Monophyletic origin of magnetotaxis and the first magnetosomes

Abstract

Horizontal gene transfer (HGT), the transfer of genetic material other than by descent, is thought to have played significant roles in the evolution and distribution of genes in prokaryotes. These include those responsible for the ability of motile, aquatic magnetotactic bacteria (MTB) to align and swim along magnetic field lines and the biomineralization of magnetosomes that are responsible for this behaviour. There is some genomic evidence that HGT might be responsible for the distribution of magnetosome genes in different phylogenetic groups of bacteria. For example, in the genomes of a number of MTB, magnetosome genes are present as clusters within a larger structure known as the magnetosome genomic island surrounded by mobile elements such as insertion sequences and transposases as well as tRNA genes. Despite this, there is no strong direct proof of HGT between these organisms. Here we show that a phylogenetic tree based on magnetosome protein amino acid sequences from a number of MTB was congruent with the tree based on the organisms' 16S rRNA gene sequences. This shows that evolution and divergence of these proteins and the 16S rRNA gene occurred similarly. This suggests that magnetotaxis originated monophyletically in the Proteobacteria phylum and implies that the common ancestor of all Proteobacteria was magnetotactic.

Deciphering unusual uncultured magnetotactic multicellular prokaryotes through genomics

“…M. bavaricum protein sequences, which involve both magnetite and greigite magnetosome production, show that these sequences are more related to each other than to Alphaproteobacteria magnetite-related protein sequences (Figure 2). This result is in agreement with previously studies based on concatenated Mam protein phylogenetic analysis Lefèvre et al, 2013a). Phylogeny based on MamQ shows that both Ca.…”

“…blakemorei and Mc. marinus are clustered, suggesting a more recent divergence between these species, which is not congruent to the phylogenetic analysis (Lefèvre et al, 2013a), the sequence similarity between Mc. marinus and Mv.…”

“…M. multicellularis and phylogenetic analysis indicated that the biomineralization of magnetite and greigite evolved from a common ancestor Lefèvre et al, 2013a). Here, we compared magnetotactic bacterial genomes based on the coverage and similarity value percentages used to analyze biomineralization genes on a previous study (1e À 05 E-value, 22% coverage and 50% similarity; Abreu et al, 2011).…”

“…Phylogenetic analysis based on concatenated amino-acid sequences of conserved mam genes indicate that the Ca. M. multicellularis mam genes are more similar to those of Candidatus Desulfamplus magnetomortis strain BW-1 (Lefèvre et al, 2011(Lefèvre et al, , 2013a, which are believed to be responsible for greigite magnetosome synthesis (Figure 1). When repeated mam genes (mamA, -B, -E, -K, -O and -Q) were analyzed separately (Figure 2), Magnetovibrio blakemorei and Magnetococcus marinus appeared to be most closely related to each other in most cases.…”

Genomic insights into the uncultured genus ‘Candidatus Magnetobacterium’ in the phylum Nitrospirae

“…The formation of bullet-shaped magnetite magnetosomes has been discovered in the deep-branching MTB lineages such as Deltaproteobacteria and Nitrospirae, leading to the hypothesis that the first magnetosomes were bullet-shaped magnetite particles (Lefèvre et al, 2013a). Nakazawa et al (2009) assumed that the absence of magnetosome size and morphology controlling genes (such as mamGFDC and mms6) might lead to the formation of bulletshaped magnetosomes.…”