Snapshot of iron response in Shewanella oneidensis by gene network reconstruction

Yang, Yunfeng; Harris, Daniel P.; Luo, Feng; Xiong, Wenlu; Joachimiak, Marcin P.; Wu, Liyou; Dehal, Paramvir; Jacobsen, Janet; Yang, Zamin K.; Palumbo, Anthony V.; Arkin, Adam P.; Zhou, Jizhong

doi:10.1186/1471-2164-10-131

Cited by 53 publications

(49 citation statements)

References 52 publications

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“…Among the genes induced by both iron limitation and heavy metal stress (mainly cadmium stress), there are those related to oxidative stress defense (CC0141, CC0994, CC1316), detoxification efflux pumps (CC3195, CC3197), DNA repair (CC2590) and nucleotide biosynthesis (CC0260, CC3492) (Table 3). Interestingly, 12 heat shock genes, encoding chaperones, proteases and small heat shock proteins, were also upregulated by iron limitation, as well as some genes encoding peptidases containing metals as cofactors (Table 3), what is consistent with previous observations in Shewanella oneidensis [38]. Induction of these genes might be directly mediated by the heat shock sigma factor RpoH (σ 32 ), for the reason that the own rpoH gene (CC3098) is upregulated in iron limitation (Table 3).…”

Section: Resultssupporting

confidence: 90%

“…Comparing our microarray data with other large-scale transcriptomic studies performed under iron-limiting condition in bacteria from diverse taxonomic groups [21,28,38,41,42], we observed that, in spite of the multiplicity of regulatory mechanisms, the core of iron-regulated genes is extremely conserved, including mainly those related to transport, use and storage of this metal. Some responses seems to be confined to few bacteria, such as upregulation of the heat shock response, also described in S. oneidensis [38] and downregulation of chemotaxis and motility, observed in S. meliloti [41] and A. baumannii [42].…”

Section: Resultsmentioning

confidence: 55%

“…Some responses seems to be confined to few bacteria, such as upregulation of the heat shock response, also described in S. oneidensis [38] and downregulation of chemotaxis and motility, observed in S. meliloti [41] and A. baumannii [42]. However, our study expands the range of genes involved in iron homeostasis when we consider physiological processes unique to the C. crescentus lifestyle, such as adaptation to growing in oligotrophic environments and under different oxygen tensions.…”

Section: Resultsmentioning

confidence: 99%

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Global transcriptional response of Caulobacter crescentus to iron availability

2013

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BackgroundIn the alpha subclass of proteobacteria iron homeostasis is controlled by diverse iron responsive regulators. Caulobacter crescentus, an important freshwater α-proteobacterium, uses the ferric uptake repressor (Fur) for such purpose. However, the impact of the iron availability on the C. crescentus transcriptome and an overall perspective of the regulatory networks involved remain unknown.ResultsIn this work we report the identification of iron-responsive and Fur-regulated genes in C. crescentus using microarray-based global transcriptional analyses. We identified 42 genes that were strongly upregulated both by mutation of fur and by iron limitation condition. Among them, there are genes involved in iron uptake (four TonB-dependent receptor gene clusters, and feoAB), riboflavin biosynthesis and genes encoding hypothetical proteins. Most of these genes are associated with predicted Fur binding sites, implicating them as direct targets of Fur-mediated repression. These data were validated by β-galactosidase and EMSA assays for two operons encoding putative transporters. The role of Fur as a positive regulator is also evident, given that 27 genes were downregulated both by mutation of fur and under low-iron condition. As expected, this group includes many genes involved in energy metabolism, mostly iron-using enzymes. Surprisingly, included in this group are also TonB-dependent receptors genes and the genes fixK, fixT and ftrB encoding an oxygen signaling network required for growth during hypoxia. Bioinformatics analyses suggest that positive regulation by Fur is mainly indirect. In addition to the Fur modulon, iron limitation altered expression of 113 more genes, including induction of genes involved in Fe-S cluster assembly, oxidative stress and heat shock response, as well as repression of genes implicated in amino acid metabolism, chemotaxis and motility.ConclusionsUsing a global transcriptional approach, we determined the C. crescentus iron stimulon. Many but not all of iron responsive genes were directly or indirectly controlled by Fur. The iron limitation stimulon overlaps with other regulatory systems, such as the RpoH and FixK regulons. Altogether, our results showed that adaptation of C. crescentus to iron limitation not only involves increasing the transcription of iron-acquisition systems and decreasing the production of iron-using proteins, but also includes novel genes and regulatory mechanisms.

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Section: Resultssupporting

confidence: 90%

Section: Resultsmentioning

confidence: 55%

Section: Resultsmentioning

confidence: 99%

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Global transcriptional response of Caulobacter crescentus to iron availability

2013

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“…As a result, more free Fe 2ϩ is sequestered by Dps, triggering a requirement for iron. To test this notion, we evaluated the intracellular free-iron content by measuring the expression of the ryhB gene, whose product is a small RNA responding to free Fe 2ϩ to regulate the expression of genes involved in iron metabolism (43,44). The results demonstrated that the ryhB promoter activities of the wild-type and ⌬oxyR strains were not significantly different under the same conditions, suggesting that their free-iron levels are comparable (see Fig.…”

Section: Figmentioning

confidence: 97%

Unraveling the Mechanism for the Viability Deficiency of Shewanella oneidensis oxyR Null Mutant

et al. 2015

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Oxidative stresses triggered by reactive oxygen species (ROS) that damage various cellular components are unavoidable for virtually all living organisms. In defense, microorganisms have evolved sophisticated mechanisms to sense, respond to, and battle against ROS. Shewanella oneidensis, an important research model for applied and environmental microbes, employs OxyR to mediate the response to H 2 O 2 by derepressing the production of the major H 2 O 2 scavenger KatB as a major means toward these goals. Surprisingly, despite enhanced H 2 O 2 degradation, the oxyR mutant carries a viability deficiency phenotype (plating defect), which can be suppressed by the addition of exogenous iron species. Experiments showed that the defect was not due to iron starvation. Rather, multiple lines of evidence suggested that H 2 O 2 generated abiotically in lysogeny broth (LB) is responsible for the defect by quickly killing mutant cells. We then showed that the iron species suppressed the plating defect by two distinct mechanisms, either as an H 2 O 2 scavenger without involving living cells or as an environmental cue to stimulate an OxyR-independent response to help cells cope with oxidative stress. Based on the suppression of the plating defect by overproduction of H 2 O 2 scavengers in vivo, we propose that cellular components that are vulnerable to H 2 O 2 and responsible for the defect may reside outside the cytoplasm. IMPORTANCEIn bacteria, OxyR is the major regulator controlling the cellular response to H 2 O 2 . The loss of OxyR results in reduced viability in many species, but the underlying mechanism is unknown. We showed in S. oneidensis that this defect was due to H 2 O 2 generated abiotically in LB. We then showed that this defect could be corrected by the addition of Fe 2؉ or catalase to the LB or increased intracellular production of catalase. Further analyses revealed that Fe 2؉ was able not only to decompose H 2 O 2 directly but also to stimulate the activity of OxyR-independent H 2 O 2 -scavenging enzymes. Our data indicate that iron species play a previously underappreciated role in protecting cells from H 2 O 2 in environments.

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“…Signal intensities were quantified and processed using the data analysis pipeline as previously described (Yang et al, 2009;He et al, 2010;Yang et al, 2013). Then processed GeoChip data were analyzed using the following steps: (i) remove the poor quality spots, which were flagged as 1 or 3 by ImaGene (Arrayit, Sunnyvale, CA, USA) or with a signal to noise ratio of less than 2.0; (ii) normalize the signal intensity of each spot by dividing the signal intensity by the total intensity of the microarray followed by multiplying by a constant; (iii) transform the data to the natural logarithmic form; and (iv) remove genes detected in only one out of three samples from the same elevation.…”

Section: Data Analysesmentioning

confidence: 99%

The microbial gene diversity along an elevation gradient of the Tibetan grassland

et al. 2013

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Tibet is one of the most threatened regions by climate warming, thus understanding how its microbial communities function may be of high importance for predicting microbial responses to climate changes. Here, we report a study to profile soil microbial structural genes, which infers functional roles of microbial communities, along four sites/elevations of a Tibetan mountainous grassland, aiming to explore the potential microbial responses to climate changes via a strategy of space-for-time substitution. Using a microarray-based metagenomics tool named GeoChip 4.0, we showed that microbial communities were distinct for most but not all of the sites. Substantial variations were apparent in stress, N and C-cycling genes, but they were in line with the functional roles of these genes. Cold shock genes were more abundant at higher elevations. Also, gdh converting ammonium into urea was more abundant at higher elevations, whereas ureC converting urea into ammonium was less abundant, which was consistent with soil ammonium contents. Significant correlations were observed between N-cycling genes (ureC, gdh and amoA) and nitrous oxide flux, suggesting that they contributed to community metabolism. Lastly, we found by Canonical correspondence analysis, Mantel tests and the similarity tests that soil pH, temperature, NH 4 þ -N and vegetation diversity accounted for the majority (81.4%) of microbial community variations, suggesting that these four attributes were major factors affecting soil microbial communities. On the basis of these observations, we predict that climate changes in the Tibetan grasslands are very likely to change soil microbial community functional structure, with particular impacts on microbial N-cycling genes and consequently microbe-mediated soil N dynamics.

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Snapshot of iron response in Shewanella oneidensis by gene network reconstruction

Cited by 53 publications

References 52 publications

Global transcriptional response of Caulobacter crescentus to iron availability

Global transcriptional response of Caulobacter crescentus to iron availability

Unraveling the Mechanism for the Viability Deficiency of Shewanella oneidensis oxyR Null Mutant

The microbial gene diversity along an elevation gradient of the Tibetan grassland

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