Genome-Based Metabolic Reconstruction of a Novel Uncultivated Freshwater Magnetotactic coccus “Ca. Magnetaquicoccus inordinatus” UR-1, and Proposal of a Candidate Family “Ca. Magnetaquicoccaceae”

Abstract

Magnetotactic bacteria are widely represented microorganisms that have the ability to synthesize magnetosomes. The magnetotactic cocci of the order Magnetococcales are the most frequently identified, but their classification remains unclear due to the low number of cultivated representatives. This paper reports the analysis of an uncultivated magnetotactic coccus UR-1 collected from the Uda River (in eastern Siberia). Genome analyses of this bacterium and comparison to the available Magnetococcales genomes identified a novel species called “Ca. Magnetaquicoccus inordinatus,” and a delineated candidate family “Ca. Magnetaquicoccaceae” within the order Magnetococcales is proposed. We used average amino acid identity values <55–56% and <64–65% as thresholds for the separation of families and genera, respectively, within the order Magnetococcales. Analyses of the genome sequence of UR-1 revealed a potential ability for a chemolithoautotrophic lifestyle, with the oxidation of a reduced sulfur compound and carbon assimilation by rTCA. A nearly complete magnetosome genome island, containing a set of mam and mms genes, was also identified. Further comparative analyses of the magnetosome genes showed vertical inheritance as well as horizontal gene transfer as the evolutionary drivers of magnetosome biomineralization genes in strains of the order Magnetococcales.

Bullet‐Shaped Magnetite Biomineralization Within a Magnetotactic Deltaproteobacterium: Implications for Magnetofossil Identification

“…In the past decade, significant progress has been made in identifying MTB from natural environments using culture‐independent analysis methods at the single‐cell level (Kolinko et al, 2012; Li et al, 2017). For instance, by coupling fluorescence in situ hybridization (FISH) analysis with transmission or scanning electron microscope (TEM or SEM) observation, a so‐called coupled FISH‐SEM or FISH‐TEM approach, MTB cells from natural environments can be identified phylogenetically and structurally at the single‐cell level (Koziaeva et al, 2019; Li et al, 2017, 2019; Qian et al, 2019, 2020; Zhang et al, 2017). On the other hand, rapid development of metagenomics and single‐cell genomics has enabled identification of more magnetosome gene clusters (MGCs) responsible for magnetosome biomineralization in uncultured MTB (Jogler et al, 2011; Kolinko et al, 2014, 2016; Lin et al, 2018).…”

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

“…The compared trees also indicated vertical inheritance in the Alpha-and Ca. Etaproteobacteria groups, although the occurrence of horizontal transfer events was previously established in these groups 27,31 . These types of transfers have been confirmed to have occurred recently, which is why they cannot be detected through the tree topology analysis.…”

“…Etaproteobacteria class. Genomes from this class previously were found in both saline and freshwater habitats 15,31,53 . The obtained MAG clustered with genomes isolated from freshwater environments.…”

Expanding magnetic organelle biogenesis in the domainBacteria

“…In recent years, the known extent of MTB diversity has undergone a significant expansion due to methodological advances, such as the successful cultivation of novel MTB strains e.g., 29–32 , 16S rRNA gene-based characterization e.g., 33–35 , genome mining of public repositories including GenBank and IMG/ER 17,36 , and cultivation-independent surveys of magnetosome gene clusters (MGCs, which are physically clustered groups of genes that are together responsible for magnetosomal biogenesis) 37,38 . MTB have now been further identified in other Bacterial taxa, including the Betaproteobacteria , Zetaproteobacteria , “ Candidatus Etaproteobacteria”, and “ Candidatus Lambdaproteobacteria” classes of the Proteobacteria phylum, the candidate phylum Omnitrophica (previously known as the candidate division OP3), the candidate phylum Latescibacteria (previously known as the candidate division WS3), and the phylum Planctomycetes , according to the NCBI taxonomy.…”