Snapshot of iron response in Shewanella oneidensis by gene network reconstruction

doi:10.1186/1471-2164-10-131

BMC Genomics. 2009; 10: 131.

Published online 2009 March 25. doi: 10.1186/1471-2164-10-131

PMCID: PMC2667191

Snapshot of iron response in Shewanella oneidensis by gene network reconstruction

Yunfeng Yang,¹ Daniel P Harris,¹ Feng Luo,² Wenlu Xiong,¹ Marcin Joachimiak,³ Liyou Wu,^1,⁴ Paramvir Dehal,³ Janet Jacobsen,⁵ Zamin Yang,¹ Anthony V Palumbo,¹ Adam P Arkin,^3,⁶ and Jizhong Zhou^1,⁴

¹Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA

²School of Computing, Clemson University, Clemson, SC, 29634, USA

³Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA

⁴Institute for Environmental Genomics, and Department of Botany and Microbiology, University of Oklahoma, Norman, OK, 73019, USA

⁵Computational Research Division, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA

⁶Department of Bioengineering, University of California, Berkeley, CA, 94720, USA

Corresponding author.

Yunfeng Yang: yangy/at/ornl.gov; Daniel P Harris: dph12/at/case.edu; Feng Luo: luofeng/at/clemson.edu; Wenlu Xiong: wenlu.xiong/at/gmail.com; Marcin Joachimiak: marcin/at/compbio.berkeley.edu; Liyou Wu: lwu/at/rccc.ou.edu; Paramvir Dehal: PSDehal/at/lbl.gov; Janet Jacobsen: JSJacobsen/at/lbl.gov; Zamin Yang: yangz/at/ornl.gov; Anthony V Palumbo: avp/at/ornl.gov; Adam P Arkin: APArkin/at/lbl.gov; Jizhong Zhou: jzhou/at/rccc.ou.edu

Received October 9, 2008; Accepted March 25, 2009.

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

This article has been cited by other articles in PMC.

Abstract

Background

Iron homeostasis of Shewanella oneidensis, a γ-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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