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Title: Transcriptome Profiling of Shewanella oneidensis Gene Expressionfollowing Exposure to Acidic and Alkaline pH

Abstract

The molecular response of Shewanella oneidensis MR-1 tovariations in extracellular pH was investigated based on genomewide geneexpression profiling. Microarray analysis revealed that cells elicitedboth general and specific transcriptome responses when challenged withenvironmental acid (pH 4) or base (pH 10) conditions over a 60-minperiod. Global responses included the differential expression of genesfunctionally linked to amino acid metabolism, transcriptional regulationand signal transduction, transport, cell membrane structure, andoxidative stress protection. Response to acid stress included theelevated expression of genes encoding glycogen biosynthetic enzymes,phosphate transporters, and the RNA polymerase sigma-38 factor (rpoS),whereas the molecular response to alkaline pH was characterized byupregulation of nhaA and nhaR, which are predicted to encode an Na+/H+antiporter and transcriptional activator, respectively, as well assulfate transport and sulfur metabolism genes. Collectively, theseresults suggest that S. oneidensis modulates multiple transporters, cellenvelope components, and pathways of amino acid consumption and centralintermediary metabolism as part of its transcriptome response to changingexternal pH conditions.

Authors:
; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Ernest Orlando Lawrence Berkeley NationalLaboratory, Berkeley, CA (US)
Sponsoring Org.:
USDOE Director. Office of Science. Office of AdvancedScientific Computing Research. Office of Biological and EnvironmentalResearch
OSTI Identifier:
903367
Report Number(s):
LBNL-60456
Journal ID: ISSN 0021-9193; JOBAAY; R&D Project: VGTLAA; BnR: KP1102010; TRN: US200720%%299
DOE Contract Number:
DE-AC02-05CH11231
Resource Type:
Journal Article
Resource Relation:
Journal Name: Journal of Bacteriology; Journal Volume: 188; Journal Issue: 4; Related Information: Journal Publication Date: February,2006
Country of Publication:
United States
Language:
English
Subject:
59; 54; AMINO ACIDS; CELL MEMBRANES; ENZYMES; GENES; GLYCOGEN; METABOLISM; PHOSPHATES; REGULATIONS; RNA POLYMERASES; SULFATES; SULFUR; TRANSPORT; transcriptomics microarrays

Citation Formats

Leaphart, Adam B., Thompson, Dorothea K., Huang, Katherine, Alm,Eric, Wan, Xiu-Feng, Arkin, Adam P., Brown, Steven D., Wu, Liyou, Yan,Tingfen, Liu, Xueduan, Wickham, Gene S., and Zhou, Jizhong. Transcriptome Profiling of Shewanella oneidensis Gene Expressionfollowing Exposure to Acidic and Alkaline pH. United States: N. p., 2007. Web.
Leaphart, Adam B., Thompson, Dorothea K., Huang, Katherine, Alm,Eric, Wan, Xiu-Feng, Arkin, Adam P., Brown, Steven D., Wu, Liyou, Yan,Tingfen, Liu, Xueduan, Wickham, Gene S., & Zhou, Jizhong. Transcriptome Profiling of Shewanella oneidensis Gene Expressionfollowing Exposure to Acidic and Alkaline pH. United States.
Leaphart, Adam B., Thompson, Dorothea K., Huang, Katherine, Alm,Eric, Wan, Xiu-Feng, Arkin, Adam P., Brown, Steven D., Wu, Liyou, Yan,Tingfen, Liu, Xueduan, Wickham, Gene S., and Zhou, Jizhong. Mon . "Transcriptome Profiling of Shewanella oneidensis Gene Expressionfollowing Exposure to Acidic and Alkaline pH". United States. doi:.
@article{osti_903367,
title = {Transcriptome Profiling of Shewanella oneidensis Gene Expressionfollowing Exposure to Acidic and Alkaline pH},
author = {Leaphart, Adam B. and Thompson, Dorothea K. and Huang, Katherine and Alm,Eric and Wan, Xiu-Feng and Arkin, Adam P. and Brown, Steven D. and Wu, Liyou and Yan,Tingfen and Liu, Xueduan and Wickham, Gene S. and Zhou, Jizhong},
abstractNote = {The molecular response of Shewanella oneidensis MR-1 tovariations in extracellular pH was investigated based on genomewide geneexpression profiling. Microarray analysis revealed that cells elicitedboth general and specific transcriptome responses when challenged withenvironmental acid (pH 4) or base (pH 10) conditions over a 60-minperiod. Global responses included the differential expression of genesfunctionally linked to amino acid metabolism, transcriptional regulationand signal transduction, transport, cell membrane structure, andoxidative stress protection. Response to acid stress included theelevated expression of genes encoding glycogen biosynthetic enzymes,phosphate transporters, and the RNA polymerase sigma-38 factor (rpoS),whereas the molecular response to alkaline pH was characterized byupregulation of nhaA and nhaR, which are predicted to encode an Na+/H+antiporter and transcriptional activator, respectively, as well assulfate transport and sulfur metabolism genes. Collectively, theseresults suggest that S. oneidensis modulates multiple transporters, cellenvelope components, and pathways of amino acid consumption and centralintermediary metabolism as part of its transcriptome response to changingexternal pH conditions.},
doi = {},
journal = {Journal of Bacteriology},
number = 4,
volume = 188,
place = {United States},
year = {Mon Apr 02 00:00:00 EDT 2007},
month = {Mon Apr 02 00:00:00 EDT 2007}
}
  • Shewanella oneidensis MR-1 exhibits diverse metal ion-reducing capabilities and thus is of potential utility as a bioremediation agent. Knowledge of the molecular components and regulatory mechanisms dictating cellular responses to heavy metal stress, however, remains incomplete. In a previous work, the S. oneidensis so2426 gene, annotated as a DNA-binding response regulator, was demonstrated to be specifically responsive at both the transcript and protein levels to acute chromate [Cr(VI)] challenge. To delineate the cellular function of SO2426 and its contribution to metal stress response, we integrated genetic and physiological approaches with a genome-wide screen for target gene candidates comprising the SO2426more » regulon.« less
  • To gain insight into the complex structure of the energy-generating networks in the dissimilatory metal reducer Shewanella oneidensis MR-1, global mRNA patterns were examined in cells exposed to a wide range of metal and non-metal electron acceptors. Gene expression patterns were similar irrespective of which metal ion was used as electron acceptor, with 60% of the differentially expressed genes showing similar induction or repression relative to fumarate- respiring conditions. Several groups of genes exhibited elevated expression levels in the presence of metals, including those encoding putative multidrug efflux transporters, detoxification proteins, extracytoplasmic sigma factors and PAS-domain regulators. Only one ofmore » the 42 predicted c-type cytochromes in MR-1, SO3300, displayed significantly elevated transcript levels across all metal-reducing conditions. Genes encoding decaheme cytochromes MtrC and MtrA that were previously linked to the reduction of different forms of Fe(III) and Mn(IV), exhibited only slight decreases in relative mRNA abundances under metal-reducing conditions. In contrast, specific transcriptome responses were displayed to individual non-metal electron acceptors resulting in the identification of unique groups of nitrate-, thiosulfate- and TMAO-induced genes including previously uncharacterized multi-cytochrome gene clusters. Collectively, the gene expression results reflect the fundamental differences between metal and non-metal respiratory pathways of S. oneidensis MR-1, where the coordinate induction of detoxification and stress response genes play a key role in adaptation of this organism under metal-reducing conditions. Moreover, the relative paucity and/or the constitutive nature of genes involved in electron transfer to metals is likely due to the low-specificity and the opportunistic nature of the metal-reducing electron transport pathways.« less
  • We have designed and validated the first high-density expression array for Shewanella oneidensis MR-1, consisting of 105 oligonucleotide probes differentially targeted to genes and intergenic regions of its genome. Beyond its use for global gene expression profiling, this microarray represents a platform for the identification of small non-coding RNAs, improved operon inference, and CHIP-chip studies.
  • The gamma-proteobacterium Shewanella oneidensis strain MR-1 is a metabolically versatile organism that can reduce a wide range of organic compounds, metal ions, and radionuclides. Similar to most other sequenced organisms, approximate to40% of the predicted ORFs in the S. oneidensis genome were annotated as uncharacterized "hypothetical" genes. We implemented an integrative approach by using experimental and computational analyses to provide more detailed insight into gene function. Global expression profiles were determined for cells after UV irradiation and under aerobic and suboxic growth conditions. Transcriptomic and proteomic analyses confidently identified 538 hypothetical genes as expressed in S. oneidensis cells both asmore » mRNAs and proteins (33% of all predicted hypothetical proteins). Publicly available analysis tools and databases and the expression data were applied to improve the annotation of these genes. The annotation results were scored by using a seven-category schema that ranked both confidence and precision of the functional assignment. We were able to identify homologs for nearly all of these hypothetical proteins (97%), but could confidently assign exact biochemical functions for only 16 proteins (category 1; 3%). Altogether, computational and experimental evidence provided functional assignments or insights for 240 more genes (categories 2-5; 45%). These functional annotations advance our understanding of genes involved in vital cellular processes, including energy conversion, ion transport, secondary metabolism, and signal transduction. We propose that this integrative approach offers a valuable means to undertake the enormous challenge of characterizing the rapidly growing number of hypothetical proteins with each newly sequenced genome.« less