Hidden Talents: Silent Gene Clusters Encoding Magnetic Organelle Biosynthesis in a Non-Magnetotactic Phototrophic Bacterium

Abstract

Magnetosomes are unique organelles synthesized by magnetotactic bacteria (MTB) for magnetic navigation. Their complex biosynthesis is controlled by large magnetosome gene clusters (MGC). Here, we report the discovery and comprehensive analysis of silent but functional MGCs in the non-magnetotactic phototrophic bacterium Rhodovastum atsumiense. Our findings suggest that these MGCs were acquired by horizontal gene transfer and inactivated through transcriptional silencing and antisense RNA regulation. At least several magnetosome genes from G2-11 retained functionality, as their products restore magnetosome biosynthesis in isogenic deletion mutants of the model MTB Magnetospirillum gryphiswaldense. Although G2-11 was found to form magnetosomes upon the laboratory transfer of the MGCs from M. gryphiswaldense, strong negative selection led to rapid loss of this trait upon subcultivation. Our results provide insight into the horizontal dissemination of gene clusters encoding bacterial magnetic organelles outside MTB and illuminate the potential mechanisms of their genomic preservation in a latent state.