Greigite or magnetite: Environmental and genetic determinants controlling biomineralization in magnetotactic bacteria

• Applicant: Dr. Damien Faivre
• Subject Area: Microbial Ecology and Applied Microbiology ; Biological and Biomimetic Chemistry ; Biomaterials ; Metabolism, Biochemistry and Genetics of Microorganisms ; Structural Biology
• Term: from 2014 to 2019
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 258774416

• Final Report Year: 2019

Final Report Abstract

In 2011, a new magnetotactic bacteria, Desulfamplus magnetovallimortis strain BW-1, was isolated from the Death Valley in California and cultivate in the laboratory. These bacteria are unique because of their ability to intracellularly biomineralize nanocrystals composed of either magnetite (an iron oxide of the formula Fe304) or greigite (an iron sulfide of the formula Fe3S4) within the magnetosome. This bacterial organelle allows them to navigate along magnetic field lines and the formation of magnetite and / or greigite crystals depends on culture conditions. The bacterial genome was sequenced, revealing the existence of two gene clusters potentially responsible for the synthesis of the two types of minerals. GROMA's objective is to use an integrated and multidisciplinary approach to understand the genetic and environmental determinants that lead the BW-1 model strain to biomineralize each type of mineral. Understanding these fundamental mechanisms of in vivo biomineralization can provide new and effective methods for the in vitro or in vivo production of nanoparticles of interest for biotechnological applications, particularly in the biomedical field. One of the technical challenges of the project was to control the culture conditions of the strain in order to obtain reproducible magnetite or greigite magnetosomes, depending on the physico­chemical conditions applied to the culture. These microbiological approaches have been combined with transmission electron microscopy observations to characterize biomineralized crystals. In order to determine the genes induced or repressed in the biomineralization mechanism, a global transcriptomics approach (RNA sequencing) was conducted and then supplemented by a proteomic analysis to identify the most abundant proteins in different culture conditions. Finally, the purification of recombinant proteins that can play a major role in the biomineralization process has been carried out and has allowed a first characterization of their functional properties. This study allowed a thorough characterization of the phylogeny and physiology of the BW-1 model strain. The approaches developed have also demonstrated that the biomineralization process leading to the formation of either greigite or magnetite is governed by environmental (notably via redox potential) and genetic (via two dedicated and differentially expressed gene clusters) control. These results contribute to the understanding of fundamental biomineralization processes and will feed into more applied studies by characterizing greigite crystals as contrast agents in medical imaging. The main unexpected result was the extracellular formation of iron sulfur particles and the difficulty encountered to design a process leading to cells devoid of any contaminating sample. This led to unexpected drawback and loss of time.

Publications

• 2016. Controlled Biomineralization of Magnetite in Bacteria, p. 99-116. In Faivre, D (ed.). Iron Oxides. Weinheim, Wiley-VCH Verlag
  Descamps ECT, Abbé J-B, Pignol D, Lefèvre CT
  
• 2016. Elongated magnetite nanoparticle formation from a solid ferrous precursor in a magnetotactic bacterium. Journal of the Royal Society Interface
  Baumgartner J, Menguy N, Gonzalez TP, Morin G, Widdrat M, Faivre D
  
• 2016. Growth of magnetotactic sulfate-reducing bacteria in oxygen concentration gradient medium. Environmental Microbiology Reports
  Lefèvre CT, Howse PA, Schmidt ML, Sabaty M, Menguy N, Luther GW, Bazylinski DA
  
• 2017. Desulfamplus magnetovallimortis gen. nov., sp. nov., a magnetotactic bacterium from a brackish desert spring able to biomineralize greigite and magnetite, that represents a novel lineage in the Desulfobacteraceae. Systematic Applied Microbiology
  Descamps ECT, Monteil CL, Menguy N, Ginet N, Pignol D, Bazylinski DA, Lefèvre CT
  
• 2018. Accumulation and Dissolution of Magnetite Crystals in a Magnetically Responsive Ciliate. Applied and Environmental Microbiology
  Monteil CL, Menguy N, Prévéral S, Warren A, Pignol D, Lefèvre CT
  
• 2018. Genomic study of a novel magnetotactic Alphaproteobacteria uncovers the multiple ancestry of magnetotaxis. Environmental Microbiology
  Monteil CL, Perrière G, Menguy N, Ginet N, Alonso B, Waisbord N, Cruveiller S, Pignol D, Lefèvre CT
  
• 2019. Swimming with magnets: From biological organisms to synthetic devices. Physics Reports
  Klumpp S, Lefèvre CT, Bennet M, Faivre D