Conjugative transfer of Megaplasmids pND6–1 and pND6–2 enhancing naphthalene degradation in aqueous environment: characterization and bioaugmentation prospects

Wang, Shan; Li, Shanshan; Du, Dan; Wang, Dan; Wang, Yan

doi:10.1007/s00253-019-10273-8

Cited by 8 publications

(4 citation statements)

References 44 publications

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“…The TRIS degradation-encoding Pseudomonas plasmids have high similarities to the previously described large plasmids pND6-2 from Pseudomonas putida ND6 and pS04-90 from Pseudomonas aeruginosa S04-90 [16, 17]. Both these plasmids lack the putative mobile genetic element that encodes TRIS degradation ( Fig.…”

Section: Resultsmentioning

confidence: 76%

A patchwork pathway of apparently recent origin enables degradation of the synthetic buffer compound TRIS in bacteria

Holert,

Borker,

Nübel

et al. 2023

Preprint

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The widely used synthetic chemical 2-amino-2-hydroxymethyl-propane-1,3-diol (TRIS) was long considered to be biologically inert. Herein, we describe a complete degradation pathway for the catabolism of TRIS in bacteria. By serendipity,Pseudomonas hunanensisTeo1 was isolated from sewage sludge and shown to be able to grow with TRIS as only carbon and nitrogen source. Genome sequencing and transcriptome analyses revealed two adjacent gene clusters embedded in a mobile genetic element on a conjugative plasmid to be upregulated during growth with TRIS. Conjugational transfer of this plasmid intoP. putidaKT2440 enabled this strain to grow with TRIS confirming that these clusters encode the complete TRIS degradation pathway. Heterologous gene expression inEscherichia colirevealed cluster I to encode a TRIS uptake protein, a TRIS dehydrogenase, and a TRIS aldehyde dehydrogenase, which catalyze the oxidation of TRIS into 2-hydroxymethylserine. Phylogenetic analysis suggests that the TRIS dehydrogenase proteins evolved from choline dehydrogenases. Genes encoded in cluster II encode a methylserine hydroxymethyltransferase and a D-serine dehydratase which could plausibly catalyze conversion of 2-hydroxymethylserine into pyruvate. Subsequent enrichments from wastewater purification systems led to the isolation of further TRIS-degrading bacteria from thePseudomonasandShinellagenera which all carried the respective gene clusters in a similar genetic context as strain Teo1.Our data indicate that TRIS degradation evolved by gene assembly and enzyme adaptation from multiple independent metabolic pathways. Genomic database searches showed that TRIS degradation is now globally distributed, confirming its dissemination by horizontal gene transfer.Significance statementTRIS is a synthetic organic chemical that has been mass-produced since the 1950s and is now used in countless applications in industry, medicine, and households world-wide, in parts due to its presumed biological inertness. Our results challenge this common conception, showing that TRIS is biologically degradable by an apparently recently evolved pathway, providing insight into the evolution of metabolic pathways that make such ubiquitous chemicals available as growth substrates for bacteria. Such knowledge is valuable for developing new processes of wastewater purification in times of increasing water scarcity.

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Section: Resultsmentioning

confidence: 76%

A patchwork pathway of apparently recent origin enables degradation of the synthetic buffer compound TRIS in bacteria

Holert,

Borker,

Nübel

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…The TRIS degradation-encoding Pseudomonas plasmids have high similarities to the previously described large plasmids pND6-2 from P. putida ND6 and pS04-90 from Pseudomonas aeruginosa S04-90 [ 20 , 21 ]. Both these plasmids lack the putative mobile genetic element that encodes TRIS degradation ( Fig.…”

Section: Resultsmentioning

confidence: 85%

Bacteria use a catabolic patchwork pathway of apparently recent origin for degradation of the synthetic buffer compound TRIS

Holert,

Borker,

Nübel

et al. 2024

The ISME Journal

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The synthetic buffer compound TRIS is used in countless applications and no detailed information on its degradation has been published so far. Herein, we describe the discovery of a complete bacterial degradation pathway for TRIS. By serendipity, a Pseudomonas strain was isolated from sewage sludge that was able to grow with TRIS as only carbon and nitrogen source. Genome and transcriptome analyses revealed two adjacent gene clusters embedded in a mobile genetic element on a conjugative plasmid to be involved in TRIS degradation. Heterologous gene expression revealed cluster I to encode a TRIS uptake protein, a TRIS alcohol dehydrogenase, and a TRIS aldehyde dehydrogenase, catalyzing the oxidation of TRIS into 2-hydroxymethylserine. Gene cluster II encodes a methylserine hydroxymethyltransferase and a D-serine dehydratase that plausibly catalyze the conversion of 2-hydroxymethylserine into pyruvate. Conjugational plasmid transfer into Pseudomonas putida KT2440 enabled this strain to grow with TRIS and with 2-hydromethylserine, demonstrating that the complete TRIS degradation pathway can be transmitted by horizontal gene transfer. Subsequent enrichments from wastewater purification systems led to the isolation of further TRIS-degrading bacteria from the Pseudomonas and Shinella genera carrying highly similar TRIS degradation gene clusters. Our data indicate that TRIS degradation evolved recently via gene recruitment and enzyme adaptation from multiple independent metabolic pathways and database searches suggest that the TRIS degradation pathway is now globally distributed. Overall, our study illustrates how engineered environments can enhance the emergence of new microbial metabolic pathways in short evolutionary time scales.

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“…Regarding the effect of selection pressure on plasmid transfer, the different methods used to detect transconjugants could in uence the results (Wang et al 2020). In the present study, the proportion of transconjugants in the sludge bacteria was measured by qPCR analysis.…”

Section: Discussionmentioning

confidence: 99%

The impact of pollutant as selection pressure on conjugative transfer of dioxin-catabolic plasmids harbored by Rhodococcus sp. strain p52

Zhao

Wang

et al. 2021

Environ Sci Pollut Res

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Plasmid-mediated bioaugmentation has potential application in the cleanup of recalcitrant environmental pollutants. In this study, we examined the in uence of various contaminants (in different categories or different amounts) as a selection pressure on the transfer of catabolic plasmids within an activated sludge bacteria community bioaugmented with Rhodococcus sp. strain p52 harboring pDF01 and pDF02. The distinguishable genera of transconjugants were isolated under the stresses of phenanthrene, dibenzothiophene, and dibenzo-p-dioxin. The difference in genomic G + C content (5.0 ~ 27.5%) between transconjugants and strain p52 indicated the transfer of the catabolic plasmids crossing phylogenetic boundaries. The speci c removal rates in activated sludge reactors for phenanthrene, dibenzothiophene, and dibenzo-p-dioxin were elevated in turn. The three contaminants exerted different degrees of in uence on the activated sludge bacteria bearing the catabolic plasmids. The highest proportion of transconjugants was detected in the reactor fed with dibenzo-p-dioxin. Additionally, as dibenzo-p-dioxin from 10 to 80 mg/L was fed into the reactors, the proportion of transconjugants increased. Film mating tests demonstrated that the plasmid transfer frequency varied among recipients under the contaminant stresses of phenanthrene, dibenzothiophene, and dibenzo-p-dioxin. Our study provides a characterization of the recalcitrant contaminants as a selection pressure that can modulate catabolic plasmid transfer during genetic bioaugmentation for the removal of contaminants.

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Conjugative transfer of Megaplasmids pND6–1 and pND6–2 enhancing naphthalene degradation in aqueous environment: characterization and bioaugmentation prospects

Cited by 8 publications

References 44 publications

A patchwork pathway of apparently recent origin enables degradation of the synthetic buffer compound TRIS in bacteria

A patchwork pathway of apparently recent origin enables degradation of the synthetic buffer compound TRIS in bacteria

Bacteria use a catabolic patchwork pathway of apparently recent origin for degradation of the synthetic buffer compound TRIS

The impact of pollutant as selection pressure on conjugative transfer of dioxin-catabolic plasmids harbored by Rhodococcus sp. strain p52

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