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Recovery and genome reconstruction of novel magnetotactic Elusimicrobiota from bog soil

Abstract

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.

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Fig. 1: The composition of the microbial community of the analyzed black bog soil.
Fig. 2: TEM images of enriched magnetic cells.
Fig. 3: Maximum-likelihood phylogenomic tree of all known Elusimicrobiota, all MTB genomes previously known or obtained in this work.
Fig. 4: Magnetosome gene clusters of the investigated Elusimicrobiota genomes.

Data availability

Raw reads of metagenomic 16S rRNA gene sequencing of soil, filtrate and magnetic fraction were deposited in the NCBI Sequence Read Archive under the accession numbers SRR19138506, SRR19138505 and SRR19078916. DUR002 and DUR003 genome sequences have been deposited in GenBank under the accession numbers JAJAPY000000000 and JAJAPZ000000000 (BioProject number PRJNA769424). The raw metagenomic read data have been deposited in the NCBI Sequence Read Archive under the accession numbers SRR16235686 and SRR16235685. All data generated and analyzed in this study are also available in figshare [66] and in the supplementary information accompanying this paper.

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Acknowledgements

We thank Prof. Aharon Oren for his expert guidance in nomenclature. We also thank Prof. Jillian Banfield and Banfield Lab for the providing additional information about 1499 genome. Bioinformatic analyses were performed using computing resources at the Core Research Facility ‘Bioengineering’ (Research Center of Biotechnology RAS) and SciBear OU (https://sci-bear.com/). TEM studies were carried out at Electron microscopy laboratory of Moscow State University Biology Faculty. The reported study was partially funded by RFBR (project number 20-34-90116) and by the Ministry of Science and Higher Education of the Russian Federation.

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MU, VK, and DG conceived and designed experiments. MU and LA collected samples. LA carried out magnetic enrichment. MU and MK performed bioinformatics data processing. MU, VK, MD and DG carried out the phylogenetic and comparative genomic analyses. MU performed TEM analysis. RB and MS carried out real-time PCR. MU, MD, VK, LA and DG analyzed the data and drafted the original manuscript. All authors read and approved the final manuscript.

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Correspondence to Denis Grouzdev.

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Uzun, M., Koziaeva, V., Dziuba, M. et al. Recovery and genome reconstruction of novel magnetotactic Elusimicrobiota from bog soil. ISME J 17, 204–214 (2023). https://doi.org/10.1038/s41396-022-01339-z

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