Abstract

Magnetotactic bacteria (MTB) are a large, polyphyletic group of aquatic microorganisms capable of absorbing large amounts of iron and synthesizing intercellular nano-scaled nanoparticles termed magnetosomes. In our previous transcriptomic studies, we discovered that a novel gene (MGMSRv2_2046, termed as mg2046) in Magnetospirillum gryphiswaldense strain MSR-1 was significantly up-regulated during the period of magnetosome synthesis. In the present study, we constructed a MSR-1 mutant strain with deletion of mg2046 (termed Δmg2046) in order to evaluate the role of this gene in cell physiological status and magnetosome formation process. In comparison with wild-type MSR-1, Δmg2046 showed similar cell growth, but much lower cell magnetic response, smaller number and size of magnetosomes, and reduced iron absorption ability. mg2046 deletion evidently disrupted iron uptake, and redox equilibrium, and strongly inhibited transcription of dissimilatory denitrification pathway genes. Our experimental findings, taken together with results of gene homology analysis, indicate that Mg2046 acts as a positive regulator in MSR-1 under microaerobic conditions, responding to hypoxia signals and participating in regulation of oxygen metabolism, in part as a co-regulator of dissimilatory denitrification pathway with oxygen sensor MgFnr (MGMSRv2_2946, termed as Mg2946). Mg2046 is clearly involved in coupled regulation of cellular oxygen, iron and nitrogen metabolism under micro-aerobic or anaerobic conditions. Our findings help explain how MSR-1 cells initiate dissimilatory denitrification pathway and overcome energy deficiency under microaerobic conditions, and have broader implications regarding bacterial survival and energy metabolism strategies under hypoxia.

Highlights

  • Magnetotactic bacteria (MTB) are a polyphyletic group of prokaryotes found in aquatic and sedimentary environments worldwide (Faivre and Schüler, 2008)

  • Our findings suggest that Mg2046 is involved indirectly in the early stage of magnetosome synthesis, and directly in the mature stage through regulation of various metabolic pathways – redox reactions driven by terminal oxidases and dissimilatory denitrification

  • This study was focused on the role of novel protein Mg2046 in MSR-1 cell growth and magnetosome synthesis

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Summary

Introduction

Magnetotactic bacteria (MTB) are a polyphyletic group of prokaryotes found in aquatic and sedimentary environments worldwide (Faivre and Schüler, 2008). MTB play a key role in environmental iron cycling in view of their worldwide distribution and capacity for iron assimilation into magnetosome. Clustering of mam and mms (magnetosome membrane protein genes) typically observed in magnetosome island (MAI, part of MTB genome), is genetic determinant of magnetite biomineralization (Komeili, 2012). This sophisticated, stepwise process has been extensively studied based on deletion of single, multi, or full operon of these genes (Murat et al, 2010; Quinlan et al, 2011; Raschdorf et al, 2013; Lohse et al, 2014, 2016). Increasing experimental evidence shows clearly that magnetosome synthesis in MTB is controlled by mam/mms genes and various genes related to basic cellular metabolism in MTB

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