Abstract
BackgroundThe discovery of membrane-enclosed, metabolically functional organelles in Bacteria has transformed our understanding of the subcellular complexity of prokaryotic cells. Biomineralization of magnetic nanoparticles within magnetosomes by magnetotactic bacteria (MTB) is a fascinating example of prokaryotic organelles. Magnetosomes, as nano-sized magnetic sensors in MTB, facilitate cell navigation along the local geomagnetic field, a behaviour referred to as magnetotaxis or microbial magnetoreception. Recent discovery of novel MTB outside the traditionally recognized taxonomic lineages suggests that MTB diversity across the domain Bacteria are considerably underestimated, which limits understanding of the taxonomic distribution and evolutionary origin of magnetosome organelle biogenesis.ResultsHere, we perform the most comprehensive metagenomic analysis available of MTB communities and reconstruct metagenome-assembled MTB genomes from diverse ecosystems. Discovery of MTB in acidic peatland soils suggests widespread MTB occurrence in waterlogged soils in addition to subaqueous sediments and water bodies. A total of 168 MTB draft genomes have been reconstructed, which represent nearly a 3-fold increase over the number currently available and more than double the known MTB species at the genome level. Phylogenomic analysis reveals that these genomes belong to 13 Bacterial phyla, six of which were previously not known to include MTB. These findings indicate a much wider taxonomic distribution of magnetosome organelle biogenesis across the domain Bacteria than previously thought. Comparative genome analysis reveals a vast diversity of magnetosome gene clusters involved in magnetosomal biogenesis in terms of gene content and synteny residing in distinct taxonomic lineages. Phylogenetic analyses of core magnetosome proteins in this largest available and taxonomically diverse dataset support an unexpectedly early evolutionary origin of magnetosome biomineralization, likely ancestral to the origin of the domain Bacteria.ConclusionsThese findings expand the taxonomic and phylogenetic diversity of MTB across the domain Bacteria and shed new light on the origin and evolution of microbial magnetoreception. Potential biogenesis of the magnetosome organelle in the close descendants of the last bacterial common ancestor has important implications for our understanding of the evolutionary history of bacterial cellular complexity and emphasizes the biological significance of the magnetosome organelle.AvdtuUL8bNKQaZ224H3AxpVideo
Highlights
The discovery of membrane-enclosed, metabolically functional organelles in Bacteria has transformed our understanding of the subcellular complexity of prokaryotic cells
This long-held view was revised after numerous recent discoveries of a diverse group of highly organized, membrane-enclosed organelles in the domains Bacteria and Archaea associated with specific cellular functions [1,2,3]
magnetotactic bacteria (MTB) have been found broadly in diverse aquatic ecosystems, including some extreme environments such as hot springs [49, 50], saline-alkaline lakes [51], acidic lagoons and mine drainage systems [37, 52], and deep-sea sediments [53], but reports of MTB in soils are limited to a few studies that were published almost 30 years ago [22, 23]
Summary
The discovery of membrane-enclosed, metabolically functional organelles in Bacteria has transformed our understanding of the subcellular complexity of prokaryotic cells. It was accepted widely that intracellular, membranebounded, metabolically functional organelles are present exclusively in eukaryotic cells and that they are absent from Bacteria and Archaea. This long-held view was revised after numerous recent discoveries of a diverse group of highly organized, membrane-enclosed organelles in the domains Bacteria and Archaea associated with specific cellular functions [1,2,3]. The taxonomic distribution, origin and evolution of prokaryotic organelles remain largely elusive It is still unclear whether organelle biogenesis emerged early or late during the evolution of Bacteria and Archaea, posing problems for elucidating the evolutionary history of cellular complexity. Considering that magnetoreception occurs widely in both micro- and macro-
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
