Identification and Genomic Characterization of Two Previously Unknown Magnetotactic Nitrospirae
Magnetotactic bacteria (MTB) are a group of microbes that biomineralize membrane-bound, nanosized magnetite (Fe3O4), and/or greigite (Fe3S4) crystals in intracellular magnetic organelle magnetosomes. MTB belonging to the Nitrospirae phylum can form up to several hundreds of Fe3O4 magnetosome crystal...
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| Format: | Article |
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Frontiers Media S.A.
2021-07-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.690052/full |
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| author | Wensi Zhang Wensi Zhang Wensi Zhang Yinzhao Wang Li Liu Li Liu Li Liu Yongxin Pan Yongxin Pan Yongxin Pan Wei Lin Wei Lin |
| author_facet | Wensi Zhang Wensi Zhang Wensi Zhang Yinzhao Wang Li Liu Li Liu Li Liu Yongxin Pan Yongxin Pan Yongxin Pan Wei Lin Wei Lin |
| author_sort | Wensi Zhang |
| collection | DOAJ |
| description | Magnetotactic bacteria (MTB) are a group of microbes that biomineralize membrane-bound, nanosized magnetite (Fe3O4), and/or greigite (Fe3S4) crystals in intracellular magnetic organelle magnetosomes. MTB belonging to the Nitrospirae phylum can form up to several hundreds of Fe3O4 magnetosome crystals and dozens of sulfur globules in a single cell. These MTB are widespread in aquatic environments and sometimes account for a significant proportion of microbial biomass near the oxycline, linking these lineages to the key steps of global iron and sulfur cycling. Despite their ecological and biogeochemical importance, our understanding of the diversity and ecophysiology of magnetotactic Nitrospirae is still very limited because this group of MTB remains unculturable. Here, we identify and characterize two previously unknown MTB populations within the Nitrospirae phylum through a combination of 16S rRNA gene-based and genome-resolved metagenomic analyses. These two MTB populations represent distinct morphotypes (rod-shaped and coccoid, designated as XYR, and XYC, respectively), and both form more than 100 bullet-shaped magnetosomal crystals per cell. High-quality draft genomes of XYR and XYC have been reconstructed, and they represent a novel species and a novel genus, respectively, according to their average amino-acid identity values with respect to available genomes. Accordingly, the names Candidatus Magnetobacterium cryptolimnobacter and Candidatus Magnetomicrobium cryptolimnococcus for XYR and XYC, respectively, were proposed. Further comparative genomic analyses of XYR, XYC, and previously reported magnetotactic Nitrospirae reveal the general metabolic potential of this MTB group in distinct microenvironments, including CO2 fixation, dissimilatory sulfate reduction, sulfide oxidation, nitrogen fixation, or denitrification processes. A remarkably conserved magnetosome gene cluster has been identified across Nitrospirae MTB genomes, indicating its putative important adaptive roles in these bacteria. Taken together, the present study provides novel insights into the phylogenomic diversity and ecophysiology of this intriguing, yet poorly understood MTB group. |
| first_indexed | 2024-12-16T16:05:44Z |
| format | Article |
| id | doaj.art-c032023d055d41208052c60b05ae5138 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-16T16:05:44Z |
| publishDate | 2021-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-c032023d055d41208052c60b05ae51382022-12-21T22:25:21ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-07-011210.3389/fmicb.2021.690052690052Identification and Genomic Characterization of Two Previously Unknown Magnetotactic NitrospiraeWensi Zhang0Wensi Zhang1Wensi Zhang2Yinzhao Wang3Li Liu4Li Liu5Li Liu6Yongxin Pan7Yongxin Pan8Yongxin Pan9Wei Lin10Wei Lin11Key Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing, ChinaFrance-China Joint Laboratory for Evolution and Development of Magnetotactic Multicellular Organisms, Chinese Academy of Sciences, Beijing, ChinaCollege of Earth and Planetary Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, ChinaKey Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing, ChinaFrance-China Joint Laboratory for Evolution and Development of Magnetotactic Multicellular Organisms, Chinese Academy of Sciences, Beijing, ChinaCollege of Earth and Planetary Sciences, University of Chinese Academy of Sciences, Beijing, ChinaKey Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing, ChinaFrance-China Joint Laboratory for Evolution and Development of Magnetotactic Multicellular Organisms, Chinese Academy of Sciences, Beijing, ChinaCollege of Earth and Planetary Sciences, University of Chinese Academy of Sciences, Beijing, ChinaKey Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing, ChinaFrance-China Joint Laboratory for Evolution and Development of Magnetotactic Multicellular Organisms, Chinese Academy of Sciences, Beijing, ChinaMagnetotactic bacteria (MTB) are a group of microbes that biomineralize membrane-bound, nanosized magnetite (Fe3O4), and/or greigite (Fe3S4) crystals in intracellular magnetic organelle magnetosomes. MTB belonging to the Nitrospirae phylum can form up to several hundreds of Fe3O4 magnetosome crystals and dozens of sulfur globules in a single cell. These MTB are widespread in aquatic environments and sometimes account for a significant proportion of microbial biomass near the oxycline, linking these lineages to the key steps of global iron and sulfur cycling. Despite their ecological and biogeochemical importance, our understanding of the diversity and ecophysiology of magnetotactic Nitrospirae is still very limited because this group of MTB remains unculturable. Here, we identify and characterize two previously unknown MTB populations within the Nitrospirae phylum through a combination of 16S rRNA gene-based and genome-resolved metagenomic analyses. These two MTB populations represent distinct morphotypes (rod-shaped and coccoid, designated as XYR, and XYC, respectively), and both form more than 100 bullet-shaped magnetosomal crystals per cell. High-quality draft genomes of XYR and XYC have been reconstructed, and they represent a novel species and a novel genus, respectively, according to their average amino-acid identity values with respect to available genomes. Accordingly, the names Candidatus Magnetobacterium cryptolimnobacter and Candidatus Magnetomicrobium cryptolimnococcus for XYR and XYC, respectively, were proposed. Further comparative genomic analyses of XYR, XYC, and previously reported magnetotactic Nitrospirae reveal the general metabolic potential of this MTB group in distinct microenvironments, including CO2 fixation, dissimilatory sulfate reduction, sulfide oxidation, nitrogen fixation, or denitrification processes. A remarkably conserved magnetosome gene cluster has been identified across Nitrospirae MTB genomes, indicating its putative important adaptive roles in these bacteria. Taken together, the present study provides novel insights into the phylogenomic diversity and ecophysiology of this intriguing, yet poorly understood MTB group.https://www.frontiersin.org/articles/10.3389/fmicb.2021.690052/fullmagnetotactic bacteriaNitrospiraemetagenomicsmagnetotaxismagnetosome gene cluster |
| spellingShingle | Wensi Zhang Wensi Zhang Wensi Zhang Yinzhao Wang Li Liu Li Liu Li Liu Yongxin Pan Yongxin Pan Yongxin Pan Wei Lin Wei Lin Identification and Genomic Characterization of Two Previously Unknown Magnetotactic Nitrospirae Frontiers in Microbiology magnetotactic bacteria Nitrospirae metagenomics magnetotaxis magnetosome gene cluster |
| title | Identification and Genomic Characterization of Two Previously Unknown Magnetotactic Nitrospirae |
| title_full | Identification and Genomic Characterization of Two Previously Unknown Magnetotactic Nitrospirae |
| title_fullStr | Identification and Genomic Characterization of Two Previously Unknown Magnetotactic Nitrospirae |
| title_full_unstemmed | Identification and Genomic Characterization of Two Previously Unknown Magnetotactic Nitrospirae |
| title_short | Identification and Genomic Characterization of Two Previously Unknown Magnetotactic Nitrospirae |
| title_sort | identification and genomic characterization of two previously unknown magnetotactic nitrospirae |
| topic | magnetotactic bacteria Nitrospirae metagenomics magnetotaxis magnetosome gene cluster |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2021.690052/full |
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