Detection of interphylum transfers of the magnetosome gene cluster in magnetotactic bacteria

Abstract

Magnetosome synthesis in magnetotactic bacteria (MTB) is regarded as a very ancient evolutionary process that dates back to deep-branching phyla. Magnetotactic bacteria belonging to one of such phyla, <i>Nitrospirota</i>, contain the classical genes for the magnetosome synthesis (e.g., <i>mam</i>, <i>mms</i>) and <i>man</i> genes, which were considered to be specific for this group. However, the recent discovery of <i>man</i> genes in MTB from the <i>Thermodesulfobacteriota</i> phylum has raised several questions about the inheritance of these genes in MTB. In this work, three new <i>man</i> genes containing MTB genomes affiliated with <i>Nitrospirota</i> and <i>Thermodesulfobacteriota,</i> were obtained. By applying reconciliation with these and the previously published MTB genomes, we demonstrate that the last common ancestor of all <i>Nitrospirota</i> was most likely not magnetotactic as assumed previously. Instead, our findings suggest that the genes for magnetosome synthesis were transmitted to the phylum <i>Nitrospirota</i> by horizontal gene transfer (HGT), which is the first case of the interphylum transfer of magnetosome genes detected to date. Furthermore, we provide evidence for the HGT of magnetosome genes from the <i>Magnetobacteriaceae</i> to the <i>Dissulfurispiraceae</i> family within <i>Nitrospirota.</i> Thus, our results imply a more significant role of HGT in the MTB evolution than deemed before and challenge the hypothesis of the ancient origin of magnetosome synthesis.