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

Abstract

Horizontal gene transfer is a powerful source of innovations in prokaryotes that can affect almost any cellular system, including microbial organelles. However, typically rapid loss of non-functional gene acquisitions obscures the mechanisms determining the fate of horizontally transferable genes. Here, we report the first discovery of a horizontally inherited gene cluster encoding biosynthesis of magnetosomes, the organelles used by magnetotactic bacteria for navigation, in a non-magnetotactic phototrophic bacterium Rhodovastum atsumiense. We show that these clusters were inactivated through transcriptional silencing and antisense RNA regulation, but retain functionality, as several genes were able to complement the orthologous deletions in a remotely related magnetotactic bacterium. The laboratory transfer of foreign magnetosome genes to R. atsumiense was found to endow the strain with magnetosome biosynthesis, but strong negative selection led to rapid loss of this trait upon subcultivation. Our results provide insight into the horizontal dissemination of gene clusters encoding complex prokaryotic organelles and illuminate the potential mechanisms of their genomic preservation in a dormant state.