Genetic and Ultrastructural Analysis Reveals the Key Players and Initial Steps of Bacterial Magnetosome Membrane Biogenesis.
Magnetosomes of magnetotactic bacteria contain well-ordered nanocrystals for magnetic navigation and have recently emerged as the most sophisticated model system to study the formation of membrane bounded organelles in prokaryotes. Magnetosome biosynthesis is thought to begin with the formation of a dedicated compartment, the magnetosome membrane (MM), in which the biosynthesis of a magnetic mineral is strictly controlled. While the biomineralization of magnetosomes and their subsequent assembly into linear chains recently have become increasingly well studied, the molecular mechanisms and early stages involved in MM formation remained poorly understood. In the Alphaproteobacterium Magnetospirillum gryphiswaldense, approximately 30 genes were found to control magnetosome biosynthesis. By cryo-electron tomography of several key mutant strains we identified the gene complement controlling MM formation in this model organism. Whereas the putative magnetosomal iron transporter MamB was most crucial for the process and caused the most severe MM phenotype upon elimination, MamM, MamQ and MamL were also required for the formation of wild-type-like MMs. A subset of seven genes (mamLQBIEMO) combined within a synthetic operon was sufficient to restore the formation of intracellular membranes in the absence of other genes from the key mamAB operon. Tracking of de novo magnetosome membrane formation by genetic induction revealed that magnetosomes originate from unspecific cytoplasmic membrane locations before alignment into coherent chains. Our results indicate that no single factor alone is essential for MM formation, which instead is orchestrated by the cumulative action of several magnetosome proteins.
Department Biology I-Microbiology, Ludwig Maximilian University Munich, Planegg-Martinsried, Germany.|Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Planegg-Martinsried, Germany.
Oliver
0000-0003-1558-059X
O
Raschdorf
Department Biology I-Microbiology, Ludwig Maximilian University Munich, Planegg-Martinsried, Germany.
Yvonne
0000-0001-6910-2273
Y
Forstner
Department Biology I-Microbiology, Ludwig Maximilian University Munich, Planegg-Martinsried, Germany.
Isabel
I
Kolinko
Department of Microbiology, University of Bayreuth, Bayreuth, Germany.
René
R
Uebe
Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Planegg-Martinsried, Germany.
Jürgen M
0000-0002-6402-8315
JM
Plitzko
Department of Microbiology, University of Bayreuth, Bayreuth, Germany.
Dirk
D
Schüler
D027682:Cation Transport Proteins / Q000235:genetics; D002462:Cell Membrane / Q000378:metabolism*; D052203:Ferrosoferric Oxide / Q000378:metabolism; D007501:Iron / Q000378:metabolism; D055944:Magnetosomes / Q000235:genetics / Q000378:metabolism / Q000648:ultrastructure; D042201:Magnetospirillum / Q000235:genetics / Q000378:metabolism*
D027682:Cation Transport Proteins; D007501:Iron; D052203:Ferrosoferric Oxide