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...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Yuchun Yang, Holger Daims, Yang Liu, Craig W. Herbold, Petra Pjevac, Jih-Gaw Lin, Meng Li, Ji-Dong Gu
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2020
Materias:
Acceso en línea:https://doaj.org/article/e829222d367a4825939c652d8a1bf670
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:e829222d367a4825939c652d8a1bf670
record_format dspace
spelling oai:doaj.org-article:e829222d367a4825939c652d8a1bf6702021-11-15T15:57:03ZActivity and Metabolic Versatility of Complete Ammonia Oxidizers in Full-Scale Wastewater Treatment Systems10.1128/mBio.03175-192150-7511https://doaj.org/article/e829222d367a4825939c652d8a1bf6702020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.03175-19https://doaj.org/toc/2150-7511ABSTRACT 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.Yuchun YangHolger DaimsYang LiuCraig W. HerboldPetra PjevacJih-Gaw LinMeng LiJi-Dong GuAmerican Society for Microbiologyarticlecomammox Nitrospiracyanasefull-scale WWTPshomoacetate fermentationmetabolic versatilityMicrobiologyQR1-502ENmBio, Vol 11, Iss 2 (2020)
institution DOAJ
collection DOAJ
language EN
topic comammox Nitrospira
cyanase
full-scale WWTPs
homoacetate fermentation
metabolic versatility
Microbiology
QR1-502
spellingShingle comammox Nitrospira
cyanase
full-scale WWTPs
homoacetate fermentation
metabolic versatility
Microbiology
QR1-502
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
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.
format article
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
title 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_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_sort activity and metabolic versatility of complete ammonia oxidizers in full-scale wastewater treatment systems
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/e829222d367a4825939c652d8a1bf670
work_keys_str_mv AT yuchunyang activityandmetabolicversatilityofcompleteammoniaoxidizersinfullscalewastewatertreatmentsystems
AT holgerdaims activityandmetabolicversatilityofcompleteammoniaoxidizersinfullscalewastewatertreatmentsystems
AT yangliu activityandmetabolicversatilityofcompleteammoniaoxidizersinfullscalewastewatertreatmentsystems
AT craigwherbold activityandmetabolicversatilityofcompleteammoniaoxidizersinfullscalewastewatertreatmentsystems
AT petrapjevac activityandmetabolicversatilityofcompleteammoniaoxidizersinfullscalewastewatertreatmentsystems
AT jihgawlin activityandmetabolicversatilityofcompleteammoniaoxidizersinfullscalewastewatertreatmentsystems
AT mengli activityandmetabolicversatilityofcompleteammoniaoxidizersinfullscalewastewatertreatmentsystems
AT jidonggu activityandmetabolicversatilityofcompleteammoniaoxidizersinfullscalewastewatertreatmentsystems
_version_ 1718427062367158272