Special Issue "Genomics of Bacterial Metal Resistance"

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Microbial Genetics and Genomics".

Deadline for manuscript submissions: closed (30 September 2018).

Special Issue Editors

Prof. Dr. Alessio Mengoni
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Guest Editor
Department of Biology, University of Florence, Italy
Interests: nitrogen-fixing symbiosis; serpentine soils, microbiome of metal hyperaccumulating plants
Special Issues and Collections in MDPI journals
Prof. Carlo Viti
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Guest Editor
Department of Agriculture, Food, Environment and Forestry, University of Florence, Florence, Italy
Interests: microbial ecology; metagenomics; phenomics
Special Issues and Collections in MDPI journals
Prof. Dr. Raymond J. Turner
E-Mail Website
Guest Editor
Department of Biological Sciences, University of Calgary, Calgary, AB T2N 1N4, Canada
Interests: bacteria; system response to metals; metal ions; biofilms; toxicity; antimicrobial properties; bioremediation; metal nanomaterials
Special Issues and Collections in MDPI journals
Prof. Li-Nan Huang
E-Mail
Guest Editor
Sun Yat-Sen University, Guangzhou, P.R. China

Special Issue Information

Dear Colleagues,

Bacteria develop metal resistance in a variety of environments, both natural and anthropogenic. Metal resistant bacteria are routinely isolated from natural metal ion rich environments as well as metal polluted sites from mining/refining/manufacturing operations. Additionally, we now recognize an increased metal load from our dense city populations leading to high metal accumulation in water treatment plants. Further there is now an increased use of metal-based antimicrobials to help with solutions to the antimicrobial resistance era threats.  All these metal load situations lead to bacteria evolving metal resistance.  Metal ion resistance may be through specific gene(s) or operon(s) evolved for resistance towards a specific metal.  Or the resistance may be due to a combination of genes expressed uniquely that leads to a physiology of either specific or multimetal resistance. Additionally, evolving metal resistance may also lead to develop antibiotic resistance. Finally, bacterial communities of heavy-metal contaminated sites are also important examples of evolution and adaptation of biotic communities and a source of biotechnologically relevant strains.

Here, we are recognizing the important field of bacterial metal resistance through a targeted Special Issue on genomics.

We kindly invite researchers working on any of these areas to submit their original research or review articles to this Special Issue.

Prof. Alessio Mengoni
Prof. Carlo Viti
Prof. Raymond J. Turner
Prof. Li-Nan Huang
Guest Editors

Manuscript Submission Information

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Genes is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 1800 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • pangenome
  • genomic islands
  • heavy metals
  • metalloids
  • metal resistance genes
  • metal stress genes
  • metal response
  • metal gene prevalence
  • biofilm
  • metagenomics
  • microbiome
  • serpentine
  • mining
  • bioremediation

Published Papers (12 papers)

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Research

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Open AccessArticle
Genomic and Transcriptomic Changes That Mediate Increased Platinum Resistance in Cupriavidus metallidurans
Genes 2019, 10(1), 63; https://doi.org/10.3390/genes10010063 - 18 Jan 2019
Cited by 1
Abstract
The extensive anthropogenic use of platinum, a rare element found in low natural abundance in the Earth’s continental crust and one of the critical raw materials in the EU innovation partnership framework, has resulted in increased concentrations in surface environments. To minimize its [...] Read more.
The extensive anthropogenic use of platinum, a rare element found in low natural abundance in the Earth’s continental crust and one of the critical raw materials in the EU innovation partnership framework, has resulted in increased concentrations in surface environments. To minimize its spread and increase its recovery from the environment, biological recovery via different microbial systems is explored. In contrast, studies focusing on the effects of prolonged exposure to Pt are limited. In this study, we used the metal-resistant Cupriavidus metallidurans NA4 strain to explore the adaptation of environmental bacteria to platinum exposure. We used a combined Nanopore–Illumina sequencing approach to fully resolve all six replicons of the C. metallidurans NA4 genome, and compared them with the C. metallidurans CH34 genome, revealing an important role in metal resistance for its chromid rather than its megaplasmids. In addition, we identified the genomic and transcriptomic changes in a laboratory-evolved strain, displaying resistance to 160 µM Pt4+. The latter carried 20 mutations, including a large 69.9 kb deletion in its plasmid pNA4_D (89.6 kb in size), and 226 differentially-expressed genes compared to its parental strain. Many membrane-related processes were affected, including up-regulation of cytochrome c and a lytic transglycosylase, down-regulation of flagellar and pili-related genes, and loss of the pNA4_D conjugative machinery, pointing towards a significant role in the adaptation to platinum. Full article
(This article belongs to the Special Issue Genomics of Bacterial Metal Resistance)
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Open AccessArticle
Using a Chemical Genetic Screen to Enhance Our Understanding of the Antimicrobial Properties of Gallium against Escherichia coli
Genes 2019, 10(1), 34; https://doi.org/10.3390/genes10010034 - 09 Jan 2019
Cited by 1
Abstract
The diagnostic and therapeutic agent gallium offers multiple clinical and commercial uses including the treatment of cancer and the localization of tumors, among others. Further, this metal has been proven to be an effective antimicrobial agent against a number of microbes. Despite the [...] Read more.
The diagnostic and therapeutic agent gallium offers multiple clinical and commercial uses including the treatment of cancer and the localization of tumors, among others. Further, this metal has been proven to be an effective antimicrobial agent against a number of microbes. Despite the latter, the fundamental mechanisms of gallium action have yet to be fully identified and understood. To further the development of this antimicrobial, it is imperative that we understand the mechanisms by which gallium interacts with cells. As a result, we screened the Escherichia coli Keio mutant collection as a means of identifying the genes that are implicated in prolonged gallium toxicity or resistance and mapped their biological processes to their respective cellular system. We discovered that the deletion of genes functioning in response to oxidative stress, DNA or iron–sulfur cluster repair, and nucleotide biosynthesis were sensitive to gallium, while Ga resistance comprised of genes involved in iron/siderophore import, amino acid biosynthesis and cell envelope maintenance. Altogether, our explanations of these findings offer further insight into the mechanisms of gallium toxicity and resistance in E. coli. Full article
(This article belongs to the Special Issue Genomics of Bacterial Metal Resistance)
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Open AccessArticle
Genomic Islands Confer Heavy Metal Resistance in Mucilaginibacter kameinonensis and Mucilaginibacter rubeus Isolated from a Gold/Copper Mine
Genes 2018, 9(12), 573; https://doi.org/10.3390/genes9120573 - 23 Nov 2018
Abstract
Heavy metals (HMs) are compounds that can be hazardous and impair growth of living organisms. Bacteria have evolved the capability not only to cope with heavy metals but also to detoxify polluted environments. Three heavy metal-resistant strains of Mucilaginibacer rubeus and one of [...] Read more.
Heavy metals (HMs) are compounds that can be hazardous and impair growth of living organisms. Bacteria have evolved the capability not only to cope with heavy metals but also to detoxify polluted environments. Three heavy metal-resistant strains of Mucilaginibacer rubeus and one of Mucilaginibacter kameinonensis were isolated from the gold/copper Zijin mining site, Longyan, Fujian, China. These strains were shown to exhibit high resistance to heavy metals with minimal inhibitory concentration reaching up to 3.5 mM Cu(II), 21 mM Zn(II), 1.2 mM Cd(II), and 10.0 mM As(III). Genomes of the four strains were sequenced by Illumina. Sequence analyses revealed the presence of a high abundance of heavy metal resistance (HMR) determinants. One of the strain, M. rubeus P2, carried genes encoding 6 putative PIB-1-ATPase, 5 putative PIB-3-ATPase, 4 putative Zn(II)/Cd(II) PIB-4 type ATPase, and 16 putative resistance-nodulation-division (RND)-type metal transporter systems. Moreover, the four genomes contained a high abundance of genes coding for putative metal binding chaperones. Analysis of the close vicinity of these HMR determinants uncovered the presence of clusters of genes potentially associated with mobile genetic elements. These loci included genes coding for tyrosine recombinases (integrases) and subunits of mating pore (type 4 secretion system), respectively allowing integration/excision and conjugative transfer of numerous genomic islands. Further in silico analyses revealed that their genetic organization and gene products resemble the Bacteroides integrative and conjugative element CTnDOT. These results highlight the pivotal role of genomic islands in the acquisition and dissemination of adaptive traits, allowing for rapid adaption of bacteria and colonization of hostile environments. Full article
(This article belongs to the Special Issue Genomics of Bacterial Metal Resistance)
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Open AccessArticle
Unintentional Genomic Changes Endow Cupriavidus metallidurans with an Augmented Heavy-Metal Resistance
Genes 2018, 9(11), 551; https://doi.org/10.3390/genes9110551 - 13 Nov 2018
Cited by 1
Abstract
For the past three decades, Cupriavidus metallidurans has been one of the major model organisms for bacterial tolerance to heavy metals. Its type strain CH34 contains at least 24 gene clusters distributed over four replicons, allowing for intricate and multilayered metal responses. To [...] Read more.
For the past three decades, Cupriavidus metallidurans has been one of the major model organisms for bacterial tolerance to heavy metals. Its type strain CH34 contains at least 24 gene clusters distributed over four replicons, allowing for intricate and multilayered metal responses. To gain organic mercury resistance in CH34, broad-spectrum mer genes were introduced in a previous work via conjugation of the IncP-1β plasmid pTP6. However, we recently noted that this CH34-derived strain, MSR33, unexpectedly showed an increased resistance to other metals (i.e., Co2+, Ni2+, and Cd2+). To thoroughly investigate this phenomenon, we resequenced the entire genome of MSR33 and compared its DNA sequence and basal gene expression profile to those of its parental strain CH34. Genome comparison identified 11 insertions or deletions (INDELs) and nine single nucleotide polymorphisms (SNPs), whereas transcriptomic analysis displayed 107 differentially expressed genes. Sequence data implicated the transposition of IS1088 in higher Co2+ and Ni2+ resistances and altered gene expression, although the precise mechanisms of the augmented Cd2+ resistance in MSR33 remains elusive. Our work indicates that conjugation procedures involving large complex genomes and extensive mobilomes may pose a considerable risk toward the introduction of unwanted, undocumented genetic changes. Special efforts are needed for the applied use and further development of small nonconjugative broad-host plasmid vectors, ideally involving CRISPR-related and advanced biosynthetic technologies. Full article
(This article belongs to the Special Issue Genomics of Bacterial Metal Resistance)
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Open AccessArticle
Cupriavidus metallidurans Strains with Different Mobilomes and from Distinct Environments Have Comparable Phenomes
Genes 2018, 9(10), 507; https://doi.org/10.3390/genes9100507 - 18 Oct 2018
Cited by 1
Abstract
Cupriavidus metallidurans has been mostly studied because of its resistance to numerous heavy metals and is increasingly being recovered from other environments not typified by metal contamination. They host a large and diverse mobile gene pool, next to their native megaplasmids. Here, we [...] Read more.
Cupriavidus metallidurans has been mostly studied because of its resistance to numerous heavy metals and is increasingly being recovered from other environments not typified by metal contamination. They host a large and diverse mobile gene pool, next to their native megaplasmids. Here, we used comparative genomics and global metabolic comparison to assess the impact of the mobilome on growth capabilities, nutrient utilization, and sensitivity to chemicals of type strain CH34 and three isolates (NA1, NA4 and H1130). The latter were isolated from water sources aboard the International Space Station (NA1 and NA4) and from an invasive human infection (H1130). The mobilome was expanded as prophages were predicted in NA4 and H1130, and a genomic island putatively involved in abietane diterpenoids metabolism was identified in H1130. An active CRISPR-Cas system was identified in strain NA4, providing immunity to a plasmid that integrated in CH34 and NA1. No correlation between the mobilome and isolation environment was found. In addition, our comparison indicated that the metal resistance determinants and properties are conserved among these strains and thus maintained in these environments. Furthermore, all strains were highly resistant to a wide variety of chemicals, much broader than metals. Only minor differences were observed in the phenomes (measured by phenotype microarrays), despite the large difference in mobilomes and the variable (shared by two or three strains) and strain-specific genomes. Full article
(This article belongs to the Special Issue Genomics of Bacterial Metal Resistance)
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Open AccessArticle
Distribution of the pco Gene Cluster and Associated Genetic Determinants among Swine Escherichia coli from a Controlled Feeding Trial
Genes 2018, 9(10), 504; https://doi.org/10.3390/genes9100504 - 18 Oct 2018
Cited by 1
Abstract
Copper is used as an alternative to antibiotics for growth promotion and disease prevention. However, bacteria developed tolerance mechanisms for elevated copper concentrations, including those encoded by the pco operon in Gram-negative bacteria. Using cohorts of weaned piglets, this study showed that the [...] Read more.
Copper is used as an alternative to antibiotics for growth promotion and disease prevention. However, bacteria developed tolerance mechanisms for elevated copper concentrations, including those encoded by the pco operon in Gram-negative bacteria. Using cohorts of weaned piglets, this study showed that the supplementation of feed with copper concentrations as used in the field did not result in a significant short-term increase in the proportion of pco-positive fecal Escherichia coli. The pco and sil (silver resistance) operons were found concurrently in all screened isolates, and whole-genome sequencing showed that they were distributed among a diversity of unrelated E. coli strains. The presence of pco/sil in E. coli was not associated with elevated copper minimal inhibitory concentrations (MICs) under a variety of conditions. As found in previous studies, the pco/sil operons were part of a Tn7-like structure found both on the chromosome or on plasmids in the E. coli strains investigated. Transfer of a pco/sil IncHI2 plasmid from E. coli to Salmonella enterica resulted in elevated copper MICs in the latter. Escherichia coli may represent a reservoir of pco/sil genes transferable to other organisms such as S. enterica, for which it may represent an advantage in the presence of copper. This, in turn, has the potential for co-selection of resistance to antibiotics. Full article
(This article belongs to the Special Issue Genomics of Bacterial Metal Resistance)
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Open AccessArticle
Genomic and Biotechnological Characterization of the Heavy-Metal Resistant, Arsenic-Oxidizing Bacterium Ensifer sp. M14
Genes 2018, 9(8), 379; https://doi.org/10.3390/genes9080379 - 27 Jul 2018
Cited by 2
Abstract
Ensifer (Sinorhizobium) sp. M14 is an efficient arsenic-oxidizing bacterium (AOB) that displays high resistance to numerous metals and various stressors. Here, we report the draft genome sequence and genome-guided characterization of Ensifer sp. M14, and we describe a pilot-scale installation applying [...] Read more.
Ensifer (Sinorhizobium) sp. M14 is an efficient arsenic-oxidizing bacterium (AOB) that displays high resistance to numerous metals and various stressors. Here, we report the draft genome sequence and genome-guided characterization of Ensifer sp. M14, and we describe a pilot-scale installation applying the M14 strain for remediation of arsenic-contaminated waters. The M14 genome contains 6874 protein coding sequences, including hundreds not found in related strains. Nearly all unique genes that are associated with metal resistance and arsenic oxidation are localized within the pSinA and pSinB megaplasmids. Comparative genomics revealed that multiple copies of high-affinity phosphate transport systems are common in AOBs, possibly as an As-resistance mechanism. Genome and antibiotic sensitivity analyses further suggested that the use of Ensifer sp. M14 in biotechnology does not pose serious biosafety risks. Therefore, a novel two-stage installation for remediation of arsenic-contaminated waters was developed. It consists of a microbiological module, where M14 oxidizes As(III) to As(V) ion, followed by an adsorption module for As(V) removal using granulated bog iron ores. During a 40-day pilot-scale test in an abandoned gold mine in Zloty Stok (Poland), water leaving the microbiological module generally contained trace amounts of As(III), and dramatic decreases in total arsenic concentrations were observed after passage through the adsorption module. These results demonstrate the usefulness of Ensifer sp. M14 in arsenic removal performed in environmental settings. Full article
(This article belongs to the Special Issue Genomics of Bacterial Metal Resistance)
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Open AccessArticle
Integrase-Controlled Excision of Metal-Resistance Genomic Islands in Acinetobacter baumannii
Genes 2018, 9(7), 366; https://doi.org/10.3390/genes9070366 - 20 Jul 2018
Cited by 1
Abstract
Genomic islands (GIs) are discrete gene clusters encoding for a variety of functions including antibiotic and heavy metal resistance, some of which are tightly associated to lineages of the core genome phylogenetic tree. We have investigated the functions of two distinct integrase genes [...] Read more.
Genomic islands (GIs) are discrete gene clusters encoding for a variety of functions including antibiotic and heavy metal resistance, some of which are tightly associated to lineages of the core genome phylogenetic tree. We have investigated the functions of two distinct integrase genes in the mobilization of two metal resistant GIs, G08 and G62, of Acinetobacter baumannii. Real-time PCR demonstrated integrase-dependent GI excision, utilizing isopropyl β-d-1-thiogalactopyranoside IPTG-inducible integrase genes in plasmid-based mini-GIs in Escherichia coli. In A. baumannii, integrase-dependent excision of the original chromosomal GIs could be observed after mitomycin C induction. In both E. coli plasmids and A. baumannii chromosome, the rate of excision and circularization was found to be dependent on the expression level of the integrases. Susceptibility testing in A. baumannii strain ATCC 17978, A424, and their respective ΔG62 and ΔG08 mutants confirmed the contribution of the GI-encoded efflux transporters to heavy metal decreased susceptibility. In summary, the data evidenced the functionality of two integrases in the excision and circularization of the two Acinetobacter heavy-metal resistance GIs, G08 and G62, in E. coli, as well as when chromosomally located in their natural host. These recombination events occur at different frequencies resulting in genome plasticity and may participate in the spread of resistance determinants in A. baumannii. Full article
(This article belongs to the Special Issue Genomics of Bacterial Metal Resistance)
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Open AccessFeature PaperArticle
Possible Role of Envelope Components in the Extreme Copper Resistance of the Biomining Acidithiobacillus ferrooxidans
Genes 2018, 9(7), 347; https://doi.org/10.3390/genes9070347 - 10 Jul 2018
Cited by 3
Abstract
Acidithiobacillus ferrooxidans resists extremely high concentrations of copper. Strain ATCC 53993 is much more resistant to the metal compared with strain ATCC 23270, possibly due to the presence of a genomic island in the former one. The global response of strain ATCC 53993 [...] Read more.
Acidithiobacillus ferrooxidans resists extremely high concentrations of copper. Strain ATCC 53993 is much more resistant to the metal compared with strain ATCC 23270, possibly due to the presence of a genomic island in the former one. The global response of strain ATCC 53993 to copper was analyzed using iTRAQ (isobaric tag for relative and absolute quantitation) quantitative proteomics. Sixty-seven proteins changed their levels of synthesis in the presence of the metal. On addition of CusCBA efflux system proteins, increased levels of other envelope proteins, such as a putative periplasmic glucan biosynthesis protein (MdoG) involved in the osmoregulated synthesis of glucans and a putative antigen O polymerase (Wzy), were seen in the presence of copper. The expression of A. ferrooxidansmdoG or wzy genes in a copper sensitive Escherichia coli conferred it a higher metal resistance, suggesting the possible role of these components in copper resistance of A. ferrooxidans. Transcriptional levels of genes wzy, rfaE and wzz also increased in strain ATCC 23270 grown in the presence of copper, but not in strain ATCC 53993. Additionally, in the absence of this metal, lipopolysaccharide (LPS) amounts were 3-fold higher in A. ferrooxidans ATCC 53993 compared with strain 23270. Nevertheless, both strains grown in the presence of copper contained similar LPS quantities, suggesting that strain 23270 synthesizes higher amounts of LPS to resist the metal. On the other hand, several porins diminished their levels in the presence of copper. The data presented here point to an essential role for several envelope components in the extreme copper resistance by this industrially important acidophilic bacterium. Full article
(This article belongs to the Special Issue Genomics of Bacterial Metal Resistance)
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Open AccessFeature PaperArticle
Using a Chemical Genetic Screen to Enhance Our Understanding of the Antibacterial Properties of Silver
Genes 2018, 9(7), 344; https://doi.org/10.3390/genes9070344 - 06 Jul 2018
Cited by 7
Abstract
It is essential to understand the mechanisms by which a toxicant is capable of poisoning the bacterial cell. The mechanism of action of many biocides and toxins, including numerous ubiquitous compounds, is not fully understood. For example, despite the widespread clinical and commercial [...] Read more.
It is essential to understand the mechanisms by which a toxicant is capable of poisoning the bacterial cell. The mechanism of action of many biocides and toxins, including numerous ubiquitous compounds, is not fully understood. For example, despite the widespread clinical and commercial use of silver (Ag), the mechanisms describing how this metal poisons bacterial cells remains incomplete. To advance our understanding surrounding the antimicrobial action of Ag, we performed a chemical genetic screen of a mutant library of Escherichia coli—the Keio collection, in order to identify Ag sensitive or resistant deletion strains. Indeed, our findings corroborate many previously established mechanisms that describe the antibacterial effects of Ag, such as the disruption of iron-sulfur clusters containing proteins and certain cellular redox enzymes. However, the data presented here demonstrates that the activity of Ag within the bacterial cell is more extensive, encompassing genes involved in cell wall maintenance, quinone metabolism and sulfur assimilation. Altogether, this study provides further insight into the antimicrobial mechanism of Ag and the physiological adaption of E. coli to this metal. Full article
(This article belongs to the Special Issue Genomics of Bacterial Metal Resistance)
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Review

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Open AccessReview
Heavy Metal Resistance Determinants of the Foodborne Pathogen Listeria monocytogenes
Genes 2019, 10(1), 11; https://doi.org/10.3390/genes10010011 - 24 Dec 2018
Cited by 1
Abstract
Listeria monocytogenes is ubiquitous in the environment and causes the disease listeriosis. Metal homeostasis is one of the key processes utilized by L. monocytogenes in its role as either a saprophyte or pathogen. In the environment, as well as within an animal host, [...] Read more.
Listeria monocytogenes is ubiquitous in the environment and causes the disease listeriosis. Metal homeostasis is one of the key processes utilized by L. monocytogenes in its role as either a saprophyte or pathogen. In the environment, as well as within an animal host, L. monocytogenes needs to both acquire essential metals and mitigate toxic levels of metals. While the mechanisms associated with acquisition and detoxification of essential metals such as copper, iron, and zinc have been extensively studied and recently reviewed, a review of the mechanisms associated with non-essential heavy metals such as arsenic and cadmium is lacking. Resistance to both cadmium and arsenic is frequently encountered in L. monocytogenes, including isolates from human listeriosis. In addition, a growing body of work indicates the association of these determinants with other cellular functions such as virulence, suggesting the importance of further study in this area. Full article
(This article belongs to the Special Issue Genomics of Bacterial Metal Resistance)
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Open AccessReview
Harnessing Rhizobia to Improve Heavy-Metal Phytoremediation by Legumes
Genes 2018, 9(11), 542; https://doi.org/10.3390/genes9110542 - 08 Nov 2018
Cited by 3
Abstract
Rhizobia are bacteria that can form symbiotic associations with plants of the Fabaceae family, during which they reduce atmospheric di-nitrogen to ammonia. The symbiosis between rhizobia and leguminous plants is a fundamental contributor to nitrogen cycling in natural and agricultural ecosystems. Rhizobial microsymbionts [...] Read more.
Rhizobia are bacteria that can form symbiotic associations with plants of the Fabaceae family, during which they reduce atmospheric di-nitrogen to ammonia. The symbiosis between rhizobia and leguminous plants is a fundamental contributor to nitrogen cycling in natural and agricultural ecosystems. Rhizobial microsymbionts are a major reason why legumes can colonize marginal lands and nitrogen-deficient soils. Several leguminous species have been found in metal-contaminated areas, and they often harbor metal-tolerant rhizobia. In recent years, there have been numerous efforts and discoveries related to the genetic determinants of metal resistance by rhizobia, and on the effectiveness of such rhizobia to increase the metal tolerance of host plants. Here, we review the main findings on the metal resistance of rhizobia: the physiological role, evolution, and genetic determinants, and the potential to use native and genetically-manipulated rhizobia as inoculants for legumes in phytoremediation practices. Full article
(This article belongs to the Special Issue Genomics of Bacterial Metal Resistance)
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