Comparative analysis of magnetosome gene clusters in magnetotactic bacteria provides further evidence for horizontal gene transfer

Abstract

The organization of magnetosome genes was analysed in all available complete or partial genomic sequences of magnetotactic bacteria (MTB), including the magnetosome island (MAI) of the magnetotactic marine vibrio strain MV-1 determined in this study. The MAI was found to differ in gene content and organization between Magnetospirillum species and strains MV-1 or MC-1. Although a similar organization of magnetosome genes was found in all MTB, distinct variations in gene order and sequence similarity were uncovered that may account for the observed diversity of biomineralization, cell biology and magnetotaxis found in various MTB. While several magnetosome genes were present in all MTB, others were confined to Magnetospirillum species, indicating that the minimal set of genes required for magnetosome biomineralization might be smaller than previously suggested. A number of novel candidate genes were implicated in magnetosome formation by gene cluster comparison. Based on phylogenetic and compositional evidence we present a model for the evolution of magnetotaxis within the Alphaproteobacteria, which suggests the independent horizontal transfer of magnetosome genes from an unknown ancestor of magnetospirilla into strains MC-1 and MV-1.

Common ancestry of iron oxide- and iron-sulfide-based biomineralization in magnetotactic bacteria

“…The mms6, mamD, mamC, mamF, mamG, mamJ, mamX and mamY genes, strongly conserved in most magnetite-producing magnetotactic Alphaproteobacteria (Jogler et al, 2009a), were not found in our sequences or in the genome of D. magneticus (Nakazawa et al, 2009). These genes are considered to be of great importance in controlling magnetosome size and morphology in MTB of the Alphaproteobacteria.…”

“…These genes are responsible for controlling the size and morphology of magnetite crystals in MTB, as well as magnetosome chain organization (Schü ler, 2004). Comparisons between the MAIs of different cultured magnetite-producing MTB show that gene content and organization differ among them and are thought to be responsible for differences in magnetosome crystal morphology and size and magnetosome organization (Jogler et al, 2009a).…”

“…According to a current model (Jogler et al, 2009a), magnetite magnetosome genes were acquired by the magnetospirilla, the coccus Candidatus Magnetococcus marinus strain MC-1 (Schü bbe et al, 2009) and the vibrio Candidatus Magnetovibrio blakemorei strain MV-1 (Schü bbe et al, 2009) through independent events of horizontal gene transfer from an unknown ancestor. The close phylogenetic affinity of the magnetospirilla to a genus of photosynthetic bacteria, Phaeospirillum, suggests that the ancestor of these two groups of prokaryotes might have been a phototrophic organism.…”

“…The close phylogenetic affinity of the magnetospirilla to a genus of photosynthetic bacteria, Phaeospirillum, suggests that the ancestor of these two groups of prokaryotes might have been a phototrophic organism. The absence of selective pressure for magnetotaxis and the loss of the MAI might have led to the occurrence of non-magnetotactic representatives within the MTB (Jogler et al, 2009a). This model, however, describes magnetotaxis evolution only within the Alphaproteobacteria and considers only genes related to magnetite biomineralization.…”

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).…”