Structure and Evolution of Chlorate Reduction Composite Transposons

ABSTRACT The genes for chlorate reduction in six bacterial strains were analyzed in order to gain insight into the metabolism. A newly isolated chlorate-reducing bacterium (Shewanella algae ACDC) and three previously isolated strains (Ideonella dechloratans, Pseudomonas sp. strain PK, and Dechloroma...

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Autores principales:	Iain C. Clark, Ryan A. Melnyk, Anna Engelbrektson, John D. Coates
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Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
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spelling	oai:doaj.org-article:645456570c884c9589a913823b5966992021-11-15T15:43:08ZStructure and Evolution of Chlorate Reduction Composite Transposons10.1128/mBio.00379-132150-7511https://doaj.org/article/645456570c884c9589a913823b5966992013-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00379-13https://doaj.org/toc/2150-7511ABSTRACT The genes for chlorate reduction in six bacterial strains were analyzed in order to gain insight into the metabolism. A newly isolated chlorate-reducing bacterium (Shewanella algae ACDC) and three previously isolated strains (Ideonella dechloratans, Pseudomonas sp. strain PK, and Dechloromarinus chlorophilus NSS) were genome sequenced and compared to published sequences (Alicycliphilus denitrificans BC plasmid pALIDE01 and Pseudomonas chloritidismutans AW-1). De novo assembly of genomes failed to join regions adjacent to genes involved in chlorate reduction, suggesting the presence of repeat regions. Using a bioinformatics approach and finishing PCRs to connect fragmented contigs, we discovered that chlorate reduction genes are flanked by insertion sequences, forming composite transposons in all four newly sequenced strains. These insertion sequences delineate regions with the potential to move horizontally and define a set of genes that may be important for chlorate reduction. In addition to core metabolic components, we have highlighted several such genes through comparative analysis and visualization. Phylogenetic analysis places chlorate reductase within a functionally diverse clade of type II dimethyl sulfoxide (DMSO) reductases, part of a larger family of enzymes with reactivity toward chlorate. Nucleotide-level forensics of regions surrounding chlorite dismutase (cld), as well as its phylogenetic clustering in a betaproteobacterial Cld clade, indicate that cld has been mobilized at least once from a perchlorate reducer to build chlorate respiration. IMPORTANCE Genome sequencing has identified, for the first time, chlorate reduction composite transposons. These transposons are constructed with flanking insertion sequences that differ in type and orientation between organisms, indicating that this mobile element has formed multiple times and is important for dissemination. Apart from core metabolic enzymes, very little is known about the genetic factors involved in chlorate reduction. Comparative analysis has identified several genes that may also be important, but the relative absence of accessory genes suggests that this mobile metabolism relies on host systems for electron transport, regulation, and cofactor synthesis. Phylogenetic analysis of Cld and ClrA provides support for the hypothesis that chlorate reduction was built multiple times from type II dimethyl sulfoxide (DMSO) reductases and cld. In at least one case, cld has been coopted from a perchlorate reduction island for this purpose. This work is a significant step toward understanding the genetics and evolution of chlorate reduction.Iain C. ClarkRyan A. MelnykAnna EngelbrektsonJohn D. CoatesAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 4 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Iain C. Clark Ryan A. Melnyk Anna Engelbrektson John D. Coates Structure and Evolution of Chlorate Reduction Composite Transposons
description	ABSTRACT The genes for chlorate reduction in six bacterial strains were analyzed in order to gain insight into the metabolism. A newly isolated chlorate-reducing bacterium (Shewanella algae ACDC) and three previously isolated strains (Ideonella dechloratans, Pseudomonas sp. strain PK, and Dechloromarinus chlorophilus NSS) were genome sequenced and compared to published sequences (Alicycliphilus denitrificans BC plasmid pALIDE01 and Pseudomonas chloritidismutans AW-1). De novo assembly of genomes failed to join regions adjacent to genes involved in chlorate reduction, suggesting the presence of repeat regions. Using a bioinformatics approach and finishing PCRs to connect fragmented contigs, we discovered that chlorate reduction genes are flanked by insertion sequences, forming composite transposons in all four newly sequenced strains. These insertion sequences delineate regions with the potential to move horizontally and define a set of genes that may be important for chlorate reduction. In addition to core metabolic components, we have highlighted several such genes through comparative analysis and visualization. Phylogenetic analysis places chlorate reductase within a functionally diverse clade of type II dimethyl sulfoxide (DMSO) reductases, part of a larger family of enzymes with reactivity toward chlorate. Nucleotide-level forensics of regions surrounding chlorite dismutase (cld), as well as its phylogenetic clustering in a betaproteobacterial Cld clade, indicate that cld has been mobilized at least once from a perchlorate reducer to build chlorate respiration. IMPORTANCE Genome sequencing has identified, for the first time, chlorate reduction composite transposons. These transposons are constructed with flanking insertion sequences that differ in type and orientation between organisms, indicating that this mobile element has formed multiple times and is important for dissemination. Apart from core metabolic enzymes, very little is known about the genetic factors involved in chlorate reduction. Comparative analysis has identified several genes that may also be important, but the relative absence of accessory genes suggests that this mobile metabolism relies on host systems for electron transport, regulation, and cofactor synthesis. Phylogenetic analysis of Cld and ClrA provides support for the hypothesis that chlorate reduction was built multiple times from type II dimethyl sulfoxide (DMSO) reductases and cld. In at least one case, cld has been coopted from a perchlorate reduction island for this purpose. This work is a significant step toward understanding the genetics and evolution of chlorate reduction.
format	article
author	Iain C. Clark Ryan A. Melnyk Anna Engelbrektson John D. Coates
author_facet	Iain C. Clark Ryan A. Melnyk Anna Engelbrektson John D. Coates
author_sort	Iain C. Clark
title	Structure and Evolution of Chlorate Reduction Composite Transposons
title_short	Structure and Evolution of Chlorate Reduction Composite Transposons
title_full	Structure and Evolution of Chlorate Reduction Composite Transposons
title_fullStr	Structure and Evolution of Chlorate Reduction Composite Transposons
title_full_unstemmed	Structure and Evolution of Chlorate Reduction Composite Transposons
title_sort	structure and evolution of chlorate reduction composite transposons
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/645456570c884c9589a913823b596699
work_keys_str_mv	AT iaincclark structureandevolutionofchloratereductioncompositetransposons AT ryanamelnyk structureandevolutionofchloratereductioncompositetransposons AT annaengelbrektson structureandevolutionofchloratereductioncompositetransposons AT johndcoates structureandevolutionofchloratereductioncompositetransposons
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Structure and Evolution of Chlorate Reduction Composite Transposons

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