Copper-Nanocoated Ultra-Small Cells in Grain Boundaries Inside an Extinct Vent Chimney
Chemosynthetic organisms flourish around deep-sea hydrothermal vents where energy-rich fluids are emitted from metal sulfide chimneys. However, microbial life hosted in mineral assemblages in extinct chimneys lacking fluid venting remains largely unknown. The interior of extinct chimneys remains ano...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-06-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.864205/full |
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| author | Hinako Takamiya Mariko Kouduka Hitoshi Furutani Hiroki Mukai Kaoru Nakagawa Takushi Yamamoto Shingo Kato Yu Kodama Naotaka Tomioka Motoo Ito Yohey Suzuki |
| author_facet | Hinako Takamiya Mariko Kouduka Hitoshi Furutani Hiroki Mukai Kaoru Nakagawa Takushi Yamamoto Shingo Kato Yu Kodama Naotaka Tomioka Motoo Ito Yohey Suzuki |
| author_sort | Hinako Takamiya |
| collection | DOAJ |
| description | Chemosynthetic organisms flourish around deep-sea hydrothermal vents where energy-rich fluids are emitted from metal sulfide chimneys. However, microbial life hosted in mineral assemblages in extinct chimneys lacking fluid venting remains largely unknown. The interior of extinct chimneys remains anoxic where the percolation of oxygenated seawater is limited within tightly packed metal sulfide grains. Given the scarcity of photosynthetic organics in deep seawater, anaerobic microbes might inhabit the grain boundaries energetically depending on substrates derived from rock-water interactions. In this study, we reported ultra-small cells directly visualized in grain boundaries of CuFeS2 inside an extinct metal sulfide chimney from the southern Mariana Trough. Nanoscale solid analyses reveal that ultra-small cells are coated with Cu2O nanocrystals in grain boundaries enriched with C, N, and P. In situ spectroscopic and spectrometric characterizations demonstrate the distribution of organics with amide groups and a large molecular organic compound in the grain boundaries. We inferred that the ultra-small cells are anaerobes because of the fast dissolution of Cu2O nanocrystals in oxygenated solution. This Cu2O property also excludes the possibility of microbial contamination from ambient seawater during sampling. It is shown by 16S rRNA gene sequence analysis that the chimney interior is dominated by Pacearchaeota known to have anaerobic metabolisms and ultra-small cells. Our results support the potential existence of photosynthesis-independent microbial ecosystems in grain boundaries in submarine metal sulfides deposits on the early Earth. |
| first_indexed | 2024-04-13T21:19:24Z |
| format | Article |
| id | doaj.art-4e2d112a47af46edba00c272972fb1ba |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-13T21:19:24Z |
| publishDate | 2022-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-4e2d112a47af46edba00c272972fb1ba2022-12-22T02:29:34ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-06-011310.3389/fmicb.2022.864205864205Copper-Nanocoated Ultra-Small Cells in Grain Boundaries Inside an Extinct Vent ChimneyHinako Takamiya0Mariko Kouduka1Hitoshi Furutani2Hiroki Mukai3Kaoru Nakagawa4Takushi Yamamoto5Shingo Kato6Yu Kodama7Naotaka Tomioka8Motoo Ito9Yohey Suzuki10Department of Earth and Planetary Science, The University of Tokyo, Bunkyo City, JapanDepartment of Earth and Planetary Science, The University of Tokyo, Bunkyo City, JapanDepartment of Earth and Planetary Science, The University of Tokyo, Bunkyo City, JapanFaculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, JapanSolutions COE, Analytical & Measuring Instruments Division, Shimadzu Corporation, Kyoto, JapanSolutions COE, Analytical & Measuring Instruments Division, Shimadzu Corporation, Kyoto, JapanJapan Collection of Microorganisms (JCM), RIKEN BioResource Research Center, Tsukuba, JapanTOYO Corporation, Chuo City, JapanKochi Institute for Core Sample Research, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Nankoku, JapanKochi Institute for Core Sample Research, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Nankoku, JapanDepartment of Earth and Planetary Science, The University of Tokyo, Bunkyo City, JapanChemosynthetic organisms flourish around deep-sea hydrothermal vents where energy-rich fluids are emitted from metal sulfide chimneys. However, microbial life hosted in mineral assemblages in extinct chimneys lacking fluid venting remains largely unknown. The interior of extinct chimneys remains anoxic where the percolation of oxygenated seawater is limited within tightly packed metal sulfide grains. Given the scarcity of photosynthetic organics in deep seawater, anaerobic microbes might inhabit the grain boundaries energetically depending on substrates derived from rock-water interactions. In this study, we reported ultra-small cells directly visualized in grain boundaries of CuFeS2 inside an extinct metal sulfide chimney from the southern Mariana Trough. Nanoscale solid analyses reveal that ultra-small cells are coated with Cu2O nanocrystals in grain boundaries enriched with C, N, and P. In situ spectroscopic and spectrometric characterizations demonstrate the distribution of organics with amide groups and a large molecular organic compound in the grain boundaries. We inferred that the ultra-small cells are anaerobes because of the fast dissolution of Cu2O nanocrystals in oxygenated solution. This Cu2O property also excludes the possibility of microbial contamination from ambient seawater during sampling. It is shown by 16S rRNA gene sequence analysis that the chimney interior is dominated by Pacearchaeota known to have anaerobic metabolisms and ultra-small cells. Our results support the potential existence of photosynthesis-independent microbial ecosystems in grain boundaries in submarine metal sulfides deposits on the early Earth.https://www.frontiersin.org/articles/10.3389/fmicb.2022.864205/fullmetal sulfide depositssubmicron-scale biosignature analysesnanometer-scale solid characterizationsrock-hosted lifedeep-sea hydrothermal vent |
| spellingShingle | Hinako Takamiya Mariko Kouduka Hitoshi Furutani Hiroki Mukai Kaoru Nakagawa Takushi Yamamoto Shingo Kato Yu Kodama Naotaka Tomioka Motoo Ito Yohey Suzuki Copper-Nanocoated Ultra-Small Cells in Grain Boundaries Inside an Extinct Vent Chimney Frontiers in Microbiology metal sulfide deposits submicron-scale biosignature analyses nanometer-scale solid characterizations rock-hosted life deep-sea hydrothermal vent |
| title | Copper-Nanocoated Ultra-Small Cells in Grain Boundaries Inside an Extinct Vent Chimney |
| title_full | Copper-Nanocoated Ultra-Small Cells in Grain Boundaries Inside an Extinct Vent Chimney |
| title_fullStr | Copper-Nanocoated Ultra-Small Cells in Grain Boundaries Inside an Extinct Vent Chimney |
| title_full_unstemmed | Copper-Nanocoated Ultra-Small Cells in Grain Boundaries Inside an Extinct Vent Chimney |
| title_short | Copper-Nanocoated Ultra-Small Cells in Grain Boundaries Inside an Extinct Vent Chimney |
| title_sort | copper nanocoated ultra small cells in grain boundaries inside an extinct vent chimney |
| topic | metal sulfide deposits submicron-scale biosignature analyses nanometer-scale solid characterizations rock-hosted life deep-sea hydrothermal vent |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.864205/full |
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