Greigite or magnetite: Environmental and genetic determinants controlling biomineralization in magnetotactic bacteria
Biological and Biomimetic Chemistry
Biomaterials
Metabolism, Biochemistry and Genetics of Microorganisms
Structural Biology
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
(See online at https://doi.org/10.1002/9783527691395.ch5) - 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
(See online at https://doi.org/10.1098/rsif.2016.0665) - 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
(See online at https://doi.org/10.1111/1758-2229.12479) - 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
(See online at https://doi.org/10.1016/j.syapm.2017.05.001) - 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
(See online at https://doi.org/10.1128/AEM.02865-17) - 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
(See online at https://doi.org/10.1111/1462-2920.14364) - 2019. Swimming with magnets: From biological organisms to synthetic devices. Physics Reports
Klumpp S, Lefèvre CT, Bennet M, Faivre D
(See online at https://doi.org/10.1016/j.physrep.2018.10.007)
