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, Nitrospirota, contain the classical genes for the magnetosome synthesis (e.g., mam, mms) and man genes, which were considered to be specific for this group. However, the recent discovery of man genes in MTB from the Thermodesulfobacteriota phylum has raised several questions about the inheritance of these genes in MTB. In this work, three new man genes containing MTB genomes affiliated with Nitrospirota and Thermodesulfobacteriota, were obtained. By applying reconciliation with these and the previously published MTB genomes, we demonstrate that the last common ancestor of all Nitrospirota was most likely not magnetotactic as assumed previously. Instead, our findings suggest that the genes for magnetosome synthesis were transmitted to the phylum Nitrospirota 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 Magnetobacteriaceae to the Dissulfurispiraceae family within Nitrospirota. 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.

Silent gene clusters encode magnetic organelle biosynthesis in a non-magnetotactic phototrophic bacterium

“…Additionally, this would imply numerous losses of magnetotaxis genes during phylogenetic divergence, which is not a parsimonious explanation, and give only marginal importance to the role that horizontal gene transfer (HGT) could play in the MGCs evolution [ 13 , 14 ]. At the same time, multiple violations of the phylogenetic tree congruency were observed, indicating instances of HGT [ 9 , 15 – 19 ]. Moreover, the potential ability for MGCs mobilization and transfer is supported by the fact that in many of the described MTB, MGCs are found in genomic regions of plasticity, so-called genomic ma gnetosome i slands (MAI), which is supported by the deviating G + C content, codon adaptation index (CAI), tetranucleotide frequency and abundance of mobile elements [ 20 , 21 ].…”

Recent advances in studies on magnetosome‐associated proteins composing the bacterial geomagnetic sensor organelle

“…Importantly, nine genes, mamA, mamB, mamE, mamI, mamK, mamM, mamO, mamP, and mamQ (the core set of magnetosome genes), are conserved in MTB genomes regardless of magnetite/greigite producers belonging to different phyla. 62 Note that this core set of genes was also mostly conserved in MAI sequences obtained via metagenomic approaches derived from the uncultured diverse MTB, 55,61 indicating that the magnetosome-associated proteins encoded in these magnetosome genes have fundamental roles in forming or maintaining magnetosomes. By contrast, group-specific gene sets, mad and man, are identified from a portion of MTB.…”

“…Hence, to the best of the authors' knowledge, the known MTB are affiliated with the phylum Proteobacteria, including Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria, Zetaproteobacteria, Candidatus Etaproteobacteria, Candidatus Lambdaproteobacteria, and Oligoflexia (synonym Bdellovibrionota) classes; Nitrospirae (synonym Nitrospirota); Planctomycetota; Thermodesulfobacteriota (reclassified from Deltaproteobacteria), Candidatus Omnitrophica (candidate division OP3); Candidatus Latescibacteria (candidate division Nitrospinae (synonym Nitrospinota); Hydrogenedentota; Elusimicrobia (synonym Elusimicrobiota); Fibrobacteres (synonym Fibrobacterota); Candidatus Riflebacteria; and UBA10199 phyla. 55,60,61 Recent metagenomic analyses of environmental specimens indicated further expanded MTB diversity in the phyla of the domain bacteria. 61 Even with expanding insight into the phylogenetic diversity of MTB by identifications of new MTB species, MAIs were found in all known MTB genomes.…”

“…55,60,61 Recent metagenomic analyses of environmental specimens indicated further expanded MTB diversity in the phyla of the domain bacteria. 61 Even with expanding insight into the phylogenetic diversity of MTB by identifications of new MTB species, MAIs were found in all known MTB genomes. Figure 2a-d show examples of gene clusters in MAI from phylogenetically distanced MTB.…”

“…61,62 Moreover, the magnetosome genes in Nitrospirae (man) were found in MTB belonging to Nitrospirota and Thermodesulfobacteriota phyla. 61,63 These group-specific proteins seem to contribute to phylum-specific magnetite/greigite mineralization process, magnetosome formation, or magnetotactic motility. However, due to these group-specific genes being identified recently, the functions of the encoded proteins have not yet been reported.…”