Something old, something new, something borrowed; how the thermoacidophilic archaeon Sulfolobus solfataricus responds to oxidative stress.

To avoid molecular damage of biomolecules due to oxidation, all cells have evolved constitutive and responsive systems to mitigate and repair chemical modifications. Archaea have adapted to some of the most extreme environments known to support life, including highly oxidizing conditions. However, i...

Full description

Bibliographic Details
Main Authors: Walid S Maaty, Blake Wiedenheft, Pavel Tarlykov, Nathan Schaff, Joshua Heinemann, Jim Robison-Cox, Jacob Valenzuela, Amanda Dougherty, Paul Blum, C Martin Lawrence, Trevor Douglas, Mark J Young, Brian Bothner
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2009-09-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC2739297?pdf=render
_version_ 1818940830682972160
author Walid S Maaty
Blake Wiedenheft
Pavel Tarlykov
Nathan Schaff
Joshua Heinemann
Jim Robison-Cox
Jacob Valenzuela
Amanda Dougherty
Paul Blum
C Martin Lawrence
Trevor Douglas
Mark J Young
Brian Bothner
author_facet Walid S Maaty
Blake Wiedenheft
Pavel Tarlykov
Nathan Schaff
Joshua Heinemann
Jim Robison-Cox
Jacob Valenzuela
Amanda Dougherty
Paul Blum
C Martin Lawrence
Trevor Douglas
Mark J Young
Brian Bothner
author_sort Walid S Maaty
collection DOAJ
description To avoid molecular damage of biomolecules due to oxidation, all cells have evolved constitutive and responsive systems to mitigate and repair chemical modifications. Archaea have adapted to some of the most extreme environments known to support life, including highly oxidizing conditions. However, in comparison to bacteria and eukaryotes, relatively little is known about the biology and biochemistry of archaea in response to changing conditions and repair of oxidative damage. In this study transcriptome, proteome, and chemical reactivity analyses of hydrogen peroxide (H(2)O(2)) induced oxidative stress in Sulfolobus solfataricus (P2) were conducted. Microarray analysis of mRNA expression showed that 102 transcripts were regulated by at least 1.5 fold, 30 minutes after exposure to 30 microM H(2)O(2). Parallel proteomic analyses using two-dimensional differential gel electrophoresis (2D-DIGE), monitored more than 800 proteins 30 and 105 minutes after exposure and found that 18 had significant changes in abundance. A recently characterized ferritin-like antioxidant protein, DPSL, was the most highly regulated species of mRNA and protein, in addition to being post-translationally modified. As expected, a number of antioxidant related mRNAs and proteins were differentially regulated. Three of these, DPSL, superoxide dismutase, and peroxiredoxin were shown to interact and likely form a novel supramolecular complex for mitigating oxidative damage. A scheme for the ability of this complex to perform multi-step reactions is presented. Despite the central role played by DPSL, cells maintained a lower level of protection after disruption of the dpsl gene, indicating a level of redundancy in the oxidative stress pathways of S. solfataricus. This work provides the first "omics" scale assessment of the oxidative stress response for an archeal organism and together with a network analysis using data from previous studies on bacteria and eukaryotes reveals evolutionarily conserved pathways where complex and overlapping defense mechanisms protect against oxygen toxicity.
first_indexed 2024-12-20T06:45:53Z
format Article
id doaj.art-49eafbe54c2c402991239817bf001d5c
institution Directory Open Access Journal
issn 1932-6203
language English
last_indexed 2024-12-20T06:45:53Z
publishDate 2009-09-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj.art-49eafbe54c2c402991239817bf001d5c2022-12-21T19:49:42ZengPublic Library of Science (PLoS)PLoS ONE1932-62032009-09-0149e696410.1371/journal.pone.0006964Something old, something new, something borrowed; how the thermoacidophilic archaeon Sulfolobus solfataricus responds to oxidative stress.Walid S MaatyBlake WiedenheftPavel TarlykovNathan SchaffJoshua HeinemannJim Robison-CoxJacob ValenzuelaAmanda DoughertyPaul BlumC Martin LawrenceTrevor DouglasMark J YoungBrian BothnerTo avoid molecular damage of biomolecules due to oxidation, all cells have evolved constitutive and responsive systems to mitigate and repair chemical modifications. Archaea have adapted to some of the most extreme environments known to support life, including highly oxidizing conditions. However, in comparison to bacteria and eukaryotes, relatively little is known about the biology and biochemistry of archaea in response to changing conditions and repair of oxidative damage. In this study transcriptome, proteome, and chemical reactivity analyses of hydrogen peroxide (H(2)O(2)) induced oxidative stress in Sulfolobus solfataricus (P2) were conducted. Microarray analysis of mRNA expression showed that 102 transcripts were regulated by at least 1.5 fold, 30 minutes after exposure to 30 microM H(2)O(2). Parallel proteomic analyses using two-dimensional differential gel electrophoresis (2D-DIGE), monitored more than 800 proteins 30 and 105 minutes after exposure and found that 18 had significant changes in abundance. A recently characterized ferritin-like antioxidant protein, DPSL, was the most highly regulated species of mRNA and protein, in addition to being post-translationally modified. As expected, a number of antioxidant related mRNAs and proteins were differentially regulated. Three of these, DPSL, superoxide dismutase, and peroxiredoxin were shown to interact and likely form a novel supramolecular complex for mitigating oxidative damage. A scheme for the ability of this complex to perform multi-step reactions is presented. Despite the central role played by DPSL, cells maintained a lower level of protection after disruption of the dpsl gene, indicating a level of redundancy in the oxidative stress pathways of S. solfataricus. This work provides the first "omics" scale assessment of the oxidative stress response for an archeal organism and together with a network analysis using data from previous studies on bacteria and eukaryotes reveals evolutionarily conserved pathways where complex and overlapping defense mechanisms protect against oxygen toxicity.http://europepmc.org/articles/PMC2739297?pdf=render
spellingShingle Walid S Maaty
Blake Wiedenheft
Pavel Tarlykov
Nathan Schaff
Joshua Heinemann
Jim Robison-Cox
Jacob Valenzuela
Amanda Dougherty
Paul Blum
C Martin Lawrence
Trevor Douglas
Mark J Young
Brian Bothner
Something old, something new, something borrowed; how the thermoacidophilic archaeon Sulfolobus solfataricus responds to oxidative stress.
PLoS ONE
title Something old, something new, something borrowed; how the thermoacidophilic archaeon Sulfolobus solfataricus responds to oxidative stress.
title_full Something old, something new, something borrowed; how the thermoacidophilic archaeon Sulfolobus solfataricus responds to oxidative stress.
title_fullStr Something old, something new, something borrowed; how the thermoacidophilic archaeon Sulfolobus solfataricus responds to oxidative stress.
title_full_unstemmed Something old, something new, something borrowed; how the thermoacidophilic archaeon Sulfolobus solfataricus responds to oxidative stress.
title_short Something old, something new, something borrowed; how the thermoacidophilic archaeon Sulfolobus solfataricus responds to oxidative stress.
title_sort something old something new something borrowed how the thermoacidophilic archaeon sulfolobus solfataricus responds to oxidative stress
url http://europepmc.org/articles/PMC2739297?pdf=render
work_keys_str_mv AT walidsmaaty somethingoldsomethingnewsomethingborrowedhowthethermoacidophilicarchaeonsulfolobussolfataricusrespondstooxidativestress
AT blakewiedenheft somethingoldsomethingnewsomethingborrowedhowthethermoacidophilicarchaeonsulfolobussolfataricusrespondstooxidativestress
AT paveltarlykov somethingoldsomethingnewsomethingborrowedhowthethermoacidophilicarchaeonsulfolobussolfataricusrespondstooxidativestress
AT nathanschaff somethingoldsomethingnewsomethingborrowedhowthethermoacidophilicarchaeonsulfolobussolfataricusrespondstooxidativestress
AT joshuaheinemann somethingoldsomethingnewsomethingborrowedhowthethermoacidophilicarchaeonsulfolobussolfataricusrespondstooxidativestress
AT jimrobisoncox somethingoldsomethingnewsomethingborrowedhowthethermoacidophilicarchaeonsulfolobussolfataricusrespondstooxidativestress
AT jacobvalenzuela somethingoldsomethingnewsomethingborrowedhowthethermoacidophilicarchaeonsulfolobussolfataricusrespondstooxidativestress
AT amandadougherty somethingoldsomethingnewsomethingborrowedhowthethermoacidophilicarchaeonsulfolobussolfataricusrespondstooxidativestress
AT paulblum somethingoldsomethingnewsomethingborrowedhowthethermoacidophilicarchaeonsulfolobussolfataricusrespondstooxidativestress
AT cmartinlawrence somethingoldsomethingnewsomethingborrowedhowthethermoacidophilicarchaeonsulfolobussolfataricusrespondstooxidativestress
AT trevordouglas somethingoldsomethingnewsomethingborrowedhowthethermoacidophilicarchaeonsulfolobussolfataricusrespondstooxidativestress
AT markjyoung somethingoldsomethingnewsomethingborrowedhowthethermoacidophilicarchaeonsulfolobussolfataricusrespondstooxidativestress
AT brianbothner somethingoldsomethingnewsomethingborrowedhowthethermoacidophilicarchaeonsulfolobussolfataricusrespondstooxidativestress