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Snapshot of iron response in Shewanella oneidensis by gene network reconstruction.

Yang Y, Harris DP, Luo F, Xiong W, Joachimiak M, Wu L, Dehal P, Jacobsen J, Yang Z, Palumbo AV, Arkin AP, Zhou J - BMC Genomics (2009)

Bottom Line: Disruption of a novel transcriptional factor (SO1415) caused deficiency in both anaerobic iron reduction and growth with thiosulfate or TMAO as an electronic acceptor, suggesting that SO1415 is required for specific branches of anaerobic energy metabolism pathways.Using a reconstructed gene network, we identified major biological pathways that were differentially expressed during iron depletion and repletion.Genetic studies not only demonstrated the importance of iron acquisition and protein degradation for iron depletion, but also characterized a novel transcriptional factor (SO1415) with a role in anaerobic energy metabolism.

View Article: PubMed Central - HTML - PubMed

Affiliation: Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USA. yangy@ornl.gov

ABSTRACT

Background: Iron homeostasis of Shewanella oneidensis, a gamma-proteobacterium possessing high iron content, is regulated by a global transcription factor Fur. However, knowledge is incomplete about other biological pathways that respond to changes in iron concentration, as well as details of the responses. In this work, we integrate physiological, transcriptomics and genetic approaches to delineate the iron response of S. oneidensis.

Results: We show that the iron response in S. oneidensis is a rapid process. Temporal gene expression profiles were examined for iron depletion and repletion, and a gene co-expression network was reconstructed. Modules of iron acquisition systems, anaerobic energy metabolism and protein degradation were the most noteworthy in the gene network. Bioinformatics analyses suggested that genes in each of the modules might be regulated by DNA-binding proteins Fur, CRP and RpoH, respectively. Closer inspection of these modules revealed a transcriptional regulator (SO2426) involved in iron acquisition and ten transcriptional factors involved in anaerobic energy metabolism. Selected genes in the network were analyzed by genetic studies. Disruption of genes encoding a putative alcaligin biosynthesis protein (SO3032) and a gene previously implicated in protein degradation (SO2017) led to severe growth deficiency under iron depletion conditions. Disruption of a novel transcriptional factor (SO1415) caused deficiency in both anaerobic iron reduction and growth with thiosulfate or TMAO as an electronic acceptor, suggesting that SO1415 is required for specific branches of anaerobic energy metabolism pathways.

Conclusion: Using a reconstructed gene network, we identified major biological pathways that were differentially expressed during iron depletion and repletion. Genetic studies not only demonstrated the importance of iron acquisition and protein degradation for iron depletion, but also characterized a novel transcriptional factor (SO1415) with a role in anaerobic energy metabolism.

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(A) Reduction of Fe(III) citrate by MR-1 and SO1415 mutant. (B) Anaerobic growth curves of MR-1 and SO1415 mutant with thiosulfate as the electron acceptor. (C) Anaerobic growth curves of MR-1 and SO1415 mutant with TMAO as the electron acceptor.
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Figure 5: (A) Reduction of Fe(III) citrate by MR-1 and SO1415 mutant. (B) Anaerobic growth curves of MR-1 and SO1415 mutant with thiosulfate as the electron acceptor. (C) Anaerobic growth curves of MR-1 and SO1415 mutant with TMAO as the electron acceptor.

Mentions: Network analysis suggests that ten novel transcriptional factors might be involved in anaerobic energy metabolism. Among them, one gene (SO1415) was successfully inactivated from the MR-1 genome. The Fe(III) reduction rates of the SO1415 mutant and MR-1 were assessed by a ferrozine assay as described [35]. Less than half the amount of Fe(II) was produced in the mutant as compared to MR-1 after four hours of incubation (Fig. 5A), indicating that disruption of SO1415 impaired anaerobic Fe(III) reduction.


Snapshot of iron response in Shewanella oneidensis by gene network reconstruction.

Yang Y, Harris DP, Luo F, Xiong W, Joachimiak M, Wu L, Dehal P, Jacobsen J, Yang Z, Palumbo AV, Arkin AP, Zhou J - BMC Genomics (2009)

(A) Reduction of Fe(III) citrate by MR-1 and SO1415 mutant. (B) Anaerobic growth curves of MR-1 and SO1415 mutant with thiosulfate as the electron acceptor. (C) Anaerobic growth curves of MR-1 and SO1415 mutant with TMAO as the electron acceptor.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2667191&req=5

Figure 5: (A) Reduction of Fe(III) citrate by MR-1 and SO1415 mutant. (B) Anaerobic growth curves of MR-1 and SO1415 mutant with thiosulfate as the electron acceptor. (C) Anaerobic growth curves of MR-1 and SO1415 mutant with TMAO as the electron acceptor.
Mentions: Network analysis suggests that ten novel transcriptional factors might be involved in anaerobic energy metabolism. Among them, one gene (SO1415) was successfully inactivated from the MR-1 genome. The Fe(III) reduction rates of the SO1415 mutant and MR-1 were assessed by a ferrozine assay as described [35]. Less than half the amount of Fe(II) was produced in the mutant as compared to MR-1 after four hours of incubation (Fig. 5A), indicating that disruption of SO1415 impaired anaerobic Fe(III) reduction.

Bottom Line: Disruption of a novel transcriptional factor (SO1415) caused deficiency in both anaerobic iron reduction and growth with thiosulfate or TMAO as an electronic acceptor, suggesting that SO1415 is required for specific branches of anaerobic energy metabolism pathways.Using a reconstructed gene network, we identified major biological pathways that were differentially expressed during iron depletion and repletion.Genetic studies not only demonstrated the importance of iron acquisition and protein degradation for iron depletion, but also characterized a novel transcriptional factor (SO1415) with a role in anaerobic energy metabolism.

View Article: PubMed Central - HTML - PubMed

Affiliation: Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USA. yangy@ornl.gov

ABSTRACT

Background: Iron homeostasis of Shewanella oneidensis, a gamma-proteobacterium possessing high iron content, is regulated by a global transcription factor Fur. However, knowledge is incomplete about other biological pathways that respond to changes in iron concentration, as well as details of the responses. In this work, we integrate physiological, transcriptomics and genetic approaches to delineate the iron response of S. oneidensis.

Results: We show that the iron response in S. oneidensis is a rapid process. Temporal gene expression profiles were examined for iron depletion and repletion, and a gene co-expression network was reconstructed. Modules of iron acquisition systems, anaerobic energy metabolism and protein degradation were the most noteworthy in the gene network. Bioinformatics analyses suggested that genes in each of the modules might be regulated by DNA-binding proteins Fur, CRP and RpoH, respectively. Closer inspection of these modules revealed a transcriptional regulator (SO2426) involved in iron acquisition and ten transcriptional factors involved in anaerobic energy metabolism. Selected genes in the network were analyzed by genetic studies. Disruption of genes encoding a putative alcaligin biosynthesis protein (SO3032) and a gene previously implicated in protein degradation (SO2017) led to severe growth deficiency under iron depletion conditions. Disruption of a novel transcriptional factor (SO1415) caused deficiency in both anaerobic iron reduction and growth with thiosulfate or TMAO as an electronic acceptor, suggesting that SO1415 is required for specific branches of anaerobic energy metabolism pathways.

Conclusion: Using a reconstructed gene network, we identified major biological pathways that were differentially expressed during iron depletion and repletion. Genetic studies not only demonstrated the importance of iron acquisition and protein degradation for iron depletion, but also characterized a novel transcriptional factor (SO1415) with a role in anaerobic energy metabolism.

Show MeSH