Activity and Metabolic Versatility of Complete Ammonia Oxidizers in Full-Scale Wastewater Treatment Systems
ABSTRACT The recent discovery of complete ammonia oxidizers (comammox) contradicts the paradigm that chemolithoautotrophic nitrification is always catalyzed by two different microorganisms. However, our knowledge of the survival strategies of comammox in complex ecosystems, such as full-scale wastew...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2020-04-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.03175-19 |
| _version_ | 1818901036742475776 |
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| author | Yuchun Yang Holger Daims Yang Liu Craig W. Herbold Petra Pjevac Jih-Gaw Lin Meng Li Ji-Dong Gu |
| author_facet | Yuchun Yang Holger Daims Yang Liu Craig W. Herbold Petra Pjevac Jih-Gaw Lin Meng Li Ji-Dong Gu |
| author_sort | Yuchun Yang |
| collection | DOAJ |
| description | ABSTRACT The recent discovery of complete ammonia oxidizers (comammox) contradicts the paradigm that chemolithoautotrophic nitrification is always catalyzed by two different microorganisms. However, our knowledge of the survival strategies of comammox in complex ecosystems, such as full-scale wastewater treatment plants (WWTPs), remains limited. Analyses of genomes and in situ transcriptomes of four comammox organisms from two full-scale WWTPs revealed that comammox were active and showed a surprisingly high metabolic versatility. A gene cluster for the utilization of urea and a gene encoding cyanase suggest that comammox may use diverse organic nitrogen compounds in addition to free ammonia as the substrates. The comammox organisms also encoded the genomic potential for multiple alternative energy metabolisms, including respiration with hydrogen, formate, and sulfite as electron donors. Pathways for the biosynthesis and degradation of polyphosphate, glycogen, and polyhydroxyalkanoates as intracellular storage compounds likely help comammox survive unfavorable conditions and facilitate switches between lifestyles in fluctuating environments. One of the comammox strains acquired from the anaerobic tank encoded and transcribed genes involved in homoacetate fermentation or in the utilization of exogenous acetate, both pathways being unexpected in a nitrifying bacterium. Surprisingly, this strain also encoded a respiratory nitrate reductase which has not yet been found in any other Nitrospira genome and might confer a selective advantage to this strain over other Nitrospira strains in anoxic conditions. IMPORTANCE The discovery of comammox in the genus Nitrospira changes our perception of nitrification. However, genomes of comammox organisms have not been acquired from full-scale WWTPs, and very little is known about their survival strategies and potential metabolisms in complex wastewater treatment systems. Here, four comammox metagenome-assembled genomes and metatranscriptomic data sets were retrieved from two full-scale WWTPs. Their impressive and—among nitrifiers—unsurpassed ecophysiological versatility could make comammox Nitrospira an interesting target for optimizing nitrification in current and future bioreactor configurations. |
| first_indexed | 2024-12-19T20:13:22Z |
| format | Article |
| id | doaj.art-e829222d367a4825939c652d8a1bf670 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-19T20:13:22Z |
| publishDate | 2020-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-e829222d367a4825939c652d8a1bf6702022-12-21T20:07:15ZengAmerican Society for MicrobiologymBio2150-75112020-04-0111210.1128/mBio.03175-19Activity and Metabolic Versatility of Complete Ammonia Oxidizers in Full-Scale Wastewater Treatment SystemsYuchun Yang0Holger Daims1Yang Liu2Craig W. Herbold3Petra Pjevac4Jih-Gaw Lin5Meng Li6Ji-Dong Gu7Laboratory of Environmental Microbiology and Toxicology, School of Biological Sciences, The University of Hong Kong, Hong Kong SAR, Hong Kong, People’s Republic of ChinaUniversity of Vienna, Centre for Microbiology and Environmental Systems Science, Division of Microbial Ecology, Vienna, AustriaShenzhen Key Laboratory of Marine Microbiome Engineering, Institute for Advanced Study, Shenzhen University, Shenzhen, People’s Republic of ChinaUniversity of Vienna, Centre for Microbiology and Environmental Systems Science, Division of Microbial Ecology, Vienna, AustriaUniversity of Vienna, Centre for Microbiology and Environmental Systems Science, Division of Microbial Ecology, Vienna, AustriaInstitute of Environmental Engineering, National Chiao Tung University, Hsinchu City, TaiwanShenzhen Key Laboratory of Marine Microbiome Engineering, Institute for Advanced Study, Shenzhen University, Shenzhen, People’s Republic of ChinaLaboratory of Environmental Microbiology and Toxicology, School of Biological Sciences, The University of Hong Kong, Hong Kong SAR, Hong Kong, People’s Republic of ChinaABSTRACT The recent discovery of complete ammonia oxidizers (comammox) contradicts the paradigm that chemolithoautotrophic nitrification is always catalyzed by two different microorganisms. However, our knowledge of the survival strategies of comammox in complex ecosystems, such as full-scale wastewater treatment plants (WWTPs), remains limited. Analyses of genomes and in situ transcriptomes of four comammox organisms from two full-scale WWTPs revealed that comammox were active and showed a surprisingly high metabolic versatility. A gene cluster for the utilization of urea and a gene encoding cyanase suggest that comammox may use diverse organic nitrogen compounds in addition to free ammonia as the substrates. The comammox organisms also encoded the genomic potential for multiple alternative energy metabolisms, including respiration with hydrogen, formate, and sulfite as electron donors. Pathways for the biosynthesis and degradation of polyphosphate, glycogen, and polyhydroxyalkanoates as intracellular storage compounds likely help comammox survive unfavorable conditions and facilitate switches between lifestyles in fluctuating environments. One of the comammox strains acquired from the anaerobic tank encoded and transcribed genes involved in homoacetate fermentation or in the utilization of exogenous acetate, both pathways being unexpected in a nitrifying bacterium. Surprisingly, this strain also encoded a respiratory nitrate reductase which has not yet been found in any other Nitrospira genome and might confer a selective advantage to this strain over other Nitrospira strains in anoxic conditions. IMPORTANCE The discovery of comammox in the genus Nitrospira changes our perception of nitrification. However, genomes of comammox organisms have not been acquired from full-scale WWTPs, and very little is known about their survival strategies and potential metabolisms in complex wastewater treatment systems. Here, four comammox metagenome-assembled genomes and metatranscriptomic data sets were retrieved from two full-scale WWTPs. Their impressive and—among nitrifiers—unsurpassed ecophysiological versatility could make comammox Nitrospira an interesting target for optimizing nitrification in current and future bioreactor configurations.https://journals.asm.org/doi/10.1128/mBio.03175-19comammox Nitrospiracyanasefull-scale WWTPshomoacetate fermentationmetabolic versatility |
| spellingShingle | Yuchun Yang Holger Daims Yang Liu Craig W. Herbold Petra Pjevac Jih-Gaw Lin Meng Li Ji-Dong Gu Activity and Metabolic Versatility of Complete Ammonia Oxidizers in Full-Scale Wastewater Treatment Systems mBio comammox Nitrospira cyanase full-scale WWTPs homoacetate fermentation metabolic versatility |
| title | Activity and Metabolic Versatility of Complete Ammonia Oxidizers in Full-Scale Wastewater Treatment Systems |
| title_full | Activity and Metabolic Versatility of Complete Ammonia Oxidizers in Full-Scale Wastewater Treatment Systems |
| title_fullStr | Activity and Metabolic Versatility of Complete Ammonia Oxidizers in Full-Scale Wastewater Treatment Systems |
| title_full_unstemmed | Activity and Metabolic Versatility of Complete Ammonia Oxidizers in Full-Scale Wastewater Treatment Systems |
| title_short | Activity and Metabolic Versatility of Complete Ammonia Oxidizers in Full-Scale Wastewater Treatment Systems |
| title_sort | activity and metabolic versatility of complete ammonia oxidizers in full scale wastewater treatment systems |
| topic | comammox Nitrospira cyanase full-scale WWTPs homoacetate fermentation metabolic versatility |
| url | https://journals.asm.org/doi/10.1128/mBio.03175-19 |
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