Oxygen tolerance and detoxification mechanisms of highly enriched planktonic anaerobic ammonium-oxidizing (anammox) bacteria
Abstract Oxygen is a key regulatory factor of anaerobic ammonium oxidation (anammox). Although the inhibitory effect of oxygen is evident, a wide range of oxygen sensitivities of anammox bacteria have been reported so far, which makes it difficult to model the marine nitrogen loss and design anammox...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Oxford University Press
2023-05-01
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| Series: | ISME Communications |
| Online Access: | https://doi.org/10.1038/s43705-023-00251-7 |
| _version_ | 1797228635697971200 |
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| author | Satoshi Okabe Shaoyu Ye Xi Lan Keishi Nukada Haozhe Zhang Kanae Kobayashi Mamoru Oshiki |
| author_facet | Satoshi Okabe Shaoyu Ye Xi Lan Keishi Nukada Haozhe Zhang Kanae Kobayashi Mamoru Oshiki |
| author_sort | Satoshi Okabe |
| collection | DOAJ |
| description | Abstract Oxygen is a key regulatory factor of anaerobic ammonium oxidation (anammox). Although the inhibitory effect of oxygen is evident, a wide range of oxygen sensitivities of anammox bacteria have been reported so far, which makes it difficult to model the marine nitrogen loss and design anammox-based technologies. Here, oxygen tolerance and detoxification mechanisms of four genera of anammox bacteria; one marine species (“Ca. Scalindua sp.”) and four freshwater anammox species (“Ca. Brocadia sinica”, “Ca. Brocadia sapporoensis”, “Ca. Jettenia caeni”, and “Ca. Kuenenia stuttgartiensis”) were determined and then related to the activities of anti-oxidative enzymes. Highly enriched planktonic anammox cells were exposed to various levels of oxygen, and oxygen inhibition kinetics (50% inhibitory concentration (IC50) and upper O2 limits (DOmax) of anammox activity) were quantitatively determined. A marine anammox species, “Ca. Scalindua sp.”, exhibited much higher oxygen tolerance capability (IC50 = 18.0 µM and DOmax = 51.6 µM) than freshwater species (IC50 = 2.7–4.2 µM and DOmax = 10.9–26.6 µM). The upper DO limit of “Ca. Scalindua sp.” was much higher than the values reported so far (~20 µM). Furthermore, the oxygen inhibition was reversible even after exposed to ambient air for 12–24 h. The comparative genome analysis confirmed that all anammox species commonly possess the genes considered to function for reduction of O2, superoxide anion (O2 •-), and H2O2. However, the superoxide reductase (Sor)-peroxidase dependent detoxification system alone may not be sufficient for cell survival under microaerobic conditions. Despite the fact that anaerobes normally possess no or little superoxide dismutase (Sod) or catalase (Cat), only Scalindua exhibited high Sod activity of 22.6 ± 1.9 U/mg-protein with moderate Cat activity of 1.6 ± 0.7 U/mg-protein, which was consistent with the genome sequence analysis. This Sod-Cat dependent detoxification system could be responsible for the higher O2 tolerance of Scalindua than other freshwater anammox species lacking the Sod activity. |
| first_indexed | 2024-04-24T14:59:50Z |
| format | Article |
| id | doaj.art-63e147be5a3e4c0f81e5c096a4468cc7 |
| institution | Directory Open Access Journal |
| issn | 2730-6151 |
| language | English |
| last_indexed | 2024-04-24T14:59:50Z |
| publishDate | 2023-05-01 |
| publisher | Oxford University Press |
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| series | ISME Communications |
| spelling | doaj.art-63e147be5a3e4c0f81e5c096a4468cc72024-04-02T16:19:33ZengOxford University PressISME Communications2730-61512023-05-013111310.1038/s43705-023-00251-7Oxygen tolerance and detoxification mechanisms of highly enriched planktonic anaerobic ammonium-oxidizing (anammox) bacteriaSatoshi Okabe0Shaoyu Ye1Xi Lan2Keishi Nukada3Haozhe Zhang4Kanae Kobayashi5Mamoru Oshiki6Department of Environmental Engineering, Faculty of Engineering, Hokkaido UniversityDepartment of Environmental Engineering, Faculty of Engineering, Hokkaido UniversityDepartment of Environmental Engineering, Faculty of Engineering, Hokkaido UniversityDepartment of Environmental Engineering, Faculty of Engineering, Hokkaido UniversityDepartment of Environmental Engineering, Faculty of Engineering, Hokkaido UniversityDepartment of Environmental Engineering, Faculty of Engineering, Hokkaido UniversityDepartment of Environmental Engineering, Faculty of Engineering, Hokkaido UniversityAbstract Oxygen is a key regulatory factor of anaerobic ammonium oxidation (anammox). Although the inhibitory effect of oxygen is evident, a wide range of oxygen sensitivities of anammox bacteria have been reported so far, which makes it difficult to model the marine nitrogen loss and design anammox-based technologies. Here, oxygen tolerance and detoxification mechanisms of four genera of anammox bacteria; one marine species (“Ca. Scalindua sp.”) and four freshwater anammox species (“Ca. Brocadia sinica”, “Ca. Brocadia sapporoensis”, “Ca. Jettenia caeni”, and “Ca. Kuenenia stuttgartiensis”) were determined and then related to the activities of anti-oxidative enzymes. Highly enriched planktonic anammox cells were exposed to various levels of oxygen, and oxygen inhibition kinetics (50% inhibitory concentration (IC50) and upper O2 limits (DOmax) of anammox activity) were quantitatively determined. A marine anammox species, “Ca. Scalindua sp.”, exhibited much higher oxygen tolerance capability (IC50 = 18.0 µM and DOmax = 51.6 µM) than freshwater species (IC50 = 2.7–4.2 µM and DOmax = 10.9–26.6 µM). The upper DO limit of “Ca. Scalindua sp.” was much higher than the values reported so far (~20 µM). Furthermore, the oxygen inhibition was reversible even after exposed to ambient air for 12–24 h. The comparative genome analysis confirmed that all anammox species commonly possess the genes considered to function for reduction of O2, superoxide anion (O2 •-), and H2O2. However, the superoxide reductase (Sor)-peroxidase dependent detoxification system alone may not be sufficient for cell survival under microaerobic conditions. Despite the fact that anaerobes normally possess no or little superoxide dismutase (Sod) or catalase (Cat), only Scalindua exhibited high Sod activity of 22.6 ± 1.9 U/mg-protein with moderate Cat activity of 1.6 ± 0.7 U/mg-protein, which was consistent with the genome sequence analysis. This Sod-Cat dependent detoxification system could be responsible for the higher O2 tolerance of Scalindua than other freshwater anammox species lacking the Sod activity.https://doi.org/10.1038/s43705-023-00251-7 |
| spellingShingle | Satoshi Okabe Shaoyu Ye Xi Lan Keishi Nukada Haozhe Zhang Kanae Kobayashi Mamoru Oshiki Oxygen tolerance and detoxification mechanisms of highly enriched planktonic anaerobic ammonium-oxidizing (anammox) bacteria ISME Communications |
| title | Oxygen tolerance and detoxification mechanisms of highly enriched planktonic anaerobic ammonium-oxidizing (anammox) bacteria |
| title_full | Oxygen tolerance and detoxification mechanisms of highly enriched planktonic anaerobic ammonium-oxidizing (anammox) bacteria |
| title_fullStr | Oxygen tolerance and detoxification mechanisms of highly enriched planktonic anaerobic ammonium-oxidizing (anammox) bacteria |
| title_full_unstemmed | Oxygen tolerance and detoxification mechanisms of highly enriched planktonic anaerobic ammonium-oxidizing (anammox) bacteria |
| title_short | Oxygen tolerance and detoxification mechanisms of highly enriched planktonic anaerobic ammonium-oxidizing (anammox) bacteria |
| title_sort | oxygen tolerance and detoxification mechanisms of highly enriched planktonic anaerobic ammonium oxidizing anammox bacteria |
| url | https://doi.org/10.1038/s43705-023-00251-7 |
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