Dissociation between Iron and Heme Biosyntheses Is Largely Accountable for Respiration Defects of Shewanella oneidensis fur Mutants
Fu, Huihui1,2,3; Liu, Lulu1,2; Dong, Ziyang1,2; Guo, Shupan1,2; Gao, Haichun1,2
Corresponding AuthorGao, Haichun(
AbstractIron, a major protein cofactor, is essential for most organisms but can simultaneously be toxic. Iron homeostasis thus has to be effectively maintained under a range of iron regimes. This may be particularly true with Shewanella oneidensis, a representative of dissimilatory metal-reducing bacteria (DMRB), which are capable of respiring a variety of chemicals as electron acceptors (EAs), including iron ores. Although iron respiration and its regulation have been extensively studied in this bacterium, how iron homeostasis is maintained remains largely unknown. Here, we report that the loss of the iron homeostasis master regulator Fur negatively affects the respiration of all EAs tested. This defect appears mainly to be a result of reduced cytochrome c (cyt c) production, despite a decrease in the expression of reductases that are under the direct control of Fur. We also show that S. oneidensis Fur interacts with canonical Fur box motifs in F-F-x-R configuration rather than the palindromic motif proposed before. The fur mutant has lowered total iron and increased free iron contents. Under iron-rich conditions, overproduction of the major iron storage protein Bfr elevates the total iron levels of the fur mutant over those of the wildtype but does not affect free iron levels. Intriguingly, such an operation only marginally improves cyt c production by affecting heme b biosynthesis. It is established that iron dictates heme b/cyt c biosynthesis in S. oneidensis fur(+) strains, but the fur mutation annuls the dependence of heme b/cyt c biosynthesis on iron. Overall, our results suggest that Fur has a profound impact on the iron homeostasis of S. oneidensis, through which many physiological processes, especially respiration, are transformed. IMPORTANCE Iron reduction is a signature of S. oneidensis, and this process relies on a large number of type c cytochromes, which per se are iron-containing proteins. Thus, iron plays an essential and special role in iron respiration, but to date, the nature of iron metabolism and regulation of the bacterium remains largely unknown. In this study, we investigated impacts of Fur, the master regulator of iron homeostasis, on respiration. The loss of Fur causes a general defect in respiration, a result of impaired cyt c production rather than specific regulation. Additionally, the fur mutant is unresponsive to iron, resulting in imbalanced iron homeostasis and dissociation between iron and cyt c production. These findings provide important insights into the iron biology of DMRB.
Keywordiron homeostasis Shewanella Fur regulation respiration cytochrome c
Indexed BySCI
Funding ProjectNational Natural Science Foundation of China[41476105] ; Natural Science Foundation of Zhejiang Province[LZ17C010001]
WOS Research AreaBiotechnology & Applied Microbiology ; Microbiology
WOS SubjectBiotechnology & Applied Microbiology ; Microbiology
WOS IDWOS:000429665700001
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Cited Times:4[WOS]   [WOS Record]     [Related Records in WOS]
Document Type期刊论文
Corresponding AuthorGao, Haichun
Affiliation1.Zhejiang Univ, Inst Microbiol, Hangzhou, Zhejiang, Peoples R China
2.Zhejiang Univ, Coll Life Sci, Hangzhou, Zhejiang, Peoples R China
3.Chinese Acad Sci, Inst Oceanol, Qingdao, Shandong, Peoples R China
First Author AffilicationInstitute of Oceanology, Chinese Academy of Sciences
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Fu, Huihui,Liu, Lulu,Dong, Ziyang,et al. Dissociation between Iron and Heme Biosyntheses Is Largely Accountable for Respiration Defects of Shewanella oneidensis fur Mutants[J]. APPLIED AND ENVIRONMENTAL MICROBIOLOGY,2018,84(8):18.
APA Fu, Huihui,Liu, Lulu,Dong, Ziyang,Guo, Shupan,&Gao, Haichun.(2018).Dissociation between Iron and Heme Biosyntheses Is Largely Accountable for Respiration Defects of Shewanella oneidensis fur Mutants.APPLIED AND ENVIRONMENTAL MICROBIOLOGY,84(8),18.
MLA Fu, Huihui,et al."Dissociation between Iron and Heme Biosyntheses Is Largely Accountable for Respiration Defects of Shewanella oneidensis fur Mutants".APPLIED AND ENVIRONMENTAL MICROBIOLOGY 84.8(2018):18.
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