A Hypervariable 130-Kilobase Genomic Region of Magnetospirillum gryphiswaldense Comprises a Magnetosome Island Which Undergoes Frequent Rearrangements during Stationary Growth

Abstract

Genes involved in magnetite biomineralization are clustered in the genome of the magnetotactic bacterium Magnetospirillum gryphiswaldense. We analyzed a 482-kb genomic fragment, in which we identified an approximately 130-kb region representing a putative genomic "magnetosome island" (MAI). In addition to all known magnetosome genes, the MAI contains genes putatively involved in magnetosome biomineralization and numerous genes with unknown functions, as well as pseudogenes, and it is particularly rich in insertion elements. Substantial sequence polymorphism of clones from different subcultures indicated that this region undergoes frequent rearrangements during serial subcultivation in the laboratory. Spontaneous mutants affected in magnetosome formation arise at a frequency of up to 10 ؊2 after prolonged storage of cells at 4°C or exposure to oxidative stress. All nonmagnetic mutants exhibited extended and multiple deletions in the MAI and had lost either parts of or the entire mms and mam gene clusters encoding magnetosome proteins. The mutations were polymorphic with respect to the sites and extents of deletions, but all mutations were found to be associated with the loss of various copies of insertion elements, as revealed by Southern hybridization and PCR analysis. Insertions and deletions in the MAI were also found in different magnetosome-producing clones, indicating that parts of this region are not essential for the magnetic phenotype. Our data suggest that the genomic MAI undergoes frequent transposition events, which lead to subsequent deletion by homologous recombination under physiological stress conditions. This can be interpreted in terms of adaptation to physiological stress and might contribute to the genetic plasticity and mobilization of the magnetosome island.

Deciphering unusual uncultured magnetotactic multicellular prokaryotes through genomics

“…In addition, there was also the possibility of gene loss, for example, the loss of mam genes, which has been shown to occur in cultures of some magnetotactic bacteria that also lost the magnetotactic trait (Ullrich et al, 2005;Kolinko et al, 2011). This unique application of genomic sequencing and analysis of microbial environmental DNA contributed to the understanding of many physiological features involved in the behavior and multicellular life of Ca.…”

Magnetosome-containing bacteria living as symbionts of bivalves

“…gouldi represent one of the few described magnetotactic gammaproteobacteria (Simmons et al, 2004;Lefèvre et al, 2012;Wang et al, 2013). Genomic studies have shown that genes responsible for magnetosome formation are often organized within 'magnetosome islands' that contain mobile elements (Ullrich et al, 2005;Jogler et al, 2009), and recent work suggests a monophyletic origin for magnetotaxis within the proteobacteria (Lefèvre et al, 2013b). Inclusions resembling magnetosomes, but interpreted as viruses, have been noted in other thyasirid symbionts, notably in 'symbiont of Thyasira flexuosa 1' from the Mediterranean, in Figure 4; (Brissac et al, 2011), in symbionts of T. gouldi from Scotland (Southward and Southward, 1991) and of T. flexuosa from Long Beach, USA (Dufour, 2005) and Brest, France (J. Laurich, personal communication).…”

Formation of magnetite by bacteria and its application

“…A spontaneous non-magnetic mutant that lacks the magnetosome island was also obtained with the M. gryphiswaldense MSR-1 strain (Schübbe et al 2003). Various phenotypes showing altered numbers, sizes and alignment of BacMPs were isolated and analysed (Ullrich et al 2005). The mutants revealed several deletions in different regions, suggesting the occurrence of frequent transposition events in the cell.…”