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

Abstract

Magnetosomes are prokaryotic organelles produced by magnetotactic bacteria that consist of nanometer-sized magnetite (Fe(3)O(4)) or/and greigite (Fe(3)S(4)) magnetic crystals enveloped by a lipid bilayer membrane. In magnetite-producing magnetotactic bacteria, proteins present in the magnetosome membrane modulate biomineralization of the magnetite crystal. In these microorganisms, genes that encode for magnetosome membrane proteins as well as genes involved in the construction of the magnetite magnetosome chain, the mam and mms genes, are organized within a genomic island. However, partially because there are presently no greigite-producing magnetotactic bacteria in pure culture, little is known regarding the greigite biomineralization process in these organisms including whether similar genes are involved in the process. Here using culture-independent techniques, we now show that mam genes involved in the production of magnetite magnetosomes are also present in greigite-producing magnetotactic bacteria. This finding suggest that the biomineralization of magnetite and greigite did not have evolve independently (that is, magnetotaxis is polyphyletic) as once suggested. Instead, results presented here are consistent with a model in which the ability to biomineralize magnetosomes and the possession of the mam genes was acquired by bacteria from a common ancestor, that is, the magnetotactic trait is monophyletic.

Figure 1

Organization of open reading frames in two segments of DNA (contigs) from Candidatus Magnetoglobus multicellularis containing putative magnetosome-related genes compared to the organization of magnetosome genes within the magnetosome gene island of several cultivated magnetotactic bacteria. Scale bar indicates 1000 bp. Hypothetical proteins are represented as unlabeled arrows.

Figure 2

Phylogenetic analyses of Candidatus Magnetoglobus multicellularis: (a) maximum likelihood tree based on 16S rRNA gene sequences using the GTR+Γ DNA substitution model. Numbers at nodes represent bootstrap values for 1000 replicates. Numbers in parentheses are GenBank accession numbers. (b) Amino acid composition of conserved mam genes using the WAG+I+Γ+F matrix. Sequences of the uncultured MTB C. Thermomagnetovibrio paiutensis HSMV-1 (Lefèvre et al., 2010a) and Ca. Magnetobacterium bavaricum (Spring et al., 1993), both phylogenetically affiliated with the Nitrospirae phylum, are included as outgroups in this analysis. Numbers between branches are aLRT values.