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.
This is a preview of subscription content, access via your institution
Subscribe to Journal
Get full journal access for 1 year
only $9.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
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  and in the supplementary information accompanying this paper.
Steen AD, Carini ACP, Lloyd KG, Thrash JC, Deangelis KM, Fierer N. High proportions of bacteria and archaea across most biomes remain uncultured. ISME J. 2019;13:3126–30.
Lloyd KG, Steen AD, Ladau J, Yin J. Phylogenetically novel uncultured microbial cells dominate earth microbiomes. mSystems. 2018;3:e00055–18.
Marcy Y, Ouverney C, Bik EM, Lo T, Ivanova N, Garcia H, et al. Dissecting biological “dark matter” with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth. Proc Natl Acad Sci USA. 2007;104:11889–94.
Pascoal F, Costa R, Magalhães C. The microbial rare biosphere: current concepts, methods and ecological principles. FEMS Microbiol Ecol. 2021;97:fiaa227.
Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, et al. Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA. 2006;103:12115–20.
Gareev KG, Grouzdev DS, Kharitonskii PV, Kosterov A, Koziaeva VV, Sergienko ES, et al. Magnetotactic bacteria and magnetosomes: basic properties and applications. Magnetochemistry. 2021;7:86.
Lefevre CT, Bazylinski DA. Ecology, diversity, and evolution of magnetotactic bacteria. Microbiol Mol Biol Rev. 2013;77:497–526.
Lin W, Pan Y, Bazylinsky DA. Diversity and ecology of and biomineralization by magnetotactic bacteria. Environ Microbiol Rep. 2017;9:345–56.
Uebe R, Schüler D. Magnetosome biogenesis in magnetotactic bacteria. Nat Rev Microbiol. 2016;14:621–37.
Lefèvre CT, Frankel RB, Bazylinski DA. Magnetotaxis in prokaryotes. eLS. 2011. https://onlinelibrary.wiley.com/action/showCitFormats?doi=10.1002%2F9780470015902.a0000397.pub2https://onlinelibrary.wiley.com/action/showCitFormats?doi=10.1002%2F9780470015902.a0000397.pub2.
Goswami P, He K, Li J, Pan Y, Roberts AP, Lin W. Magnetotactic bacteria and magnetofossils: ecology, evolution and environmental implications. npj Biofilms Microbiomes. 2022;8:43.
Flies CB, Jonkers HM, De Beer D, Bosselmann K, Böttcher ME, Schüler D. Diversity and vertical distribution of magnetotactic bacteria along chemical gradients in freshwater microcosms. FEMS Microbiol Ecol. 2005;52:185–95.
Wolfe RS, Thauer RK, Pfennig N. A’capillary racetrack’ method for isolation of magnetotactic bacteria. FEMS Microbiol Ecol. 1987;45:31–5.
Jogler C, Lin W, Meyerdierks A, Kube M, Katzmann E, Flies C, et al. Toward cloning of the magnetotactic metagenome: identification of magnetosome island gene clusters in uncultivated magnetotactic bacteria from different aquatic sediments. Appl Environ Microbiol. 2009;75:3972–9.
Lin W, Zhang W, Paterson GA, Zhu Q, Zhao X. Expanding magnetic organelle biogenesis in the domain Bacteria. Microbiome. 2020;8:152.
Geissinger O, Herlemann DPR, Mo E, Maier UG, Brune A. The ultramicrobacterium “Elusimicrobium minutum” gen. nov., sp. nov., the first cultivated representative of the Termite Group 1 phylum. Appl Environ Microbiol. 2009;75:2831–40.
Wakako I-O, Brune A. Cospeciation of termite gut flagellates and their bacterial endosymbionts: Trichonympha species and ‘Candidatus Endomicrobium trichonymphae’. Mol Ecol. 2009;18:332–42.
Zheng H, Dietrich C, Radek R, Brune A. Endomicrobium proavitum, the first isolate of Endomicrobia class. nov. (phylum Elusimicrobia) – an ultramicrobacterium with an unusual cell cycle that fixes nitrogen with a Group IV nitrogenase. Environ Ecol Stat. 2016;18:191–204.
Méheust R, Castelle CJ, Carnevali PBM, Chen L, Amano Y, Hug LA, et al. Groundwater Elusimicrobia are metabolically diverse compared to gut microbiome Elusimicrobia and some have a novel nitrogenase paralog. ISME J. 2020;14:2907–22.
Lin H, Ascher DB, Myung Y, Lamborg CH, Hallam SJ, Gionfriddo CM, et al. Mercury methylation by metabolically versatile and cosmopolitan marine bacteria. ISME J. 2021;15:1810–25.
Parks DH, Rinke C, Chuvochina M, Chaumeil PA, Woodcroft BJ, Evans PN, et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat Microbiol. 2017;2:1533–42.
Zhang L, Gong X, Wang L, Guo K, Cao S, Zhou Y. Science of the total environment metagenomic insights into the effect of thermal hydrolysis pre-treatment on microbial community of an anaerobic digestion system. Sci Total Environ. 2021;791:148096.
Woodcroft BJ, Singleton CM, Boyd JA, Evans PN, Emerson JB, Zayed AAF, et al. Genome-centric view of carbon processing in thawing permafrost. Nature. 2018;560:49–54.
Uzun M, Alekseeva L, Krutkina M, Koziaeva V, Grouzdev D. Unravelling the diversity of magnetotactic bacteria through analysis of open genomic databases. Sci Data. 2020;7:252.
Tully BJ, Wheat CG, Glazer BT, Huber JA. A dynamic microbial community with high functional redundancy inhabits the cold, oxic subseafloor aquifer. ISME J. 2018;12:1–16.
Kirillova NP, Sileva TM, Ul’yanova TY, Rozov SY, Il’yashenko MA, Makarov MI. Digital soil map of Chashnikovo training and experimental soil ecological center, Moscow State University. Mosc Univ Soil Sci Bull. 2015;70:58–65.
Koziaeva VV, Alekseeva LM, Uzun MM, Leão P, Sukhacheva MV, Patutina EO, et al. Biodiversity of magnetotactic bacteria in the freshwater lake Beloe Bordukovskoe, Russia. Microbiology. 2020;89:348–58.
Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1.
Edgar RC, Flyvbjerg H. Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics. 2015;31:3476–82.
Edgar RC. UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. bioRxiv 2016. https://doi.org/10.1101/081257.
Pruesse E, Peplies J, Glöckner FO. SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics. 2012;28:1823–9.
Fierer N, Jackson JA, Vilgalys R, Jackson RB. Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol. 2005;71:4117–20.
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.
Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. MetaSPAdes: a new versatile metagenomic assembler. Genome Res. 2017;27:824–34.
Wu YW, Simmons BA, Singer SW. MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics. 2016;32:605–7.
Kang DD, Li F, Kirton E, Thomas A, Egan R, An H, et al. MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ. 2019;7:e7359.
Lin HH, Liao YC. Accurate binning of metagenomic contigs via automated clustering sequences using information of genomic signatures and marker genes. Sci Rep. 2016;6:12–9.
Sieber CMK, Probst AJ, Sharrar A, Thomas BC, Hess M, Tringe SG, et al. Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy. Nat Microbiol. 2018;3:836–43.
Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29:1072–5.
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.
Chaumeil P, Mussig AJ, Parks DH, Hugenholtz P. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics. 2019;36:1925–7.
Tatusova T, Dicuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. 2016;44:6614–24.
Ji R, Zhang W, Pan Y, Lin W. MagCluster: a tool for identification, annotation, and visualization of magnetosome gene clusters. Microbiol Resour Announc. 2022;11:e01031–21.
Wu S, Zhu Z, Fu L, Niu B, Li W. WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genomics. 2011;12:444.
Kanehisa M, Sato Y. KEGG Mapper for inferring cellular functions from protein sequences. Protein Sci. 2020;29:28–35.
Shaffer M, Borton MA, McGivern BB, Zayed AA, La Rosa SL. 0003 3527 8101, Solden LM, et al. DRAM for distilling microbial metabolism to automate the curation of microbiome function. Nucleic Acids Res. 2020;48:8883–900.
Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun. 2018;9:5114.
Nguyen LT, Schmidt HA, Von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32:268–74.
Kalyaanamoorthy S, Minh BQ, Wong TKF, Haeseler AVon, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14:587–9.
Hoang DT, Chernomor O, Von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol. 2018;35:518–22.
Letunic I, Bork P. Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49:W293–6.
Coleman GA, Davín AA, Mahendrarajah TA, Szánthó LL, Spang A, Hugenholtz P, et al. A rooted phylogeny resolves early bacterial evolution. Science. 2021;372:eabe0511.
Parks DH. https://github.com/dparks1134/CompareM.
Dombrowski N, Lee JH, Williams TA, Offre P, Spang A. Genomic diversity, lifestyles and evolutionary origins of DPANN archaea. FEMS Microbiol Lett. 2019;366:fnz008.
Lin W, Zhang W, Zhao X, Roberts AP, Paterson GA, Bazylinski DA, et al. Genomic expansion of magnetotactic bacteria reveals an early common origin of magnetotaxis with lineage-specific evolution. ISME J. 2018;12:1508–19.
Urakawa H, Garcia JC, Nielsen JL, Le VQ, Kozlowski JA, Stein LY, et al. Nitrosospira lacus sp. nov., a psychrotolerant, ammonia-oxidizing bacterium from sandy lake sediment. Int J Syst Evol Microbiol. 2015;65:242–50.
Kalyuzhnaya MG, De Marco P, Bowerman S, Pacheco CC, Lara JC, Lidstrom ME, et al. Methyloversatilis universalis gen. nov., sp. nov., a novel taxon within the Betaproteobacteria represented by three methylotrophic isolates. Int J Syst Evol Microbiol. 2006;56:2517–22.
Bazylinski DA, Frankel RB, Konhauser KO. Modes of biomineralization of magnetite by microbes. Geomicrobiol J. 2007;24:465–75.
Uzun M, Koziaeva V, Dziuba M, Leão P, Krutkina M, Grouzdev D. Detection of interphylum transfers of the magnetosome gene cluster in magnetotactic bacteria. Front Microbiol. 2022;13:945734.
Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil PA, et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol. 2018;36:996.
Murphy CL, Biggerstaff J, Eichhorn A, Ewing E, Shahan R, Soriano D, et al. Genomic characterization of three novel Desulfobacterota classes expand the metabolic and phylogenetic diversity of the phylum. Environ Microbiol. 2021;23:4326–43.
Konstantinidis KT, Rosselló-Móra R, Amann R. Uncultivated microbes in need of their own taxonomy. ISME J. 2017;11:2399–406.
Denise R, Abby SS, Rocha EPC. Diversification of the type IV filament superfamily into machines for adhesion, protein secretion, DNA uptake, and motility. PLoS Biol. 2019;17:e3000390.
Hennell James R, Deme JC, Kjӕr A, Alcock F, Silale A, Lauber F, et al. Structure and mechanism of the proton-driven motor that powers type 9 secretion and gliding motility. Nat Microbiol. 2021;6:221–33.
Nolan LM, Whitchurch CB, Barquist L, Katrib M, Boinett CJ, Mayho M, et al. A global genomic approach uncovers novel components for twitching motility-mediated biofilm expansion in Pseudomonas aeruginosa. Micro Genomics. 2018;4:e000229.
Uzun M, Koziaeva V, Dziuba M, Alekseeva L, Grouzdev D. Mam protein trees. 2022. https://doi.org/10.6084/m9.figshare.c.6045158.v1.
Arnoux P, Siponen MI, Lefèvre CT, Ginet N, Pignol D. Structure and evolution of the magnetochrome domains: no longer alone. Front Microbiol. 2014;5:117.
Katzmann E, Scheffel A, Gruska M, Plitzko JM, Schüler D. Loss of the actin-like protein MamK has pleiotropic effects on magnetosome formation and chain assembly in Magnetospirillum gryphiswaldense. Mol Microbiol. 2010;77:208–24.
Wagner-Döbler I, Bennasar A, Vancanneyt M, Strömpl C, Brümmer I, Eichner C, et al. Microcosm enrichment of biphenyl-degrading microbial communities from soils and sediments. Appl Environ Microbiol. 1998;64:3014–22.
Ibekwe AM, Papiernik SK, Gan J, Yates SR, Crowley DE, Yang CH. Microcosm enrichment of 1,3-dichloropropene-degrading soil microbial communities in a compost-amended soil. J Appl Microbiol. 2001;91:668–76.
Yakimov MM, Denaro R, Genovese M, Cappello S, D’Auria G, Chernikova TN, et al. Natural microbial diversity in superficial sediments of Milazzo Harbor (Sicily) and community successions during microcosm enrichment with various hydrocarbons. Environ Microbiol. 2005;7:1426–41.
Tringe SG, Von Mering C, Kobayashi A, Salamov AA, Chen K, Chang HW, et al. Comparative metagenomics of microbial communities. Science. 2005;308:554–7.
Lefèvre CT, Trubitsyn D, Abreu F, Kolinko S, Jogler C, de Almeida LGP, et al. Comparative genomic analysis of magnetotactic bacteria from the Deltaproteobacteria provides new insights into magnetite and greigite magnetosome genes required for magnetotaxis. Environ Microbiol. 2013;15:2712–35.
Wadhwa N, Berg HC. Bacterial motility: machinery and mechanisms. Nat Rev Microbiol. 2022;20:161–73.
Zhu K, Pan H, Li J, Yu-Zhang K, Zhang SD, Zhang WY, et al. Isolation and characterization of a marine magnetotactic spirillum axenic culture QH-2 from an intertidal zone of the China Sea. Res Microbiol. 2010;161:276–83.
Kaimer C, Zusman DR. Regulation of cell reversal frequency in Myxococcus xanthus requires the balanced activity of CheY-like domains in FrzE and FrzZ. Mol Microbiol. 2016;100:379–95.
Kühn MJ, Talà L, Inclan YF, Patino R, Pierrat X, Vos I, et al. Mechanotaxis directs Pseudomonas aeruginosa twitching motility. Proc Natl Acad Sci USA. 2021;118:e2101759118.
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.
The authors declare no competing interests.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
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