Bioavailability of clay-adsorbed dioxin to Sphingomonas wittichii RW1 and its associated genome-wide shifts in gene expression

TY - JOUR

T1 - Bioavailability of clay-adsorbed dioxin to Sphingomonas wittichii RW1 and its associated genome-wide shifts in gene expression

AU - Chai, Benli

AU - Tsoi, Tamara

AU - Sallach, J. Brett

AU - Liu, Cun

AU - Landgraf, Jeff

AU - Bezdek, Mark

AU - Zylstra, Gerben

AU - Li, Hui

AU - Johnston, Cliff T.

AU - Teppen, Brian J.

AU - Cole, James R.

AU - Boyd, Stephen A.

AU - Tiedje, James M.

N1 - © 2019 Elsevier B.V. This is an author-produced version of the published paper. Uploaded in accordance with the publisher’s self-archiving policy.

PY - 2019/11/21

Y1 - 2019/11/21

N2 - Polychlorinated dibenzo-p-dioxins and dibenzofurans are a group of chemically-related pollutants categorically known as dioxins. Some of their chlorinated congeners are among the most hazardous pollutants that persist in the environment. This persistence is due in part to the limited number of bacteria capable of metabolizing these compounds, but also to their limited bioavailability in soil. We used Sphingomonas wittichii strain RW1 (RW1), one of the few strains able to grow on dioxin, to characterize its ability to respond to and degrade clay-bound dioxin. We found that RW1 grew on and completely degraded dibenzo-p-dioxin (DD) intercalated into the smectite clay saponite (SAP). To characterize the effects of DD sorption on RW1 gene expression, we compared transcriptomes of RW1 grown with either free crystalline DD or DD intercalated clay, i.e. sandwiched between the clay interlayers (DDSAP). Free crystalline DD appeared to cause greater expression of toxicity and stress related functions. Genes coding for heat shock proteins, chaperones, as well as genes involved in DNA repair, and efflux were up-regulated during growth on crystalline dioxin compared to growth on intercalated dioxin. In contrast, growth on intercalated dioxin up-regulated genes that might be important in recognition and uptake mechanisms, as well as surface interaction/attachment/biofilm formation such as extracellular solute-binding protein and LuxR. These differences in gene expression may reflect the underlying adaptive mechanisms by which RW1 cells sense and deploy pathways to access dioxin intercalated into clay. These data show that intercalated DD remains bioavailable to the degrading bacterium with implications for bioremediation alternatives.

AB - Polychlorinated dibenzo-p-dioxins and dibenzofurans are a group of chemically-related pollutants categorically known as dioxins. Some of their chlorinated congeners are among the most hazardous pollutants that persist in the environment. This persistence is due in part to the limited number of bacteria capable of metabolizing these compounds, but also to their limited bioavailability in soil. We used Sphingomonas wittichii strain RW1 (RW1), one of the few strains able to grow on dioxin, to characterize its ability to respond to and degrade clay-bound dioxin. We found that RW1 grew on and completely degraded dibenzo-p-dioxin (DD) intercalated into the smectite clay saponite (SAP). To characterize the effects of DD sorption on RW1 gene expression, we compared transcriptomes of RW1 grown with either free crystalline DD or DD intercalated clay, i.e. sandwiched between the clay interlayers (DDSAP). Free crystalline DD appeared to cause greater expression of toxicity and stress related functions. Genes coding for heat shock proteins, chaperones, as well as genes involved in DNA repair, and efflux were up-regulated during growth on crystalline dioxin compared to growth on intercalated dioxin. In contrast, growth on intercalated dioxin up-regulated genes that might be important in recognition and uptake mechanisms, as well as surface interaction/attachment/biofilm formation such as extracellular solute-binding protein and LuxR. These differences in gene expression may reflect the underlying adaptive mechanisms by which RW1 cells sense and deploy pathways to access dioxin intercalated into clay. These data show that intercalated DD remains bioavailable to the degrading bacterium with implications for bioremediation alternatives.

KW - Dioxin

KW - Bioavailability

KW - Clay-adsorbed

KW - Toxicity

KW - Transcriptome

U2 - 10.1016/j.scitotenv.2019.135525

DO - 10.1016/j.scitotenv.2019.135525

M3 - Article

SN - 0048-9697

JO - Science of the Total Environment

JF - Science of the Total Environment

M1 - 135525

ER -