Unravelling the diversity of magnetotactic bacteria through analysis of open genomic databases

Abstract

Magnetotactic bacteria (MtB) are prokaryotes that possess genes for the synthesis of membranebounded crystals of magnetite or greigite, called magnetosomes. Despite over half a century of studying MTB, only about 60 genomes have been sequenced. Most belong to Proteobacteria, with a minority affiliated with the Nitrospirae, Omnitrophica, Planctomycetes, and Latescibacteria. Due to the scanty information available regarding MTB phylogenetic diversity, little is known about their ecology, evolution and about the magnetosome biomineralization process. This study presents a large-scale search of magnetosome biomineralization genes and reveals 38 new MTB genomes. Several of these genomes were detected in the phyla Elusimicrobia, Candidatus Hydrogenedentes, and Nitrospinae, where magnetotactic representatives have not previously been reported. Analysis of the obtained putative magnetosome biomineralization genes revealed a monophyletic origin capable of putative greigite magnetosome synthesis. The ecological distributions of the reconstructed MTB genomes were also analyzed and several patterns were identified. These data suggest that open databases are an excellent source for obtaining new information of interest.

Identification and Genomic Characterization of Two Previously Unknown Magnetotactic Nitrospirae

“…However, over the past decade, our knowledge of MTB diversity has been significantly expanded through the applications of cultivation-dependent and -independent approaches (Kolinko et al, 2012;Bazylinski et al, 2013;Lefèvre and Bazylinski, 2013;Lin et al, 2017a;Amor et al, 2020b). MTB have thus far been identified in at least 16 phylum-level lineages (Lin et al, 2018(Lin et al, , 2020bUzun et al, 2020), suggesting unexpected taxonomic diversity of magnetosome biogenesis and magnetotaxis across the domain Bacteria.…”

“…Magnetotactic bacteria phylogenetically affiliated within the Nitrospirae phylum are of great interest because of their biomineralization of up to several hundreds of Fe 3 O 4 magnetosomal crystals and formation of dozens of sulfur globules in a single cell, linking these microorganisms to the key steps of iron and sulfur cycling in aquatic ecosystems (Spring et al, 1993;Jogler et al, 2010;Lin et al, 2014b;Li et al, 2020). Historically, Nitrospirae MTB have only been discovered in freshwater environments (Spring et al, 1993;Flies et al, 2005;Amann et al, 2006); however, recent studies have revealed that these MTB are globally distributed in a wider range of environments than anticipated previously, including hot springs (Lefèvre et al, 2010;Uzun et al, 2020), estuary and marine ecosystems (Lin et al, 2017a;Qian et al, 2019), and acidic peatlands (Lin et al, 2020b). Due to the lack of cultivated representatives, much of our understanding of Nitrospirae MTB was obtained through 16S rRNA gene-based methods.…”

“…Recently, since the first report of a nearly complete draft genome of Candidatus (Ca.) Magnetobacterium casensis through a targeted metagenomic approach (Lin et al, 2014b), a growing number of Nitrospirae MTB genomes have been reconstructed from distinct ecosystems through applications of genome-resolved metagenomics (Lin et al, 2017b(Lin et al, , 2018(Lin et al, , 2020bKoziaeva et al, 2020;Uzun et al, 2020) and single-cell genomics (Kolinko et al, 2016). Genomic analyses of Ca.…”

Magnetotactic Bacteria and Magnetosomes: Basic Properties and Applications

“…Genomes of many MTB species were sequenced [20,21,[44][45][46][47][48][49][50][51][52][53][54][55][56][57][58][59][60], and genes specific for magnetotactic bacteria were found, which control the magnetosome formation [61,62]. These genes are located in a so-called magnetosome genomic cluster (MGC) and are responsible for the formation of the magnetosome membrane, transport of iron into magnetosomes, nucleation and growth of magnetite crystals, and the shape and size of the latter [17,[63][64][65][66][67][68][69].…”

“…Morphologically, MTB are diverse including vibrions, rods, cocci, spirilla, and so-called "multicellular" organisms [17]. According to their present phylogenetic position, MTB are classified in the following phyla: Proteobacteria, Nitrospirota, Omnitrophota, Latescibacterota, Planctomycetota, Nitrospinota, Hydrogenedentota, Elusimicrobiota, Fibrobacterota, Riflebacteria, Bdellovibrionota, UBA10199, Desulfobacterota [18][19][20][21] (Figure 2). Only a few MTB strains were isolated into a pure culture.…”