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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) Growth of SO3032 mutant and its parent strain DSP10 were compared in the presence of 120 μM 2,2'-dipyridyl. Cell density was measured at OD600 every 30 min for five days. Data are averages for triplicate cultures. (B) Growth of SO3032 mutant and DSP10 were compared in the presence of 160 μM 2,2'-dipyridyl. (C) Experimental verification of the involvement of SO2017 in iron response. Both strains were grown to OD600 of 0.6 before transferring to fresh LB medium in 1:100 dilutions with or without 240 μM 2,2'-dipyridyl.
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Figure 4: (A) Growth of SO3032 mutant and its parent strain DSP10 were compared in the presence of 120 μM 2,2'-dipyridyl. Cell density was measured at OD600 every 30 min for five days. Data are averages for triplicate cultures. (B) Growth of SO3032 mutant and DSP10 were compared in the presence of 160 μM 2,2'-dipyridyl. (C) Experimental verification of the involvement of SO2017 in iron response. Both strains were grown to OD600 of 0.6 before transferring to fresh LB medium in 1:100 dilutions with or without 240 μM 2,2'-dipyridyl.

Mentions: To test the importance of iron acquisition genes under iron depleted conditions, a putative alcaligin biosynthesis protein SO3032 was selected for examination. A mutant of SO3032 and its parental strain DSP10 were compared under iron depleted conditions. The mutant displayed a severe growth defect when grown in the presence of 120 μM iron chelator (Fig. 4A), and had only marginal growth when grown in the presence of 160 μM iron chelator (Fig. 4B). This suggests that SO3032, which is induced ~20 fold after 40 minutes of iron depletion, is required for surviving iron starvation.


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) Growth of SO3032 mutant and its parent strain DSP10 were compared in the presence of 120 μM 2,2'-dipyridyl. Cell density was measured at OD600 every 30 min for five days. Data are averages for triplicate cultures. (B) Growth of SO3032 mutant and DSP10 were compared in the presence of 160 μM 2,2'-dipyridyl. (C) Experimental verification of the involvement of SO2017 in iron response. Both strains were grown to OD600 of 0.6 before transferring to fresh LB medium in 1:100 dilutions with or without 240 μM 2,2'-dipyridyl.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: (A) Growth of SO3032 mutant and its parent strain DSP10 were compared in the presence of 120 μM 2,2'-dipyridyl. Cell density was measured at OD600 every 30 min for five days. Data are averages for triplicate cultures. (B) Growth of SO3032 mutant and DSP10 were compared in the presence of 160 μM 2,2'-dipyridyl. (C) Experimental verification of the involvement of SO2017 in iron response. Both strains were grown to OD600 of 0.6 before transferring to fresh LB medium in 1:100 dilutions with or without 240 μM 2,2'-dipyridyl.
Mentions: To test the importance of iron acquisition genes under iron depleted conditions, a putative alcaligin biosynthesis protein SO3032 was selected for examination. A mutant of SO3032 and its parental strain DSP10 were compared under iron depleted conditions. The mutant displayed a severe growth defect when grown in the presence of 120 μM iron chelator (Fig. 4A), and had only marginal growth when grown in the presence of 160 μM iron chelator (Fig. 4B). This suggests that SO3032, which is induced ~20 fold after 40 minutes of iron depletion, is required for surviving iron starvation.

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
Related in: MedlinePlus