Most cited article - PubMed ID 27483244
Effects of Secondary Plant Metabolites on Microbial Populations: Changes in Community Structure and Metabolic Activity in Contaminated Environments
Potentially toxic element (PTE) contamination deteriorates agricultural land. This study explored the accumulation of excess PTEs (Cd, Pb, and Zn) in soils by shoots of herbaceous plants growing on alluvial sediments of an abandoned mining/smelting site near the Litavka River, Czech Republic, as a means of soil remediation. Determination of total Cd, Pb, and Zn, contents in soil and plant samples decomposed with HNO3 + HCl + HF, HNO3, and H2O2, respectively, were carried out by inductively coupled optical emission spectrometry. The soil Cd, Pb, and Zn contents in the studied site ranged from 40 to 65, 3183 to 3897, and 5108 to 6553 mg kg-1, respectively, indicating serious soil contamination compared to the limits allowed by the FAO/WHO and the Czech Republic. Slightly acidic soil reactions and negative correlations between the pH, C, and N supported the assumption of relative solubility, mobility, and accumulation of studied PTEs by herbaceous species. Shoot accumulation of Cd, Pb, and Zn varied in 22 of 23 species recording a Cd content above the permissible limit. The Zn content in all plants was above the WHO limit. Except for Arabidopsis halleri, with a bioaccumulation factor (BAFshoot) > 1 for Cd and Zn, Equisetum arvense recorded a comparatively higher Cd content (10.3-28 mg kg-1) than all other species. Silene vulgaris (Moench), Leucanthemum vulgare, E. arvense, Achillea millefolium, Carex sp., Dianthus deltoides, Campanula patula, Plantago lanceolata, and Rumex acetosa accumulated more Zn than many plants (> 300 mg kg-1). Although E. arvense had a BAF < 1, it accumulated > 1000 mg Zn kg-1 and supported the phytoextraction of Zn. Only 10 species accumulated Pb above the limit permissible in plants, with L. vulgare recording the highest concentration (40 mg kg-1) among all species. Therefore, the shoots of several plant species showed promising PTE accumulation abilities and deserve more detailed studies concerning their potential use for phytoremediation of Cd-, Pb-, or Zn-contaminated soils.
- Keywords
- Equisetum arvense, Leucanthemum vulgare, Alluvial sediment, Phytoextraction, Phytoremediation, Shoot accumulation,
- MeSH
- Biodegradation, Environmental MeSH
- Mining MeSH
- Cadmium metabolism MeSH
- Soil Pollutants * metabolism MeSH
- Lead metabolism MeSH
- Soil chemistry MeSH
- Plants * metabolism MeSH
- Zinc metabolism MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Czech Republic MeSH
- Names of Substances
- Cadmium MeSH
- Soil Pollutants * MeSH
- Lead MeSH
- Soil MeSH
- Zinc MeSH
Aromatic ring-hydroxylating dioxygenases (ARHDs) play a crucial role in the aerobic biodegradation of both natural and anthropogenic aromatic compounds. Although their ability to process contaminants is not entirely understood, it is thought to have evolved from the transformation of structurally similar secondary plant metabolites (SPMs). Hence, to investigate this connection, we tested a variety of SPMs from the monoterpene and flavonoid classes as carbon sources and transcriptional effectors of several phylogenetically distant ARHD genes involved in the degradation of aromatic pollutants. Specifically, we focused on bphA1, nahA1 and phtA1 in Rhodococcus opacus C1, whose genomic analysis is also presented hereinafter, and bphA1a, nahA1-bphA1b and etbA1ab in Rhodococcus sp. WAY2. Whilst induction was only observed with (R)-carvone for bphA1a and nahA1-bphA1b of strain WAY2, and with p-cymene for nahA1 and nahA1-bphA1b of strains C1 and WAY2, respectively, an extensive inhibition by flavonoids was observed for most of the genes in both strains. To the best of our knowledge, our study is the first to report the effect of flavonoids and monoterpenes on the transcription of nahA1, etbA1 and phtA1 genes. In addition, we show that, in contrast to pseudomonads, many flavonoids inhibit the transcription of the ARHD genes in rhodococci. Thus, our work provides a new perspective on flavonoids as the transcriptional effectors of ARHDs, highlighting the significant variability of these enzymes and the divergent responses that they elicit. Moreover, our results contribute to understanding the complex interactions between microorganisms and SPMs and provide insights into the molecular basis of a number of them.
- Keywords
- Rhodococcus, aromatic pollutants, aromatic ring-hydroxylating dioxygenases, biodegradation, flavonoids, monoterpenes,
- MeSH
- Bacterial Proteins genetics metabolism MeSH
- Biodegradation, Environmental MeSH
- Dioxygenases * genetics metabolism MeSH
- Flavonoids * pharmacology metabolism MeSH
- Phylogeny MeSH
- Transcription, Genetic drug effects MeSH
- Monoterpenes * pharmacology metabolism MeSH
- Gene Expression Regulation, Bacterial drug effects MeSH
- Rhodococcus * genetics drug effects enzymology metabolism MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Bacterial Proteins MeSH
- Dioxygenases * MeSH
- Flavonoids * MeSH
- Monoterpenes * MeSH
Polychlorinated biphenyl (PCB)-contaminated soils represent a major treat for ecosystems health. Plant biostimulation of autochthonous microbial PCB degraders is a way to restore polluted sites where traditional remediation techniques are not sustainable, though its success requires the understanding of site-specific plant-microbe interactions. In an historical PCB contaminated soil, we applied DNA stable isotope probing (SIP) using 13C-labeled 4-chlorobiphenyl (4-CB) and 16S rRNA MiSeq amplicon sequencing to determine how the structure of total and PCB-degrading bacterial populations were affected by different treatments: biostimulation with Phalaris arundinacea subjected (PhalRed) or not (Phal) to a redox cycle and the non-planted controls (Bulk and BulkRed). Phal soils hosted the most diverse community and plant biostimulation induced an enrichment of Actinobacteria. Mineralization of 4-CB in SIP microcosms varied between 10% in Bulk and 39% in PhalRed soil. The most abundant taxa deriving carbon from PCB were Betaproteobacteria and Actinobacteria. Comamonadaceae was the family most represented in Phal soils, Rhodocyclaceae and Nocardiaceae in non-planted soils. Planted soils subjected to redox cycle enriched PCB degraders affiliated to Pseudonocardiaceae, Micromonosporaceae and Nocardioidaceae. Overall, we demonstrated different responses of soil bacterial taxa to specific rhizoremediation treatments and we provided new insights into the populations active in PCB biodegradation.
- MeSH
- Actinomycetales * genetics MeSH
- Bacteria MeSH
- Biodegradation, Environmental MeSH
- DNA, Bacterial genetics metabolism MeSH
- DNA metabolism MeSH
- Ecosystem MeSH
- Isotopes metabolism MeSH
- Soil Pollutants * metabolism MeSH
- Polychlorinated Biphenyls * metabolism MeSH
- Soil chemistry MeSH
- Soil Microbiology MeSH
- RNA, Ribosomal, 16S genetics metabolism MeSH
- Plants metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- DNA, Bacterial MeSH
- DNA MeSH
- Isotopes MeSH
- Soil Pollutants * MeSH
- Polychlorinated Biphenyls * MeSH
- Soil MeSH
- RNA, Ribosomal, 16S MeSH
The involvement of bacterial aromatic ring-hydroxylating dioxygenases (ARHDs) in the degradation of aromatic pollutants, such as polychlorinated biphenyls (PCBs), has been well studied. However, there is considerable speculation as to the origin of this ability. One hypothesis is centered on a connection between the ability to degrade aromatic pollutants and the necessity of soil bacteria to cope with and/or utilize secondary plant metabolites (SPMs). To investigate this connection, we researched the involvement of biphenyl 2,3-dioxygenase (BPDO), an ARHD essential for the degradation of PCBs, in the metabolism of SPMs in the soil bacterium Pseudomonas alcaliphila JAB1, a versatile degrader of PCBs. We demonstrated the ability of the strain JAB1 to transform a variety of SPMs, namely the flavonoids apigenin, flavone, flavanone, naringenin, fisetin, quercetin, morin, and catechin, caffeic acid, trans-cinnamic acid, and the monoterpenes (S)-limonene and (R)-carvone. Of those, the transformation of flavone, flavanone, and (S)-limonene was conditioned by the activity of JAB1-borne BPDO and thus was researched in more detail, and we found evidence for the limonene monooxygenase activity of the BPDO. Furthermore, the bphA gene in the strain JAB1 was demonstrated to be induced by a wide range of SPMs, with monoterpenes being the strongest inducers of the SPMs tested. Thus, our findings contribute to the growing body of evidence that ARHDs not only play a role in the catabolism of aromatic pollutants, but also of natural plant-derived aromatics, and this study supports the hypothesis that ARHDs participate in ecological processes mediated by SPMs.
- Keywords
- aromatic ring-hydroxylating dioxygenases, biphenyl dioxygenase, monoterpenes, phenolics, secondary plant metabolites,
- Publication type
- Journal Article MeSH
Certain industrial chemicals accumulate in the environment due to their recalcitrant properties. Bioremediation uses the capability of some environmental bacteria to break down these chemicals and attenuate the pollution. One such bacterial strain, designated Pvy, was isolated from sediment samples from a lagoon in Romania located near an oil refinery due to its capacity to degrade dibenzofuran (DF). The genome sequence of the Pvy strain was obtained using an Oxford Nanopore MiniION platform. According to the consensus 16S rRNA gene sequence that was compiled from six 16S rRNA gene copies contained in the genome and orthologous average nucleotide identity (OrthoANI) calculation, the Pvy strain was identified as Pseudomonas veronii, which confirmed the identification obtained with the aid of MALDI-TOF mass spectrometry and MALDI BioTyper. The genome was analyzed with respect to enzymes responsible for the overall biodegradative versatility of the strain. The Pvy strain was able to derive carbon from naphthalene (NP) and several aromatic compounds of natural origin, including salicylic, protocatechuic, p-hydroxybenzoic, trans-cinnamic, vanillic, and indoleacetic acids or vanillin, and was shown to degrade but not utilize DF. In total seven loci were found in the Pvy genome, which enables the strain to participate in the degradation of these aromatic compounds. Our experimental data also indicate that the transcription of the NP-dioxygenase α-subunit gene (ndoB), carried by the plasmid of the Pvy strain, is inducible by DF. These features make the Pvy strain a potential candidate for various bioremediation applications.
- Keywords
- Pseudomonas veronii strain Pvy, biodegradation, denitrification, dibenzofuran, dioxygenase, heavy-metal tolerance, nanopore technology, organic phosphate mineralization, whole-genome sequencing,
- MeSH
- Biodegradation, Environmental MeSH
- Dibenzofurans * MeSH
- Genomics * MeSH
- Pseudomonas MeSH
- RNA, Ribosomal, 16S MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Dibenzofurans * MeSH
- RNA, Ribosomal, 16S MeSH
Extended soil contamination by polychlorinated biphenyls (PCBs) represents a global environmental issue that can hardly be addressed with the conventional remediation treatments. Rhizoremediation is a sustainable alternative, exploiting plants to stimulate in situ the degradative bacterial communities naturally occurring in historically polluted areas. This approach can be enhanced by the use of bacterial strains that combine PCB degradation potential with the ability to promote plant and root development. With this aim, we established a collection of aerobic bacteria isolated from the soil of the highly PCB-polluted site "SIN Brescia-Caffaro" (Italy) biostimulated by the plant Phalaris arundinacea. The strains, selected on biphenyl and plant secondary metabolites provided as unique carbon source, were largely dominated by Actinobacteria and a significant number showed traits of interest for remediation, harbouring genes homologous to bphA, involved in the PCB oxidation pathway, and displaying 2,3-catechol dioxygenase activity and emulsification properties. Several strains also showed the potential to alleviate plant stress through 1-aminocyclopropane-1-carboxylate deaminase activity. In particular, we identified three Rhodococcus strains able to degrade in vitro several PCB congeners and to promote lateral root emergence in the model plant Arabidopsis thaliana in vivo. In addition, these strains showed the capacity to colonize the root system and to increase the plant biomass in PCB contaminated soil, making them ideal candidates to sustain microbial-assisted PCB rhizoremediation through a bioaugmentation approach.
- MeSH
- Arabidopsis growth & development microbiology MeSH
- Bacterial Proteins genetics metabolism MeSH
- Biodegradation, Environmental MeSH
- Gene Expression MeSH
- Catechol 2,3-Dioxygenase genetics metabolism MeSH
- Plant Roots growth & development microbiology MeSH
- Soil Pollutants metabolism MeSH
- Carbon-Carbon Lyases genetics metabolism MeSH
- Oxidation-Reduction MeSH
- Phalaris growth & development microbiology MeSH
- Polychlorinated Biphenyls metabolism MeSH
- Soil chemistry MeSH
- Soil Microbiology MeSH
- Rhodococcus enzymology genetics MeSH
- Secondary Metabolism genetics MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- 1-aminocyclopropane-1-carboxylate deaminase MeSH Browser
- Bacterial Proteins MeSH
- Catechol 2,3-Dioxygenase MeSH
- Soil Pollutants MeSH
- Carbon-Carbon Lyases MeSH
- Polychlorinated Biphenyls MeSH
- Soil MeSH
The ability of microorganisms to degrade xenobiotics can be exploited to develop cost-effective and eco-friendly bioremediation technologies. Microorganisms can degrade almost all organic pollutants, but this process might be very slow in some cases. A promising way to enhance removal of recalcitrant xenobiotics from the environment lies in the interactions between plant exudates such as plant secondary metabolites (PSMs) and microorganisms. Although there is a considerable body of evidence that PSMs can alter the microbial community composition and stimulate the microbial degradation of xenobiotics, their mechanisms of action remain poorly understood. With this in mind, our aim was to demonstrate that similarity between the chemical structures of PSMs and xenobiotics results in higher micropollutant degradation rates, and the occurrence of corresponding bacterial degradative genes. To verify this, the present study analyses the influence of syringic acid, a plant secondary metabolite, on the bacterial degradation of an herbicide, 4-chloro-2-methylphenoxyacetic acid (MCPA). In particular, the presence of appropriate MCPA degradative genes, MCPA removal efficiency and changes in samples phytotoxicity have been analyzed. Significant MCPA depletion was achieved in samples enriched with syringic acid. The results confirmed not only greater MCPA removal from the samples upon spiking with syringic acid, and thus decreased phytotoxicity, but also the presence of a greater number of genes responsible for MCPA biodegradation. 16S rRNA gene sequence analysis revealed ubiquitous enrichment of the β-proteobacteria Rhodoferax, Achromobacter, Burkholderia and Cupriavidus. The obtained results provide further confirmation that plant metabolites released into the rhizosphere can stimulate biodegradation of xenobiotics, including MCPA.
- Keywords
- Biodegradation, MCPA, PSM, Phenoxy herbicide, Syringic acid, tfdA,
- Publication type
- Journal Article MeSH
Cis-1,2-dichloroethylene (cDCE), which is a common hazardous compound, often accumulates during incomplete reductive dechlorination of higher chlorinated ethenes (CEs) at contaminated sites. Simple monoaromatics, such as toluene and phenol, have been proven to induce biotransformation of cDCE in microbial communities incapable of cDCE degradation in the absence of other carbon sources. The goal of this microcosm-based laboratory study was to discover non-toxic natural monoaromatic secondary plant metabolites (SPMEs) that could enhance cDCE degradation in a similar manner to toluene and phenol. Eight SPMEs were selected on the basis of their monoaromatic molecular structure and widespread occurrence in nature. The suitability of the SPMEs chosen to support bacterial growth and to promote cDCE degradation was evaluated in aerobic microbial cultures enriched from cDCE-contaminated soil in the presence of each SPME tested and cDCE. Significant cDCE depletions were achieved in cultures enriched on acetophenone, phenethyl alcohol, p-hydroxybenzoic acid and trans-cinnamic acid. 16S rRNA gene sequence analysis of each microbial community revealed ubiquitous enrichment of bacteria affiliated with the genera Cupriavidus, Rhodococcus, Burkholderia, Acinetobacter and Pseudomonas. Our results provide further confirmation of the previously stated secondary compound hypothesis that plant metabolites released into the rhizosphere can trigger biodegradation of environmental pollutants, including cDCE.
- MeSH
- Acetophenones metabolism MeSH
- Aerobiosis MeSH
- Bacteria genetics metabolism MeSH
- Biodegradation, Environmental MeSH
- Cinnamates metabolism MeSH
- Dichloroethylenes metabolism MeSH
- Phenylethyl Alcohol metabolism MeSH
- Phenols metabolism MeSH
- Phylogeny MeSH
- Hydroxybenzoates metabolism MeSH
- Soil Pollutants metabolism MeSH
- Microbial Consortia genetics MeSH
- Soil Microbiology MeSH
- RNA, Ribosomal, 16S MeSH
- Plants metabolism MeSH
- Secondary Metabolism MeSH
- Toluene metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- 1,2-dichloroethylene MeSH Browser
- Acetophenones MeSH
- acetophenone MeSH Browser
- Cinnamates MeSH
- cinnamic acid MeSH Browser
- Dichloroethylenes MeSH
- Phenylethyl Alcohol MeSH
- Phenols MeSH
- Hydroxybenzoates MeSH
- Soil Pollutants MeSH
- phenolic acid MeSH Browser
- RNA, Ribosomal, 16S MeSH
- Toluene MeSH
Although stinging nettle (Urtica dioica) has been shown to reduce HM (heavy metal) content in soil, its wider phytoremediation potential has been neglected. Urtica dioica was cultivated in soils contaminated with HMs or polychlorinated biphenyls (PCBs). After four months, up to 33% of the less chlorinated biphenyls and 8% of HMs (Zn, Pb, Cd) had been removed. Bacteria were isolated from the plant tissue, with the endophytic bacteria Bacillus shackletonii and Streptomyces badius shown to have the most significant effect. These bacteria demonstrated not only benefits for plant growth, but also extreme tolerance to As, Zn and Pb. Despite these results, the native phytoremediation potential of nettles could be improved by biotechnologies. Transient expression was used to investigate the functionality of the most common constitutive promoter, CaMV 35S in Urtica dioica. This showed the expression of the CUP and bphC transgenes. Collectively, our findings suggest that remediation by stinging nettle could have a much wider range of applications than previously thought.
- MeSH
- Biodegradation, Environmental * MeSH
- Genetic Engineering methods MeSH
- Plants, Genetically Modified genetics metabolism MeSH
- Cadmium metabolism MeSH
- Soil Pollutants metabolism MeSH
- Lead metabolism MeSH
- Polychlorinated Biphenyls analysis metabolism MeSH
- Promoter Regions, Genetic * genetics MeSH
- Soil chemistry MeSH
- Gene Expression Regulation, Plant genetics MeSH
- Metals, Heavy analysis metabolism MeSH
- Urtica dioica genetics metabolism MeSH
- Zinc metabolism MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Cadmium MeSH
- Soil Pollutants MeSH
- Lead MeSH
- Polychlorinated Biphenyls MeSH
- Soil MeSH
- Metals, Heavy MeSH
- Zinc MeSH