Recovery and genome reconstruction of novel magnetotactic Elusimicrobiota from bog soil.

Studying the minor part of the uncultivated microbial majority ("rare biosphere") is difficult even with modern culture-independent techniques. The enormity of microbial diversity creates particular challenges for investigating low-abundance microbial populations in soils. Strategies for selective sample enrichment to reduce community complexity can aid in studying the rare biosphere. Magnetotactic bacteria, apart from being a minor part of the microbial community, are also found in poorly studied bacterial phyla and certainly belong to a rare biosphere. The presence of intracellular magnetic crystals within magnetotactic bacteria allows for their significant enrichment using magnetic separation techniques for studies using a metagenomic approach. This work investigated the microbial diversity of a black bog soil and its magnetically enriched fraction. The poorly studied phylum representatives in the magnetic fraction were enriched compared to the original soil community. Two new magnetotactic species, Candidatus Liberimonas magnetica DUR002 and Candidatus Obscuribacterium magneticum DUR003, belonging to different classes of the relatively little-studied phylum Elusimicrobiota, were proposed. Their genomes contain clusters of magnetosome genes that differ from the previously described ones by the absence of genes encoding magnetochrome-containing proteins and the presence of unique Elusimicrobiota-specific genes, termed mae. The predicted obligately fermentative metabolism in DUR002 and lack of flagellar motility in the magnetotactic Elusimicrobiota broadens our understanding of the lifestyles of magnetotactic bacteria and raises new questions about the evolutionary advantages of magnetotaxis. The findings presented here increase our understanding of magnetotactic bacteria, soil microbial communities, and the rare biosphere.

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

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.

Alkalicaulis satelles gen. nov., sp. nov., a novel haloalkaliphile isolated from a laboratory culture cyanobacterium Geitlerinema species and proposals of Maricaulaceae fam. nov., Robiginitomaculaceae fam. nov., Maricaulales ord. nov. and Hyphomonadales ord. nov.

A prosthecate bacterial strain, designated G-192T, was isolated from decaying biomass of a haloalkaliphilic cyanobacterium Geitlerinema sp. Z-T0701. The cells were aerobic, Gram-negative, non-endospore-forming and dimorphic, occurring either as sessile bacteria with a characteristic stalk or as motile flagellated cells. The strain utilized a limited range of substrates, mostly peptonaceous, but was able to degrade whole proteins. Growth occurred at 5-46 °C (optimum, 35-40 °C), pH 7.3-10.3 (optimum, pH 8.0-9.0), 0-14 % NaCl (v/w; optimum, 2.0-6.0 %, v/w). The G+C content of the genomic DNA of strain G-192T was 66.8%. Phylogenetic analysis of the 16S rRNA gene sequence revealed that strain G-192T formed a distinct evolutionary lineage within the family Hyphomonadaceae. Strain G-192T showed the highest 16S rRNA sequence similarity to Glycocaulis profundi ZYF765T (95.2%), Oceanicaulis stylophorae GISW-4T (94.2%) and Marinicauda salina WD6-1T (95.5%). The major cellular fatty acids (>5% of the total) were C18:1 ω9c, C18:0 and 11-methyl-C18:1 ω7c. The major polar lipids were glycolipids and phospholipids. The only respiratory quinone was ubiquinone-10 (Q-10). Based on polyphasic results including phylogenomic data, the novel strain could be distinguished from other genera, which suggests that strain G-192T represents a novel species of a new genus, for which the name Alkalicaulis satelles gen. nov., sp. nov. is proposed. The type strain is G-192T (=VKM B-3306T=KCTC 72746T). The strain is the first representative of the stalked bacteria associated with a haloalkaliphilic cyanobacterium. Based on phylogenomic indices and phenotypic data, it is proposed to evolve two novel families Maricaulaceae fam. nov. and Robiginitomaculaceae fam. nov. out of the current family Hyphomonadaceae. In addition, it is proposed to place the first two families in the novel order Maricaulales ord. nov. and novel order Hyphomonadales ord. nov. is proposed to accommodate the family Hyphomonadaceae.

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

Magnetotactic bacteria (MTB) are prokaryotes that possess genes for the synthesis of membrane-bounded 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.

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

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.

Magnetospirillum kuznetsovii sp. nov., a novel magnetotactic bacterium isolated from a lake in the Moscow region.

Strain LBB-42T was isolated from sediment sampled at Lake Beloe Bordukovskoe, located in the Moscow region (Russia). Phylogenetic analyses based on 16S rRNA gene sequencing results assigned the strain to the genus Magnetospirillum. Major fatty acids were C16 : 1ω7c, C16 : 0 and C18 : 1 ω9/C18 : 1 ω7. Genome sequencing revealed a genome size of 4.40 Mbp and a G+C content of 63.4 mol%. The average nucleotide identity and digital DNA-DNA hybridization values suggested that strain LBB-42T represents a new species, for which we propose the name Magnetospirillum kuznetsovii sp. nov., with the type strain LBB-42T (=VKM B-3270T=KCTC 15749T).