Potential autotrophic carbon-fixer and Fe(II)-oxidizer Alcanivorax sp. MM125-6 isolated from Wocan hydrothermal field
The genus Alcanivorax is common in various marine environments, including in hydrothermal fields. They were previously recognized as obligate hydrocarbonoclastic bacteria, but their potential for autotrophic carbon fixation and Fe(II)-oxidation remains largely elusive. In this study, an in situ enri...
Main Authors: | , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Frontiers Media S.A.
2022-10-01
|
Series: | Frontiers in Microbiology |
Subjects: | |
Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.930601/full |
_version_ | 1811241330171445248 |
---|---|
author | Mingcong Wei Mingcong Wei Xiang Zeng Xiqiu Han Xiqiu Han Zongze Shao Qian Xie Qian Xie Chuanqi Dong Chuanqi Dong Yejian Wang Zhongyan Qiu |
author_facet | Mingcong Wei Mingcong Wei Xiang Zeng Xiqiu Han Xiqiu Han Zongze Shao Qian Xie Qian Xie Chuanqi Dong Chuanqi Dong Yejian Wang Zhongyan Qiu |
author_sort | Mingcong Wei |
collection | DOAJ |
description | The genus Alcanivorax is common in various marine environments, including in hydrothermal fields. They were previously recognized as obligate hydrocarbonoclastic bacteria, but their potential for autotrophic carbon fixation and Fe(II)-oxidation remains largely elusive. In this study, an in situ enrichment experiment was performed using a hydrothermal massive sulfide slab deployed 300 m away from the Wocan hydrothermal vent. Furthermore, the biofilms on the surface of the slab were used as an inoculum, with hydrothermal massive sulfide powder from the same vent as an energy source, to enrich the potential iron oxidizer in the laboratory. Three dominant bacterial families, Alcanivoraceae, Pseudomonadaceae, and Rhizobiaceae, were enriched in the medium with hydrothermal massive sulfides. Subsequently, strain Alcanivorax sp. MM125-6 was isolated from the enrichment culture. It belongs to the genus Alcanivorax and is closely related to Alcanivorax profundimaris ST75FaO-1T (98.9% sequence similarity) indicated by a phylogenetic analysis based on 16S rRNA gene sequences. Autotrophic growth experiments on strain MM125-6 revealed that the cell concentrations were increased from an initial 7.5 × 105 cells/ml to 3.13 × 108 cells/ml after 10 days, and that the δ13CVPDB in the cell biomass was also increased from 234.25‰ on day 2 to gradually 345.66 ‰ on day 10. The gradient tube incubation showed that bands of iron oxides and cells formed approximately 1 and 1.5 cm, respectively, below the air-agarose medium interface. In addition, the SEM-EDS data demonstrated that it can also secrete acidic exopolysaccharides and adhere to the surface of sulfide minerals to oxidize Fe(II) with NaHCO3 as the sole carbon source, which accelerates hydrothermal massive sulfide dissolution. These results support the conclusion that strain MM125-6 is capable of autotrophic carbon fixation and Fe(II) oxidization chemoautotrophically. This study expands our understanding of the metabolic versatility of the Alcanivorax genus as well as their important role(s) in coupling hydrothermal massive sulfide weathering and iron and carbon cycles in hydrothermal fields. |
first_indexed | 2024-04-12T13:33:58Z |
format | Article |
id | doaj.art-80d95a75fa1d459d9e29e2c0c7aed020 |
institution | Directory Open Access Journal |
issn | 1664-302X |
language | English |
last_indexed | 2024-04-12T13:33:58Z |
publishDate | 2022-10-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Microbiology |
spelling | doaj.art-80d95a75fa1d459d9e29e2c0c7aed0202022-12-22T03:31:05ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-10-011310.3389/fmicb.2022.930601930601Potential autotrophic carbon-fixer and Fe(II)-oxidizer Alcanivorax sp. MM125-6 isolated from Wocan hydrothermal fieldMingcong Wei0Mingcong Wei1Xiang Zeng2Xiqiu Han3Xiqiu Han4Zongze Shao5Qian Xie6Qian Xie7Chuanqi Dong8Chuanqi Dong9Yejian Wang10Zhongyan Qiu11Ocean College, Zhejiang University, Zhoushan, ChinaKey Laboratory of Submarine Geosciences, Second Institute of Oceanography, Ministry of Natural Resources, Hangzhou, ChinaKey Laboratory of Marine Biogenetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaOcean College, Zhejiang University, Zhoushan, ChinaKey Laboratory of Submarine Geosciences, Second Institute of Oceanography, Ministry of Natural Resources, Hangzhou, ChinaKey Laboratory of Marine Biogenetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, ChinaKey Laboratory of Submarine Geosciences, Second Institute of Oceanography, Ministry of Natural Resources, Hangzhou, ChinaSchool of Oceanography, Shanghai Jiao Tong University, Shanghai, ChinaKey Laboratory of Submarine Geosciences, Second Institute of Oceanography, Ministry of Natural Resources, Hangzhou, ChinaCollege of Marine Geosciences, Ocean University of China, Qingdao, ChinaKey Laboratory of Submarine Geosciences, Second Institute of Oceanography, Ministry of Natural Resources, Hangzhou, ChinaKey Laboratory of Submarine Geosciences, Second Institute of Oceanography, Ministry of Natural Resources, Hangzhou, ChinaThe genus Alcanivorax is common in various marine environments, including in hydrothermal fields. They were previously recognized as obligate hydrocarbonoclastic bacteria, but their potential for autotrophic carbon fixation and Fe(II)-oxidation remains largely elusive. In this study, an in situ enrichment experiment was performed using a hydrothermal massive sulfide slab deployed 300 m away from the Wocan hydrothermal vent. Furthermore, the biofilms on the surface of the slab were used as an inoculum, with hydrothermal massive sulfide powder from the same vent as an energy source, to enrich the potential iron oxidizer in the laboratory. Three dominant bacterial families, Alcanivoraceae, Pseudomonadaceae, and Rhizobiaceae, were enriched in the medium with hydrothermal massive sulfides. Subsequently, strain Alcanivorax sp. MM125-6 was isolated from the enrichment culture. It belongs to the genus Alcanivorax and is closely related to Alcanivorax profundimaris ST75FaO-1T (98.9% sequence similarity) indicated by a phylogenetic analysis based on 16S rRNA gene sequences. Autotrophic growth experiments on strain MM125-6 revealed that the cell concentrations were increased from an initial 7.5 × 105 cells/ml to 3.13 × 108 cells/ml after 10 days, and that the δ13CVPDB in the cell biomass was also increased from 234.25‰ on day 2 to gradually 345.66 ‰ on day 10. The gradient tube incubation showed that bands of iron oxides and cells formed approximately 1 and 1.5 cm, respectively, below the air-agarose medium interface. In addition, the SEM-EDS data demonstrated that it can also secrete acidic exopolysaccharides and adhere to the surface of sulfide minerals to oxidize Fe(II) with NaHCO3 as the sole carbon source, which accelerates hydrothermal massive sulfide dissolution. These results support the conclusion that strain MM125-6 is capable of autotrophic carbon fixation and Fe(II) oxidization chemoautotrophically. This study expands our understanding of the metabolic versatility of the Alcanivorax genus as well as their important role(s) in coupling hydrothermal massive sulfide weathering and iron and carbon cycles in hydrothermal fields.https://www.frontiersin.org/articles/10.3389/fmicb.2022.930601/fullAlcanivoraxautotrophic carbon fixationFe(II)-oxidationin situ enrichmenthydrothermal massive sulfide |
spellingShingle | Mingcong Wei Mingcong Wei Xiang Zeng Xiqiu Han Xiqiu Han Zongze Shao Qian Xie Qian Xie Chuanqi Dong Chuanqi Dong Yejian Wang Zhongyan Qiu Potential autotrophic carbon-fixer and Fe(II)-oxidizer Alcanivorax sp. MM125-6 isolated from Wocan hydrothermal field Frontiers in Microbiology Alcanivorax autotrophic carbon fixation Fe(II)-oxidation in situ enrichment hydrothermal massive sulfide |
title | Potential autotrophic carbon-fixer and Fe(II)-oxidizer Alcanivorax sp. MM125-6 isolated from Wocan hydrothermal field |
title_full | Potential autotrophic carbon-fixer and Fe(II)-oxidizer Alcanivorax sp. MM125-6 isolated from Wocan hydrothermal field |
title_fullStr | Potential autotrophic carbon-fixer and Fe(II)-oxidizer Alcanivorax sp. MM125-6 isolated from Wocan hydrothermal field |
title_full_unstemmed | Potential autotrophic carbon-fixer and Fe(II)-oxidizer Alcanivorax sp. MM125-6 isolated from Wocan hydrothermal field |
title_short | Potential autotrophic carbon-fixer and Fe(II)-oxidizer Alcanivorax sp. MM125-6 isolated from Wocan hydrothermal field |
title_sort | potential autotrophic carbon fixer and fe ii oxidizer alcanivorax sp mm125 6 isolated from wocan hydrothermal field |
topic | Alcanivorax autotrophic carbon fixation Fe(II)-oxidation in situ enrichment hydrothermal massive sulfide |
url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.930601/full |
work_keys_str_mv | AT mingcongwei potentialautotrophiccarbonfixerandfeiioxidizeralcanivoraxspmm1256isolatedfromwocanhydrothermalfield AT mingcongwei potentialautotrophiccarbonfixerandfeiioxidizeralcanivoraxspmm1256isolatedfromwocanhydrothermalfield AT xiangzeng potentialautotrophiccarbonfixerandfeiioxidizeralcanivoraxspmm1256isolatedfromwocanhydrothermalfield AT xiqiuhan potentialautotrophiccarbonfixerandfeiioxidizeralcanivoraxspmm1256isolatedfromwocanhydrothermalfield AT xiqiuhan potentialautotrophiccarbonfixerandfeiioxidizeralcanivoraxspmm1256isolatedfromwocanhydrothermalfield AT zongzeshao potentialautotrophiccarbonfixerandfeiioxidizeralcanivoraxspmm1256isolatedfromwocanhydrothermalfield AT qianxie potentialautotrophiccarbonfixerandfeiioxidizeralcanivoraxspmm1256isolatedfromwocanhydrothermalfield AT qianxie potentialautotrophiccarbonfixerandfeiioxidizeralcanivoraxspmm1256isolatedfromwocanhydrothermalfield AT chuanqidong potentialautotrophiccarbonfixerandfeiioxidizeralcanivoraxspmm1256isolatedfromwocanhydrothermalfield AT chuanqidong potentialautotrophiccarbonfixerandfeiioxidizeralcanivoraxspmm1256isolatedfromwocanhydrothermalfield AT yejianwang potentialautotrophiccarbonfixerandfeiioxidizeralcanivoraxspmm1256isolatedfromwocanhydrothermalfield AT zhongyanqiu potentialautotrophiccarbonfixerandfeiioxidizeralcanivoraxspmm1256isolatedfromwocanhydrothermalfield |