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Sphingomonas wittichii Strain RW1 Genome-Wide Gene Expression Shifts in Response to Dioxins and Clay

Sphingomonas wittichii strain RW1 (RW1) is one of the few strains that can grow on dibenzo-p-dioxin (DD). We conducted a transcriptomic study of RW1 using RNA-Seq to outline transcriptional responses to DD, dibenzofuran (DF), and the smectite clay mineral saponite with succinate as carbon source. Th...

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Autores principales: Chai, Benli, Tsoi, Tamara V., Iwai, Shoko, Liu, Cun, Fish, Jordan A., Gu, Cheng, Johnson, Timothy A., Zylstra, Gerben, Teppen, Brian J., Li, Hui, Hashsham, Syed A., Boyd, Stephen A., Cole, James R., Tiedje, James M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4911050/
https://www.ncbi.nlm.nih.gov/pubmed/27309357
http://dx.doi.org/10.1371/journal.pone.0157008
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author Chai, Benli
Tsoi, Tamara V.
Iwai, Shoko
Liu, Cun
Fish, Jordan A.
Gu, Cheng
Johnson, Timothy A.
Zylstra, Gerben
Teppen, Brian J.
Li, Hui
Hashsham, Syed A.
Boyd, Stephen A.
Cole, James R.
Tiedje, James M.
author_facet Chai, Benli
Tsoi, Tamara V.
Iwai, Shoko
Liu, Cun
Fish, Jordan A.
Gu, Cheng
Johnson, Timothy A.
Zylstra, Gerben
Teppen, Brian J.
Li, Hui
Hashsham, Syed A.
Boyd, Stephen A.
Cole, James R.
Tiedje, James M.
author_sort Chai, Benli
collection PubMed
description Sphingomonas wittichii strain RW1 (RW1) is one of the few strains that can grow on dibenzo-p-dioxin (DD). We conducted a transcriptomic study of RW1 using RNA-Seq to outline transcriptional responses to DD, dibenzofuran (DF), and the smectite clay mineral saponite with succinate as carbon source. The ability to grow on DD is rare compared to growth on the chemically similar DF even though the same initial dioxygenase may be involved in oxidation of both substrates. Therefore, we hypothesized the reason for this lies beyond catabolic pathways and may concern genes involved in processes for cell-substrate interactions such as substrate recognition, transport, and detoxification. Compared to succinate (SUC) as control carbon source, DF caused over 240 protein-coding genes to be differentially expressed, whereas more than 300 were differentially expressed with DD. Stress response genes were up-regulated in response to both DD and DF. This effect was stronger with DD than DF, suggesting a higher toxicity of DD compared to DF. Both DD and DF caused changes in expression of genes involved in active cross-membrane transport such as TonB-dependent receptor proteins, but the patterns of change differed between the two substrates. Multiple transcription factor genes also displayed expression patterns distinct to DD and DF growth. DD and DF induced the catechol ortho- and the salicylate/gentisate pathways, respectively. Both DD and DF induced the shared down-stream aliphatic intermediate compound pathway. Clay caused category-wide down-regulation of genes for cell motility and chemotaxis, particularly those involved in the synthesis, assembly and functioning of flagella. This is an environmentally important finding because clay is a major component of soil microbes’ microenvironment influencing local chemistry and may serve as a geosorbent for toxic pollutants. Similar to clay, DD and DF also affected expression of genes involved in motility and chemotaxis.
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spelling pubmed-49110502016-07-06 Sphingomonas wittichii Strain RW1 Genome-Wide Gene Expression Shifts in Response to Dioxins and Clay Chai, Benli Tsoi, Tamara V. Iwai, Shoko Liu, Cun Fish, Jordan A. Gu, Cheng Johnson, Timothy A. Zylstra, Gerben Teppen, Brian J. Li, Hui Hashsham, Syed A. Boyd, Stephen A. Cole, James R. Tiedje, James M. PLoS One Research Article Sphingomonas wittichii strain RW1 (RW1) is one of the few strains that can grow on dibenzo-p-dioxin (DD). We conducted a transcriptomic study of RW1 using RNA-Seq to outline transcriptional responses to DD, dibenzofuran (DF), and the smectite clay mineral saponite with succinate as carbon source. The ability to grow on DD is rare compared to growth on the chemically similar DF even though the same initial dioxygenase may be involved in oxidation of both substrates. Therefore, we hypothesized the reason for this lies beyond catabolic pathways and may concern genes involved in processes for cell-substrate interactions such as substrate recognition, transport, and detoxification. Compared to succinate (SUC) as control carbon source, DF caused over 240 protein-coding genes to be differentially expressed, whereas more than 300 were differentially expressed with DD. Stress response genes were up-regulated in response to both DD and DF. This effect was stronger with DD than DF, suggesting a higher toxicity of DD compared to DF. Both DD and DF caused changes in expression of genes involved in active cross-membrane transport such as TonB-dependent receptor proteins, but the patterns of change differed between the two substrates. Multiple transcription factor genes also displayed expression patterns distinct to DD and DF growth. DD and DF induced the catechol ortho- and the salicylate/gentisate pathways, respectively. Both DD and DF induced the shared down-stream aliphatic intermediate compound pathway. Clay caused category-wide down-regulation of genes for cell motility and chemotaxis, particularly those involved in the synthesis, assembly and functioning of flagella. This is an environmentally important finding because clay is a major component of soil microbes’ microenvironment influencing local chemistry and may serve as a geosorbent for toxic pollutants. Similar to clay, DD and DF also affected expression of genes involved in motility and chemotaxis. Public Library of Science 2016-06-16 /pmc/articles/PMC4911050/ /pubmed/27309357 http://dx.doi.org/10.1371/journal.pone.0157008 Text en © 2016 Chai et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Chai, Benli
Tsoi, Tamara V.
Iwai, Shoko
Liu, Cun
Fish, Jordan A.
Gu, Cheng
Johnson, Timothy A.
Zylstra, Gerben
Teppen, Brian J.
Li, Hui
Hashsham, Syed A.
Boyd, Stephen A.
Cole, James R.
Tiedje, James M.
Sphingomonas wittichii Strain RW1 Genome-Wide Gene Expression Shifts in Response to Dioxins and Clay
title Sphingomonas wittichii Strain RW1 Genome-Wide Gene Expression Shifts in Response to Dioxins and Clay
title_full Sphingomonas wittichii Strain RW1 Genome-Wide Gene Expression Shifts in Response to Dioxins and Clay
title_fullStr Sphingomonas wittichii Strain RW1 Genome-Wide Gene Expression Shifts in Response to Dioxins and Clay
title_full_unstemmed Sphingomonas wittichii Strain RW1 Genome-Wide Gene Expression Shifts in Response to Dioxins and Clay
title_short Sphingomonas wittichii Strain RW1 Genome-Wide Gene Expression Shifts in Response to Dioxins and Clay
title_sort sphingomonas wittichii strain rw1 genome-wide gene expression shifts in response to dioxins and clay
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4911050/
https://www.ncbi.nlm.nih.gov/pubmed/27309357
http://dx.doi.org/10.1371/journal.pone.0157008
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