Resistance to ag(i) cations in bacteria: environments, genes and proteins. - Related Documents




#
Rank
Similarity
Title + Abs.
Year
PMID
012345
18801.0000Resistance to ag(i) cations in bacteria: environments, genes and proteins. Bacterial resistance to Ag(I) has been reported periodically with isolates from many environments where toxic levels of silver might be expected to occur, but initial reports were limited to the occurrence of resistant bacteria. The availability of silver-resistance conferring DNA sequences now allow genetic and mechanistic studies that had basically been missing. The genes determining Ag(I) resistance were sequenced from a plasmid found in a burn ward isolate. The 14.2 kb determinant contains seven recognized genes, arranged in three mRNA transcriptional units. The silE gene determines an extracellular (periplasmic space) metal-binding protein of 123 amino acids, including ten histidine residues implicated in Ag(I) binding. SilE is homologous to PcoE, of copper resistance. The next two genes, silR and silS, determine a two protein, histidine-kinase membrane sensor and aspartyl phosphate transcriptional responder, similar to other two component systems such as CzcR and CzcS (for cadmium, zinc and cobalt resistance) and PcoR and PcoS (for copper resistance). The remaining four genes, silCBAP, are co-transcribed and appear to determine Ag(+) efflux, with SilCBA homologous to CzcCBA, a three component cation/proton antiporter, and SilP a novel P-type ATPase with a amino-terminal histidine-rich cation-specificity region. The effects of increasing Ag(+) concentrations and growth medium halides (Cl-, Br- and I-) have been characterized, with lower Cl- concentrations facilitating resistance and higher concentrations toxicity. The properties of this unique Ag(I)-binding SilE protein are being characterized. Sequences similar to the silver-resistance DNA are being characterized by Southern blot DNA/DNA hybridization, PCR in vitro DNA synthesis and DNA sequencing. More than 25 additional closely related sequences have been identified in bacteria from diverse sources. Initial DNA sequencing results shows approximately 5-20% differences in DNA sequences.199918475907
18910.9997Arsenate detoxification in a Pseudomonad hypertolerant to arsenic. Pseudomonas sp. strain As-1, obtained from an electroplating industrial effluent, was capable of growing aerobically in growth medium supplemented with up to 65 mM arsenate (As (V)), significantly higher concentrations than those tolerated by other reference arsenic resistant bacteria. The majority of the arsenic was detected in culture supernatants as arsenite (As (III)) and X-ray absorbance spectroscopy suggested that 30% of this cell-bound arsenic was As (V), 65% As (III) and 5% of arsenic was associated with sulphur. PCR analysis using primers designed against arsenic resistance genes of other Gram-negative bacteria confirmed the presence of an arsenic resistance operon comprising of three genes, arsR, arsB and arsC in order of predicted transcription, and consistent with a role in intracellular reduction of As (V) and efflux of As (III). In addition to this classical arsenic resistance mechanism, other biochemical responses to arsenic were implicated. Novel arsenic-binding proteins were purified from cellular fractions, while proteomic analysis of arsenic-induced cultures identified the upregulation of additional proteins not normally associated with the metabolism of arsenic. Cross-talk with a network of proteins involved in phosphate metabolism was suggested by these studies, consistent with the similarity between the phosphate and arsenate anions.200717160678
44220.9996Mercuric reductase in environmental gram-positive bacteria sensitive to mercury. According to existing data, mercury resistance operons (mer operons) are in general thought to be rare in bacteria, other than those from mercury-contaminated sites. We have found that a high proportion of strains in environmental isolates of Gram-positive bacteria express mercuric reductase (MerA protein): the majority of these strains are apparently sensitive to mercury. The expression of MerA was also inducible in all cases. These results imply the presence of phenotypically cryptic mer resistance operons, with both the merA (mercuric reductase) and merR (regulatory) genes still present, but the possible absence of the transport function required to complete the resistance mechanism. This indicates that mer operons or parts thereof are more widely spread in nature than is suggested by the frequency of mercury-resistant bacteria.19921427009
845530.9996RT-PCR: characterization of long multi-gene operons and multiple transcript gene clusters in bacteria. Reverse transcription (RT)-PCR is a valuable tool widely used for analysis of gene expression. In bacteria, RT-PCR is helpful beyond standard protocols of northern blot RNA/DNA hybridization (to identify transcripts) and primer extension (to locate their start points), as these methods have been difficult with transcripts that are low in abundance or unstable, similar to long multi-gene operons. In this report, RT-PCR is adapted to analyze transcripts that form long multi-gene operons--where they start and where they stop. The transcripts can also be semiquantitated to follow the expression of genes under different growth conditions. Examples using RT-PCR are presented with two different multi-gene systems for metal cation resistance to silver and mercury ions. The silver resistance system [9 open reading frames (ORFs); 12.5 kb] is shown by RT-PCR to synthesize three nonoverlapping messenger RNAs that are transcribed divergently. In the mercury resistance system (8 ORFs; 6.3 kb), all the genes are transcribed in the same orientation, and two promoter sites produce overlapping transcripts. For RT-PCR, reverse transcriptase enzyme is used to synthesize first-strand cDNA that is used as a template for PCR amplification of single-gene products, from the beginning, middle or end of long multi-gene, multi-transcript gene clusters.199910572645
632440.9996Genetic and biochemical basis of tetracycline resistance. Properties of several, well characterized, tetracycline resistance determinants were compared. The determinants in Tn1721 and Tn10 (both from Gram-negative bacteria) each contain two genes; one encodes a repressor that regulates both its own transcription and that of a membrane protein that confers resistance by promoting efflux of the drug. Determinants from Gram-positive bacteria also encode efflux proteins, but expression of resistance is probably regulated by translational attenuation. The likely tetracycline binding site (a common dipeptide) in each efflux protein was predicted. The presence of the common binding site is consistent with the ability of an efflux protein originating in Bacillus species to be expressed in Escherichia coli.19863542941
29250.9996Mechanisms underlying expression of Tn10 encoded tetracycline resistance. Tetracycline-resistance determinants encoding active efflux of the drug are widely distributed in gram-negative bacteria and unique with respect to genetic organization and regulation of expression. Each determinant consists of two genes called tetA and tetR, which are oriented with divergent polarity, and between them is a central regulatory region with overlapping promoters and operators. The amino acid sequences of the encoded proteins are 43-78% identical. The resistance protein TetA is a tetracycline/metal-proton antiporter located in the cytoplasmic membrane, while the regulatory protein TetR is a tetracycline inducible repressor. TetR binds via a helix-turn-helix motif to the two tet operators, resulting in repression of both genes. A detailed model of the repressor-operator complex has been proposed on the basis of biochemical and genetic data. The tet genes are differentially regulated so that repressor synthesis can occur before the resistance protein is expressed. This has been demonstrated for the Tn10-encoded tet genes and may be a common property of all tet determinants, as suggested by the similar locations of operators with respect to promoters. Induction is mediated by a tetracycline-metal complex and requires only nanomolar concentrations of the drug. This is the most sensitive effector-inducible system of transcriptional regulation known to date. The crystal structure of the TetR-tetracycline/metal complex shows the Tet repressor in the induced, non-DNA binding conformation. The structural interpretation of many noninducible TetR mutants has offered insight into the conformational changes associated with the switch between inducing and repressing structures of TetR. Tc is buried in the core of TetR, where it is held in place by multiple contacts to the protein.19947826010
47760.9996Novel nickel resistance genes from the rhizosphere metagenome of plants adapted to acid mine drainage. Metal resistance determinants have traditionally been found in cultivated bacteria. To search for genes involved in nickel resistance, we analyzed the bacterial community of the rhizosphere of Erica andevalensis, an endemic heather which grows at the banks of the Tinto River, a naturally metal-enriched and extremely acidic environment in southwestern Spain. 16S rRNA gene sequence analysis of rhizosphere DNA revealed the presence of members of five phylogenetic groups of Bacteria and the two main groups of Archaea mostly associated with sites impacted by acid mine drainage (AMD). The diversity observed and the presence of heavy metals in the rhizosphere led us to construct and screen five different metagenomic libraries hosted in Escherichia coli for searching novel nickel resistance determinants. A total of 13 positive clones were detected and analyzed. Insights about their possible mechanisms of resistance were obtained from cellular nickel content and sequence similarities. Two clones encoded putative ABC transporter components, and a novel mechanism of metal efflux is suggested. In addition, a nickel hyperaccumulation mechanism is proposed for a clone encoding a serine O-acetyltransferase. Five clones encoded proteins similar to well-characterized proteins but not previously reported to be related to nickel resistance, and the remaining six clones encoded hypothetical or conserved hypothetical proteins of uncertain functions. This is the first report documenting nickel resistance genes recovered from the metagenome of an AMD environment.200717675438
26770.9995Molecular characterization of resistance-nodulation-division transporters from solvent- and drug-resistant bacteria in petroleum-contaminated soil. PCR assays for analyzing resistance-nodulation-division transporters from solvent- and drug-resistant bacteria in soil were developed. Sequence analysis of amplicons showed that the PCR successfully retrieved transporter gene fragments from soil. Most of the genes retrieved from petroleum-contaminated soils formed a cluster (cluster PCS) that was distantly related to known transporter genes. Competitive PCR showed that the abundance of PCS genes is increased in petroleum-contaminated soil.200515640241
845680.9995Identification of genes required by Bacillus thuringiensis for survival in soil by transposon-directed insertion site sequencing. Transposon-directed insertion site sequencing was used to identify genes required by Bacillus thuringiensis to survive in non-axenic plant/soil microcosms. A total of 516 genetic loci fulfilled the criteria as conferring survival characteristics. Of these, 127 (24.6 %) were associated with uptake and transport systems; 227 loci (44.0 %) coded for enzymatic properties; 49 (9.5 %) were gene regulation or sensory loci; 40 (7.8 %) were structural proteins found in the cell envelope or had enzymatic activities related to it and 24 (4.7 %) were involved in the production of antibiotics or resistance to them. Eighty-three (16.1 %) encoded hypothetical proteins or those of unknown function. The ability to form spores was a key survival characteristic in the microcosms: bacteria, inoculated in either spore or vegetative form, were able to multiply and colonise the soil, whereas a sporulation-deficient mutant was not. The presence of grass seedlings was critical to colonisation. Bacteria labelled with green fluorescent protein were observed to adhere to plant roots. The sporulation-specific promoter of spo0A, the key regulator of sporulation, was strongly activated in the rhizosphere. In contrast, the vegetative-specific promoters of spo0A and PlcR, a pleiotropic regulator of genes with diverse activities, were only very weakly activated.201424310935
48490.9995Evidence for high affinity nickel transporter genes in heavy metal resistant Streptomyces spec. We have isolated 25 new strains of streptomycetes from soil samples of a polluted site at the former uranium mine, Wismut, in eastern Thuringia, Germany. The strains grew on medium containing 1 mM NiCl2 and thus were resistant to the heavy metal ion. Seven of the strains were further characterized. All of these strains were resistant to heavy metals in various degrees with up to 10 mM resistance against NiCl2 supplied with the liquid minimal growth medium. The high level of resistance prompted us to look for high affinity nickel transporter genes thought to provide a means to eliminate the excess nickel ions form the cells. Degenerate oligonucleotide primers derived from sequences of P-type ATPase transporter genes of Gram negative bacteria identified a fragment which shows deduced amino acid sequence similarities to known high affinity nickel transporters. Investigation of two genes obtained from the isolates Streptomyces spec. E8 and F4 showed high sequence divergence. This was unexpected since a transmissible plasmid had been thought to convey heavy metal resistance.200011199488
9327100.9995Detection of the merA gene and its expression in the environment. Bacterial transformation of mercury in the environment has received much attention owing to the toxicity of both the ionic form and organomercurial compounds. Bacterial resistance to mercury and the role of bacteria in mercury cycling have been widely studied. The genes specifying the required functions for resistance to mercury are organized on the mer operon. Gene probing methodologies have been used for several years to detect specific gene sequences in the environment that are homologous to cloned mer genes. While mer genes have been detected in a wide variety of environments, less is known about the expression of these genes under environmental conditions. We combined new methodologies for recovering specific gene mRNA transcripts and mercury detection with a previously described method for determining biological potential for mercury volatilization to examine the effect of mercury concentrations and nutrient availability on rates of mercury volatilization and merA transcription. Levels of merA-specific transcripts and Hg(II) volatilization were influenced more by microbial activity (as manipulated by nutrient additions) than by the concentration of total mercury. The detection of merA-specific transcripts in some samples that did not reduce Hg(II) suggests that rates of mercury volatilization in the environment may not always be proportional to merA transcription.19968849424
443110.9995Deletion mutant analysis of the Staphylococcus aureus plasmid pI258 mercury-resistance determinant. Deletion mutant analysis of the mercury-resistant determinant (mer operon) from the Staphylococcus aureus plasmid pI258 was used to verify the location of the merA and merB genes and to show the existence of mercuric ion transport gene(s). ORF5 was confirmed to be a transport gene and has an amino acid product sequence homologous to the merT gene products from several gram-negative bacteria and a Bacillus species. Deletion analysis established that inactivation of merA on a broad-spectrum mer resistance determinant resulted in a mercury-hypersensitive phenotype. Gene dosage had no apparent effect on the level of resistance conferred by the intact mer operon or on the expression of an inducible phenotype, except that when the intact pI258 mer operon was on a high copy number plasmid, uninduced cells possessed a volatilization rate that was at most only 3.5-fold less than that observed for induced cells. There was no need for mercury ion transport proteins for full resistance when the mer operon was expressed in a high copy number plasmid.19911954576
175120.9995The acquired pco gene cluster in Salmonella enterica mediates resistance to copper. The pervasive environmental metal contamination has led to selection of heavy-metal resistance genes in bacteria. The pco and sil clusters are located on a mobile genetic element and linked to heavy-metal resistance. These clusters have been found in Salmonella enterica serovars isolated from human clinical cases and foods of animal origin. This may be due to the use of heavy metals, such as copper, in animal feed for their antimicrobial and growth promotion properties. The sil cluster can be found alone or in combination with pco cluster, either in the chromosome or on a plasmid. Previous reports have indicated that sil, but not pco, cluster contributes to copper resistance in S. enterica Typhimurium. However, the role of the pco cluster on the physiology of non-typhoidal S. enterica remains poorly understood. To understand the function of the pco gene cluster, a deletion mutant of pcoABCD genes was constructed using allelic exchange mutagenesis. Deletion of pcoABCD genes inhibited growth of S. enterica in high-copper medium, but only under anaerobic environment. Complementation of the mutant reversed the growth phenotype. The survival of S. enterica in RAW264.7 macrophages was not affected by the loss of pcoABCD genes. This study indicates that the acquired pco cluster is crucial for copper detoxification in S. enterica, but it is not essential for intracellular replication within macrophages.202439290517
6339130.9995Novel acid resistance genes from the metagenome of the Tinto River, an extremely acidic environment. Microorganisms that thrive in acidic environments are endowed with specialized molecular mechanisms to survive under this extremely harsh condition. In this work, we performed functional screening of six metagenomic libraries from planktonic and rhizosphere microbial communities of the Tinto River, an extremely acidic environment, to identify genes involved in acid resistance. This approach has revealed 15 different genes conferring acid resistance to Escherichia coli, most of which encoding putative proteins of unknown function or previously described proteins not known to be related to acid resistance. Moreover, we were able to assign function to one unknown and three hypothetical proteins. Among the recovered genes were the ClpXP protease, the transcriptional repressor LexA and nucleic acid-binding proteins such as an RNA-binding protein, HU and Dps. Furthermore, nine of the retrieved genes were cloned and expressed in Pseudomonas putida and Bacillus subtilis and, remarkably, most of them were able to expand the capability of these bacteria to survive under severe acid stress. From this set of genes, four presented a broad-host range as they enhance the acid resistance of the three different organisms tested. These results expand our knowledge about the different strategies used by microorganisms to survive under extremely acid conditions.201323145860
180140.9995Bacterial resistances to inorganic mercury salts and organomercurials. Environmental and clinical isolates of mercury-resistant (resistant to inorganic mercury salts and organomercurials) bacteria have genes for the enzymes mercuric ion reductase and organomercurial lyase. These genes are often plasmid-encoded, although chromosomally encoded resistance determinants have been occasionally identified. Organomercurial lyase cleaves the C-Hg bond and releases Hg(II) in addition to the appropriate organic compound. Mercuric reductase reduces Hg(II) to Hg(O), which is nontoxic and volatilizes from the medium. Mercuric reductase is a FAD-containing oxidoreductase and requires NAD(P)H and thiol for in vitro activity. The crystal structure of mercuric ion reductase has been partially solved. The primary sequence and the three-dimensional structure of the mercuric reductase are significantly homologous to those of other flavin-containing oxidoreductases, e.g., glutathione reductase and lipoamide dehydrogenase. The active site sequences are the most conserved region among these flavin-containing enzymes. Genes encoding other functions have been identified on all mercury ion resistance determinants studied thus far. All mercury resistance genes are clustered into an operon. Hg(II) is transported into the cell by the products of one to three genes encoded on the resistance determinants. The expression of the operon is regulated and is inducible by Hg(II). In some systems, the operon is inducible by both Hg(II) and some organomercurials. In gram-negative bacteria, two regulatory genes (merR and merD) were identified. The (merR) regulatory gene is transcribed divergently from the other genes in gram-negative bacteria. The product of merR represses operon expression in the absence of the inducers and activates transcription in the presence of the inducers. The product of merD coregulates (modulates) the expression of the operon. Both merR and merD gene products bind to the same operator DNA. The primary sequence of the promoter for the polycistronic mer operon is not ideal for efficient transcription by the RNA polymerase. The -10 and -35 sequences are separated by 19 (gram-negative systems) or 20 (gram-positive systems) nucleotides, 2 or 3 nucleotides longer than the 17-nucleotide optimum distance for binding and efficient transcription by the Escherichia coli sigma 70-containing RNA polymerase. The binding site of MerR is not altered by the presence of Hg(II) (inducer). Experimental data suggest that the MerR-Hg(II) complex alters the local structure of the promoter region, facilitating initiation of transcription of the mer operon by the RNA polymerase. In gram-positive bacteria MerR also positively regulates expression of the mer operon in the presence of Hg(II).19921311113
6188150.9995Quinolone mode of action. Physical studies have further defined interactions of quinolones with their principal target, DNA gyrase. The binding of quinolones to the DNA gyrase-DNA complex suggests 2 possible binding sites of differing affinities. Mutations in either the gyrase A gene (gyrA) or the gyrase B gene (gyrB) that affect quinolone susceptibility also affect drug binding, with resistance mutations causing decreased binding and hypersusceptibility mutations causing increased binding. Combinations of mutations in both GyrA and GyrB have further demonstrated the contribution of both subunits to the quinolone sensitivity of intact bacteria and purified DNA gyrase. A working model postulates initial binding of quinolones to proximate sites on GyrA and GyrB. This initial binding then produces conformational changes that expose additional binding sites, possibly involving DNA. Quinolones also inhibit the activities of Escherichia coli topoisomerase IV (encoded by the parC and parE genes), but at concentrations higher than those inhibiting DNA gyrase. The patterns of resistance mutations in gryA and parC suggest that topoisomerase IV may be a secondary drug target in E. coli and Neisseria gonorrhoeae. In contrast, in Staphylococcus aureus these patterns suggest that topoisomerase IV may be a primary target of quinolone action. Regulation of expression of membrane efflux transporters may contribute to quinolone susceptibility in both Gram-positive and Gram-negative bacteria. The substrate profile of the NorA efflux transporter of S. aureus correlates with the extent to which the activity of quinolone substrates is affected by overexpression of NorA. In addition, the Emr transporter of E. coli affects susceptibility to nalidixic acid, and the MexAB OprK transport system of Pseudomonas aeruginosa affects susceptibility to ciprofloxacin.(ABSTRACT TRUNCATED AT 250 WORDS)19958549276
6325160.9995Repressed multidrug resistance genes in Streptomyces lividans. Multidrug resistance (MDR) systems are ubiquitously present in prokaryotes and eukaryotes and defend both types of organisms against toxic compounds in the environment. Four families of MDR systems have been described, each family removing a broad spectrum of compounds by a specific membrane-bound active efflux pump. In the present study, at least four MDR systems were identified genetically in the soil bacterium Streptomyces lividans. The resistance genes of three of these systems were cloned and sequenced. Two of them are accompanied by a repressor gene. These MDR gene sequences are found in most other Streptomyces species investigated. Unlike the constitutively expressed MDR genes in Escherichia coli and other gram-negative bacteria, all of the Streptomyces genes were repressed under laboratory conditions, and resistance arose by mutations in the repressor genes.200312937892
173170.9995Loss of Mobile Genomic Islands in Metal-Resistant, Hydrogen-Oxidizing Cupriavidus metallidurans. The genome of the metal-resistant, hydrogen-oxidizing bacterium Cupriavidus metallidurans strain CH34 contains horizontally acquired plasmids and genomic islands. Metal-resistance determinants on the two plasmids may exert genetic dominance over other related determinants. To investigate whether these recessive determinants can be activated in the absence of the dominant ones, the transcriptome of the highly zinc-sensitive deletion mutant Δe4 (ΔcadA ΔzntA ΔdmeF ΔfieF) of the plasmid-free parent AE104 was characterized using gene arrays. As a consequence of some unexpected results, close examination by PCR and genomic resequencing of strains CH34, AE104, Δe4, and others revealed that the genomic islands CMGI2, 3, 4, D, and E, but no other islands or recessive determinants, were deleted in some of these strains. Provided that wild-type CH34 was kept under alternating zinc and nickel selection pressure, no comparable deletions occurred. All current data suggest that genes were actually deleted and were not, as surmised previously, silenced in the respective strain. As a consequence, a cured database was compiled from the newly generated and previously published gene array data. An analysis of data from this database indicated that some genes of recessive, no longer needed determinants were nevertheless expressed and upregulated. Their products may interact with those of the dominant determinants to mediate a mosaic phenotype. The ability to contribute to such a mosaic phenotype may prevent deletion of the recessive determinant. The data suggest that the bacterium actively modifies its genome to deal with metal stress and at the same time ensures metal homeostasis. IMPORTANCE In their natural environment, bacteria continually acquire genes by horizontal gene transfer, and newly acquired determinants may become dominant over related ones already present in the host genome. When a bacterium is taken into laboratory culture, it is isolated from the horizontal gene transfer network. It can no longer gain genes but instead may lose them. This phenomenon was indeed observed in Cupriavidus metallidurans for the loss key metal resistance determinants when no selection pressure was kept continuously. However, some recessive metal resistance determinants were maintained in the genome. It is proposed that they might contribute some accessory genes to related dominant resistance determinants, for instance periplasmic metal-binding proteins or two-component regulatory systems. Alternatively, they may remain in the genome only because their DNA serves as a scaffold for the nucleoid. Using C. metallidurans as an example, this study sheds light on the fate and function of horizontally acquired genes in bacteria.202234910578
8218180.9995Mechanism of plasmic-mediated resistance to cadmium in Staphylococcus aureus. The mechanism of plasmid-mediated resistance to cadmium in Staphylococcus aureus was investigated. Protein synthesis in cell-free extracts from resistant or susceptible bacteria was equally susceptible to inhibition by Cd(2+), but spheroplasts from resistant bacteria retained their resistance. Resistant bacteria did not have a decreased affinity for cations in general, nor was active metabolism required for exclusion of Cd(2+). The kinetics of Cd(2+) uptake into susceptible and resistant bacteria suggested that the conformation of membrane proteins in resistant bacteria may be important in the exclusion of Cd(2+).19751137361
8686190.9995Improving Cadmium Resistance in Escherichia coli Through Continuous Genome Evolution. Cadmium (Cd) is a heavy metal that is extremely toxic to many organisms; however, microbes are highly adaptable to extreme conditions, including heavy metal contamination. Bacteria can evolve in the natural environment, generating resistant strains that can be studied to understand heavy-metal resistance mechanisms, but obtaining such adaptive strains usually takes a long time. In this study, the genome replication engineering assisted continuous evolution (GREACE) method was used to accelerate the evolutionary rate of the Escherichia coli genome to screen for E. coli mutants with high resistance to cadmium. As a result, a mutant (8mM-CRAA) with a minimum inhibitory concentration (MIC) of 8 mM cadmium was generated; this MIC value was approximately eightfold higher than that of the E. coli BL21(DE3) wild-type strain. Sequencing revealed 329 single nucleotide polymorphisms (SNPs) in the genome of the E. coli mutant 8mM-CRAA. These SNPs as well as RNA-Seq data on gene expression induced by cadmium were used to analyze the genes related to cadmium resistance. Overexpression, knockout and mutation of the htpX (which encodes an integral membrane heat shock protein) and gor (which encodes glutathione reductase) genes revealed that these two genes contribute positively to cadmium resistance in E. coli. Therefore, in addition to the previously identified cadmium resistance genes zntA and capB, many other genes are also involved in bacterial cadmium resistance. This study assists us in understanding the mechanism of microbial cadmium resistance and facilitating the application of heavy-metal remediation.201930842762