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論文

A Widespread group of large plasmids in methanotrophic ${it Methanoperedens}$ archaea

Schoelmerich, M. C.*; Oubouter, H. T.*; Sachdeva, R.*; Penev, P. I.*; 天野 由記; West-Roberts, J.*; Welte, C. U.*; Banfield, J. F.*

Nature Communications (Internet), 13, p.7085_1 - 7085_11, 2022/11

 被引用回数:3 パーセンタイル:80.68(Multidisciplinary Sciences)

Anaerobic methanotrophic archaea (ANME) make energy from the breakdown of methane, an important driver of global warming, yet the extrachromosomal genetic elements that impact the activities of ANME are little understood. Here we describe large plasmids associated with ANME of the Methanoperedens Genus. These have been maintained in two enrichment bioreactors that are highly dominated by different ${it Methanoperedens}$ species and associate with ${it Methanoperedens}$ species in other anaerobic environments. By manual curation we show that two of the plasmids are large (155,607 bp and 191,912 bp), circular, and replicate bidirectionally. The group of ${it Methanoperedens}$ species that carry these plasmids is related to ${it M. nitroreducens}$,${it M. ferrireducens}$ and ${it M. manganicus}$ and the plasmids occur in the same copy number as the main chromosome. The larger plasmid encodes transporters that potentially enhance ${it Methanoperedens}$ access to Ni, which is required for the MCR complex, Co required for the cobalamin cofactor needed for methyltransferases tied to central processes and amino acid uptake. We show that many plasmid genes are actively transcribed, including genes involved in plasmid chromosome maintenance and segregation, a Co$$^{2+}$$/Ni$$^{2+}$$ transporter and cell protective proteins. Notably, plasmid-borne genes for a ribosomal protein uL16 and adjacent elongation factor eEF2 are highly expressed. These are not encoded in the host ${it Methanoperedens}$ genome, indicating an obligate interdependence between this plasmid and its host. The finding of plasmids of ${it Methanoperedens}$ opens the way for the development of genetic vectors that could be used to probe little understood aspects of ${it Methanoperedens}$ physiology. Ultimately, this may provide a route to introduce or alter genes that may enhance growth and overall metabolism to accelerate methane oxidation rates.

論文

Patterns of gene content and co-occurrence constrain the evolutionary path toward animal association in Candidate Phyla Radiation bacteria

Jaffe, A. L.*; Thomas, A. D.*; He, C.*; Keren, R.*; Valentin-Alvarado, L. E.*; Munk, P.*; Bouma-Gregson, K.*; Farag, I. F.*; 天野 由記; Sachdeva, R.*; et al.

mBio, 12(4), p.e00521-21_1 - e00521-21_21, 2021/08

 被引用回数:16 パーセンタイル:90.71(Microbiology)

Candidate Phyla Radiation (CPR) bacteria are small, likely episymbiotic organisms found across Earth's ecosystems. Despite their prevalence, the distribution of CPR lineages across habitats and the genomic signatures of transitions amongst these habitats remain unclear. Hear, we expand the genome inventory for Absconditabacteria (SR1), Gracilibacteria, and Saccharibacteria (TM7), CPR bacteria known to occur in both animal-associated and environmental microbiomes, and investigate variation in gene content with habitat of origin. By overlaying phylogeny with habitat information, we show that bacteria from these three lineages have undergone multiple transitions from environmental habitats into animal microbiomes. Based on co-occurrence analyses of hundreds of metagenomes, we extend the prior suggestion that certain TM7 have broad bacterial host ranges and constrain possible host relationships for SR1 and Gracilibacteria. Full-proteome analyses show that animal-associated TM7 have smaller gene repertoires than their environmental counterparts and are enriched in numerous protein families, including those likely functioning in amino acid metabolism, phage defense, and detoxification of peroxide. In contrast, some freshwater TM7 encodea putative rhodopsin. For protein families exhibiting the clearest patterns of differential habitat distribution, we compared protein and species phylogenies to estimate the incidence of lateral gene transfer and genomic loss occurring over the species tree. These analyses suggest that habitat transitions were likely not accompanied by large transfer or loss events, but rather were associated with continuous proteome remodeling. Thus, we speculate that CPR habitat transitions were driven largely by availability of suitable host taxa, and were reinforced by acquisition and loss of some capacities.

論文

Groundwater $$Elusimicrobia$$ are metabolically diverse compared to gut microbiome $$Elusimicrobia$$ and some have a novel nitrogenase paralog

M$'e$heust, R.*; Castelle, C. J.*; Matheus Carnevali, P. B.*; Farag, I. F.*; He, C.*; Chen, L.-X.*; 天野 由記; Hug, L. A.*; Banfield, J. F.*

ISME Journal, 14(12), p.2907 - 2922, 2020/12

 被引用回数:34 パーセンタイル:94.46(Ecology)

We reconstructed 94 draft-quality, non-redundant genomes from diverse animal-associated and natural environments. Genomes group into 12 clades, 10 of which previously lacked reference genomes. Groundwater-associated $$Elusimicrobia$$ are predicted to be capable of heterotrophic or autotrophic lifestyles, reliant on oxygen or nitrate/nitrite-dependent respiration of fatty acids, or a variety of organic compounds and Rnf-dependent acetogenesis with hydrogen and carbon dioxide as the substrates. Genomes from two clades of groundwater-associated $$Elusimicrobia$$ often encode a new homologous group of nitrogenase-like proteins that co-occur with an extensive suite of radical SAM-based proteins. We identified similar genomic loci in genomes of bacteria from the Gracilibacteria and Myxococcus phyla and predict that the gene clusters reduce a tetrapyrrole, possibly to form a novel cofactor. The animal-associated $$Elusimicrobia$$ clades nest phylogenetically within two groundwater-associated clades. Thus, we propose an evolutionary trajectory in which some $$Elusimicrobia$$ adapted to animal-associated lifestyles from groundwater-associated species via genome reduction.

論文

Clades of huge phages from across Earth's ecosystems

Al-Shayeb, B.*; Sachdeva, R.*; Chen, L.-X.*; Ward, F.*; Munk, P.*; Devoto, A.*; Castelle, C. J.*; Olm, M. R.*; Bouma-Gregson, K.*; 天野 由記; et al.

Nature, 578(7795), p.425 - 431, 2020/02

 被引用回数:187 パーセンタイル:99.48(Multidisciplinary Sciences)

Phage typically have small genomes and depend on their bacterial hosts for replication. We generated metagenomic datasets from many diverse ecosystems and reconstructed hundreds of huge phage genomes, between 200 kbp and 716 kbp in length. Thirty four genomes were manually curated to completion, including the largest phage genomes yet reported. Expanded genetic repertoires include diverse and new CRISPR-Cas systems, tRNAs, tRNA synthetases, tRNA modification enzymes, initiation and elongation factors and ribosomal proteins. Phage CRISPR have the capacity to silence host transcription factors and translational genes, potentially as part of a larger interaction network that intercepts translation to redirect biosynthesis to phage-encoded functions. Some phage repurpose bacterial systems for phage-defense to eliminate competing phage. We phylogenetically define seven major clades of huge phage from human and other animal microbiomes, oceans, lakes, sediments, soils and the built environment. We conclude that large gene inventories reflect a conserved biological strategy, observed across a broad bacterial host range and resulting in the distribution of huge phage across Earth's ecosystems.

論文

Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria

Matheus Carnevali, P. B.*; Schulz, F.*; Castelle, C. J.*; Kantor, R. S.*; Shih, P.*; Sharon, I.*; Santini, J.*; Olm, M. R.*; 天野 由記; Thomas, B. C.*; et al.

Nature Communications (Internet), 10, p.463_1 - 463_15, 2019/01

 被引用回数:27 パーセンタイル:84.25(Multidisciplinary Sciences)

The metabolic platform in which microbial aerobic respiration evolved is tightly linked to the origins of Cyanobacteria (Oxyphotobacteria). Melainabacteria and Sericytochromatia, close phylogenetic neighbores to Oxyphotobacteria comprise both fermentative and aerobic representatives, or clades that are capablee of both. Here, we predict the metabolisms of Margulisbacteria from two distinct environments and Saganbacteria, and compare them to genomes of organisms from the related lineages. Melainabacteria BJ4A obtained from Mizunami site are potentially able to use O$$_{2}$$ and other terminal electron acceptors. The type C heme-copper oxygen reductase found in Melainabacteria BJ4A may be adapted to low O$$_{2}$$ levels, as expected for microaerophilic or anoxic environments such as the subsurface. Notably, Melainabacteria BJ4A seems to have a branched electron transport chain, with one branch leading to a cytochrome d ubiquinol oxidoreductase and the other one leading to the type C heme-copper oxygen reductase. Both these enzymes have high affinity for O$$_{2}$$, thus are adapted to low O$$_{2}$$ levels. These contemporary lineages have representatives with fermentative H$$_{2}$$-based metabolism, lineages capable of aerobic or anaerobic respiration, and lineages with both. Our findings support the idea that the ancestor of these lineages was an anaerobe in which fermentation and H$$_{2}$$ metabolism were central metabolic features.

論文

Ecological and genomic profiling of anaerobic methane-oxidizing archaea in a deep granitic environment

伊能 康平*; Hernsdorf, A. W.*; 今野 祐多*; 幸塚 麻里子*; 柳川 克則*; 加藤 信吾*; 砂村 道成*; 広田 秋成*; 東郷 洋子*; 伊藤 一誠*; et al.

ISME Journal, 12(1), p.31 - 47, 2018/01

 被引用回数:45 パーセンタイル:91.3(Ecology)

岐阜県瑞浪市の超深地層研究所において、深度300メートルの地下水を地下坑道から採取し、地下微生物の生態系を調査した。その結果、花崗岩深部でマグマ由来のメタンに依存した微生物生態系が存在することを明らかにした。

論文

Potential for microbial H$$_{2}$$ and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments

Hernsdorf, A. W.*; 天野 由記; 宮川 和也; 伊勢 孝太郎; 鈴木 庸平*; Anantharaman, K.*; Probst, A. J.*; Burstein, D.*; Thomas, B. C.*; Banfield, J. F.*

ISME Journal, 11, p.1915 - 1929, 2017/03

AA2016-0002.pdf:2.21MB

 被引用回数:78 パーセンタイル:95.93(Ecology)

地層処分システムにおける微生物影響の可能性を評価するために、北海道の幌延深地層研究センター地下施設を利用して、堆積岩地下の生態系における微生物群集構造と代謝機能について調査を行った。全体として、微生物生態系は多様な系統群からなる微生物種で構成されており、その多くはこれまで培養されていない生物門に属していることが示された。大部分の微生物種は、酸化型[NiFe]ヒドロゲナーゼあるいはフェレドキシンをベースとする代謝経路を可能にする電子分岐型[FeFe]ヒドロゲナーゼを介して水素代謝をおこなうことが明らかになった。水素代謝と関連して、多くの微生物が炭素,窒素,鉄および硫黄を代謝することが推定された。特に、ANME-2dというメタン酸化を行う古細菌として知られている未培養微生物が、鉄関連の代謝反応を行う可能性が示唆された。得られた結果から、幌延堆積岩環境における微生物群集の生態学的概念モデルを推定した。

論文

A New view of the tree of life

Hug, L. A.*; Baker, B. J.*; Anantharaman, K.*; Brown, C. T.*; Probst, A. J.*; Castelle, C. J.*; Butterfield, C. N.*; Hernsdorf, A. W.*; 天野 由記; 伊勢 孝太郎; et al.

Nature Microbiology (Internet), 1(5), p.16048_1 - 16048_6, 2016/05

 被引用回数:1110 パーセンタイル:99.97(Microbiology)

生命の系統樹は生物学において最も重要な中心テーマの一つである。遺伝子調査によると、莫大な数のブランチの存在が示唆されているが、フルスケールに近い系統樹でさえわかりにくいのが現状である。本研究では、これまでに報告されてきた配列情報に加えて、新たに取得した未培養生物のゲノム情報を用いて、バクテリア,アーキア,真核生物を含む系統樹を更新した。系統樹の描写は、全体的な概容とそれぞれの主要な系統における多様性のスナップショットの両方について行った。その結果、バクテリアの多様化の優勢性が示され、培養されていない生物種の重要性とともに主要な放射構造においてそれらの生物種の重要な進化が集中している現象が強調された。

口頭

Sulfur and hydrogen metabolism linked to CO$$_{2}$$ fixation by abundant Nitrospirae in the deep subsurface

天野 由記; Anantharaman, K.*; Tomas, B. C.*; Olm, M.*; Burstein, D.*; Castelle, C. J.*; 別部 光里*; 宮川 和也; 岩月 輝希; 鈴木 庸平*; et al.

no journal, , 

The bacterial phylum Nitrospirae is phylogenetically diverse. There are relatively few isolated representatives available for laboratory study and the physiology, functions and distributions of these bacteria across environments remain largely unknown. To understand the ecological role of Nitrospirae in the deep subsurface, we analyzed metagenomically-derived near complete genomes from groundwaters associated with granite and sedimentary rock where Nitrospirae are very abundant. The bacteria are autotrophs that fix CO$$_{2}$$ via the Wood-Ljungdahl pathway and reductive TCA cycles. The genomes encode versatile energy-generating pathways that involve sulfate reduction, hydrogen oxidation and nitrite reduction. Phylogenetic analyses indicate that the organisms are most similar to the isolated magnetotactic bacterium, Candidatus Magnetobacterium bavaricum, with only 89-91% 16S rRNA gene sequence identity. These Nitrospirae bacteria appear to play critical ecosystem roles as primary producers and they are likely central to sulfur cycling in the deep subsurface.

口頭

Vast metabolic and phylogenetic diversity shared across deep subsurface environments

天野 由記; Diamond, S.*; Lavy, A.*; Anantharaman, K.*; 宮川 和也; 岩月 輝希; 別部 光里*; 鈴木 庸平*; Thomas, B. C.*; Banfield, J. F.*

no journal, , 

We investigated the microbiology two Japanese subsurface research sites and compared the major groups of organisms lacking cultivated representatives found from other subsurface sites, including a Colorado aquifer and deep aquifers underlying the Crystal Geyser. We analyzed metagenomic data 19 samples from the Horonobe site and 7 from the Mizunami site. DNA sequences from each sample were assembled independently and scaffolds encoding the ribosomal protein S3 sequence were identified. The major characteristic of the microbiology of the Mizumani site that distinguished it from the Horonobe site is local very high abundances of Nitrospirae, Parcubacteria, Ignavibacteria, ANME-2D and Micrarchaeota. In contrast, the Horonobe site has locations that are highly enriched in Altarchiales, Syntrophobacteriales, Atribacteria, ANME-2D and Methanogens. Beyond reshaping the Tree of Life, the societal importance of these discoveries remains little known. However, given the huge inventory of new groups of proteins and pathways in the genomes of these organisms, it is reasonable to anticipate major discoveries will hold relevance, for example, in terms of pharmaceutical discovery. Given the importance of the subsurface as a potential host environment for storage of nuclear waste, finding some commonality would indicate the general relevance of information from one site for prediction of the characteristics of other sites.

口頭

Existence and the role of subsurface biofilm in the deep sedimentary rock environment of the Horonobe area, Hokkaido, Japan

天野 由記; 別部 光里*; 遠藤 貴志*; 根本 一昭*; 佐藤 智文*; Thomas, B. C.*; Banfield, J. F.*

no journal, , 

We investigated the geochemical and microbial properties of groundwater samples and the habitat of biofilm collected from a borehole drilled in the Horonobe Underground Research Laboratories (Horonobe URL) at Horonobe area, Hokkaido, Japan. Samples were collected from a borehole at 140 m below the surface in the Horonobe URL, and the time series changes of geochemistry, microbial abundance, and microbial diversity were monitored for four days. To understand the ecological role of the biofilm in the deep subsurface, we analyzed metagenomically derived genome data from the groundwater samples. From the results of microscopic observation, it is indicated that abundant biofilm were collected in the groundwater samples. Analysis of 16S rRNA gene by next generation sequencing indicates that the biofilms were dominated by Candidatus Altiarchaeales (SM1 Euryarchaeon) in the methane- carbonate-rich groundwater. The genomes encode autotrophic metabolism that fix CO$$_{2}$$ via the Wood-Ljungdahl pathway and reductive tricarboxylic acid (TCA) cycles. The genes for polysaccharide biosynthesis were detected in the SM1 genomes. Biofilm phase were also characterized with accumulation/sorption of heavy metals such as Cr, Fe, Ni, Cu, Pb, Ce, Nd, U and Th. From the calculation of the bioaccumulation factor for the concentration of heavy metals, it is possible that the biofilms selectively accumulate heavy metals according to their metabolic activity. Hence, it is necessary to evaluate mechanisms of interaction between heavy metals, microbial community structure and metabolic activities of biofilms. The biofilm-mineral interaction provides an implication for the possible retardation of radionuclide migration in subsurface hydrology, which is of practical interest in geological disposal systems for high-level radioactive waste.

口頭

Spatial distribution of biofilm-forming Archaea in the deep sedimentary rock environment of the Horonobe area, Hokkaido, Japan

天野 由記; 別部 光里*; 佐藤 智文*; 望月 陽人; Thomas, B. C.*; Banfield, J. F.*

no journal, , 

The presence of microbes in deep subsurface environments may have important implications for the safety of underground repositories for high-level radioactive wastes. It has been suggested that biofilm may not exist in the deep subsurface due to low water flux, energy supply and physical space. We investigated spatial distribution of biofilm-forming Archaea, Candidatus Altiarchaeales, and the geochemical and microbiological properties of groundwater samples via study of boreholes drilled in the Horonobe Underground Research Laboratories (Horonobe URL), Horonobe area, Hokkaido, Japan. Samples were collected from four boreholes at 140, 250, 350 m below the surface in the Horonobe URL, and the time series changes of geochemistry, microbial abundance, and microbial diversity were monitored over several years. Analysis of metagenome and 16S rRNA genes by next generation sequencing indicates that the biofilms in methane- carbonate-rich groundwater were mainly dominated by Candidatus Altiarchaeales. Based on the section volume and the amount of discharged groundwater from the borehole, it is suggested that the biofilms occur within porous sedimentary rocks or fracture surfaces, rather than on the borehole walls. The biofilm accumulates heavy metals including Cr, Fe, Ni, Cu, Pb, Ce, Nd, U and Th. From the calculation of the bioaccumulation factor for the concentration of heavy metals, it is possible that the biofilms selectively accumulate heavy metals. Thus, the presence of biofilms provides a mechanism for retardation of radionuclide migration in the subsurface. This is of practical interest from the perspective of geological disposal systems for high-level radioactive waste in the deep subsurface.

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