A novel role for Crp in controlling magnetosome biosynthesis in Magnetospirillum gryphiswaldense MSR-1

Tong Wen,Wei Jiang,Ying Li,Fangfang Guo,Yunpeng Zhang,Jiesheng Tian,Jilun Li

doi:10.1038/srep21156

Tong Wen, Wei Jiang + Show 5 more

Open Access

https://doi.org/10.1038/srep21156

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Journal: Scientific Reports	Publication Date: Feb 1, 2016
Citations: 8	License type: CC BY 4.0

Affiliation: China Agricultural University

Abstract

Magnetotactic bacteria (MTB) are specialized microorganisms that synthesize intracellular magnetite particles called magnetosomes. Although many studies have focused on the mechanism of magnetosome synthesis, it remains unclear how these structures are formed. Recent reports have suggested that magnetosome formation is energy dependent. To investigate the relationship between magnetosome formation and energy metabolism, a global regulator, named Crp, which mainly controls energy and carbon metabolism in most microorganisms, was genetically disrupted in Magnetospirillum gryphiswaldense MSR-1. Compared with the wild-type or complemented strains, the growth, ferromagnetism and intracellular iron content of crp-deficient mutant cells were dramatically decreased. Transmission electron microscopy (TEM) showed that magnetosome synthesis was strongly impaired by the disruption of crp. Further gene expression profile analysis showed that the disruption of crp not only influenced genes related to energy and carbon metabolism, but a series of crucial magnetosome island (MAI) genes were also down regulated. These results indicate that Crp is essential for magnetosome formation in MSR-1. This is the first time to demonstrate that Crp plays an important role in controlling magnetosome biomineralization and provides reliable expression profile data that elucidate the mechanism of Crp regulation of magnetosome formation in MSR-1.

Highlights

Magnetosomes are intracellular biological membrane-enveloped nano-sized magnetic particles formed by magnetotactic bacteria (MTB)[1,2]
The results indicate that many pathways involved in carbon and energy metabolism were affected by the deletion of crp, including those involved in pentose and glucuronate interconversions, oxidative phosphorylation and peptidoglycan biosynthesis
By comparing with the previously reported MgFnr (MGR_2553) of Crp/Fnr family protein in MSR-118, along with two other Crp/Fnr family proteins from E. coli (U068_c0718, GenBank: CP011342.2) and Caulobacter crescentus (Caul_2975, GenBank: CP000927.1), an alphaproteobacterial model organism which is closely related to MSR-119, a high homology is shown among the four proteins in their cyclic nucleotide-binding domain (Fig. 1 blue frame) and HTH DNA-binding domain (Fig. 1 red frame)

Summary

Introduction

Magnetosomes are intracellular biological membrane-enveloped nano-sized magnetic particles formed by magnetotactic bacteria (MTB)[1,2]. A magnetosome membrane protein, MamK, has been shown to function as both an ATPase and a GTPase[10] These results suggest that the synthesis of the magnetosome in MTB is an energy-dependent process and that the metabolic energy in the cell influences magnetosome formation. To investigate the relationship between magnetosome formation and energy metabolism, we disrupted the crp gene in Magnetospirillum gryphiswaldense MSR-1 and complemented the mutant strain. To understand the mechanism of Crp regulation of magnetosome synthesis in M. gryphiswaldense MSR-1, transcriptional expression profiles of the MSR-1 wild-type and crp mutant strains were compared. Many genes located on the MAI were down regulated by the disruption of crp These results indicated that the global carbon and energy metabolism regulator Crp plays a key role in controlling magnetosome biosynthesis in M. gryphiswaldense MSR-1

Methods

Results

Conclusion