can create antibiotic-resistant reservoirs in soils and waters that ultimately threaten human and animal health. In agriculture, heavy metal usage sustains multidrug-resistant organisms in livestock and crop systems, complicating efforts to curb AMR via antibiotic stewardship alone.^[129] Industrial emissions and urban pollution with metals similarly contribute to a backbone of resistance in microbial communities. Clinically, metal-driven co-selection (e.g., via copper or arsenic resistance genes linked to drug resistance) means that hospitals and war zones alike must contend with pathogens whose multidrug resistance may have been incubated by exposure to metals rather than therapeutic antibiotics.^[130]

Mechanistically, heavy metals and antibiotics are intertwined in microbial evolution. Co-resistance (genes carried together on plasmids or integrons) and cross-resistance (common efflux pumps or protective enzymes) create direct molecular links between metal tolerance and antibiotic resistance.^[131] Co-regulatory circuits demonstrate that bacteria’s response to a toxic metal can automatically induce antibiotic resistance phenotypes.^[132] Metals also amplify horizontal gene transfer, speeding the propagation of ARGs through communities and across species boundaries. ^[133] They trigger stress responses and mutagenesis pathways that can spawn new resistance mutations and favor hardy phenotypes like glyoxalase-rich, oxidative-stress-resistant cells. The special case of nickel highlights how an essential yet toxic metal can spur co-selection: nickel contamination selects for Ni-dependent enzymes (like glyoxalase I) and Ni-resistant efflux systems, indirectly arming bacteria against multiple stresses, including antibiotics.^[134] Meanwhile, “glyoxalase-positive” bacteria exemplify how metabolic resilience to one stress (methylglyoxal from either metals or immune attack) can confer an advantage under antibiotic treatment or within host environments.^[135] In light of these insights, combating antibiotic resistance demands an integrated approach. Environmental regulations should limit heavy metal pollutants, and remediation of contaminated sites could help diminish the environmental reservoir of ARGs.^[136] In agriculture, finding alternatives to heavy metal feed additives (or judiciously limiting their use) is key to preventing co-selection of superbugs at the source. Improved waste management – treating metal-rich industrial and hospital wastewater – may reduce the collateral selection for resistance in downstream ecosystems. From a research perspective, there is a need for continued surveillance of metals in high-risk environments (e.g. densely populated urban soils, aquaculture ponds, conflict zones) and how they correlate with resistomes, as well as mechanistic studies into novel co-regulatory or cross-resistance pathways (for instance, the role of other metal-responsive regulators, or the impact of nanomaterials and metalloid pollutants on AMR gene mobility).

Overall, heavy metals and antibiotic resistance are two sides of the same coin in microbial ecology. Heavy metal contamination is not just an environmental toxicology issue; it is directly linked to the public health challenge of AMR. Addressing one without the other would be a half-measure. A One Health strategy that encompasses environmental metal pollution control, sustainable agricultural practices, and prudent antibiotic use is essential to stem the tide of resistance. By recognizing heavy metals as silent drivers of antibiotic resistance, we can design more effective interventions to protect the efficacy of life-saving antibiotics for future generations.

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75. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
76. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
77. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
78. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
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80. Effects of heavy metals pollution on the co-selection of metal and antibiotic resistance in urban rivers in UK and India.. Gupta S, Graham DW, Sreekrishnan TR, Ahammad SZ.. (Environmental Pollution. 2022)
81. Effects of heavy metals pollution on the co-selection of metal and antibiotic resistance in urban rivers in UK and India.. Gupta S, Graham DW, Sreekrishnan TR, Ahammad SZ.. (Environmental Pollution. 2022)
82. Effects of heavy metals pollution on the co-selection of metal and antibiotic resistance in urban rivers in UK and India.. Gupta S, Graham DW, Sreekrishnan TR, Ahammad SZ.. (Environmental Pollution. 2022)
83. Effects of heavy metals pollution on the co-selection of metal and antibiotic resistance in urban rivers in UK and India.. Gupta S, Graham DW, Sreekrishnan TR, Ahammad SZ.. (Environmental Pollution. 2022)
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85. Metabolomic Profiling Reveals the Role of Copper Homeostasis in Arabidopsis Under Heavy Metal Stress.. Zhao, X., Xu, S., Zhang, H., Wang, L., & Chen, Y.. (Frontiers in Microbiology)
86. Metabolomic Profiling Reveals the Role of Copper Homeostasis in Arabidopsis Under Heavy Metal Stress.. Zhao, X., Xu, S., Zhang, H., Wang, L., & Chen, Y.. (Frontiers in Microbiology)
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95. Effects of heavy metals pollution on the co-selection of metal and antibiotic resistance in urban rivers in UK and India.. Gupta S, Graham DW, Sreekrishnan TR, Ahammad SZ.. (Environmental Pollution. 2022)
96. Effects of heavy metals pollution on the co-selection of metal and antibiotic resistance in urban rivers in UK and India.. Gupta S, Graham DW, Sreekrishnan TR, Ahammad SZ.. (Environmental Pollution. 2022)
97. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
98. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
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100. Metabolomic Profiling Reveals the Role of Copper Homeostasis in Arabidopsis Under Heavy Metal Stress.. Zhao, X., Xu, S., Zhang, H., Wang, L., & Chen, Y.. (Frontiers in Microbiology)
101. Metabolomic Profiling Reveals the Role of Copper Homeostasis in Arabidopsis Under Heavy Metal Stress.. Zhao, X., Xu, S., Zhang, H., Wang, L., & Chen, Y.. (Frontiers in Microbiology)
102. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
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104. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
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115. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
116. Livestock-associated methicillin-resistant Staphylococcus aureus in Korea: antimicrobial resistance and molecular characteristics of LA-MRSA strains isolated from pigs, pig farmers, and farm environment.. Back SH, Eom HS, Lee HH, Lee GY, Park KT, Yang SJ.. (J Vet Sci. 2020)
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119. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
120. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
121. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
122. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
123. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
124. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
125. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
126. Metabolomic Profiling Reveals the Role of Copper Homeostasis in Arabidopsis Under Heavy Metal Stress.. Zhao, X., Xu, S., Zhang, H., Wang, L., & Chen, Y.. (Frontiers in Microbiology)
127. The Interactions Between Antibiotic Resistance Genes and Heavy Metal Pollution Under Co-Selective Pressure Influenced the Bio-Enzyme Activity.. Qi Z, Qi Y, Le Z, Han F, Li F, Yang H, Zhang T, Feng Y, Liu R, Sun Y.. (Front Chem. 2021)
128. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
129. Nasal Carriage of mecA-Positive Methicillin-Resistant Staphylococcus aureus in Pigs Exhibits Dose–Response to Zinc Supplementation.. Amachawadi RG, Scott HM, Nitikanchana S, Vinasco J, Tokach MD, Dritz SS, Nelssen JL, Goodband RD, Nagaraja TG.. (Foodborne Pathog Dis. 2015)
130. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
131. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
132. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms.. Bazzi W, Abou Fayad AG, Nasser A, Haraoui L-P, Dewachi O, Abou-Sitta G, Nguyen V-K, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM.. (Front Microbiol. 2020)
133. Metabolomic Profiling Reveals the Role of Copper Homeostasis in Arabidopsis Under Heavy Metal Stress.. Zhao, X., Xu, S., Zhang, H., Wang, L., & Chen, Y.. (Frontiers in Microbiology)
134. Identification of glyoxalase A in group B Streptococcus and its contribution to methylglyoxal tolerance and virulence.. Akbari MS, Joyce LR, Spencer BL, Brady A, McIver KS, Doran KS.. (Infection and Immunity. 2025)
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136. Effects of heavy metals pollution on the co-selection of metal and antibiotic resistance in urban rivers in UK and India.. Gupta S, Graham DW, Sreekrishnan TR, Ahammad SZ.. (Environmental Pollution. 2022)