Activity and metabolic versatility of complete ammonia oxidizers in full-scale wastewater treatment systems

Yuchun Yang; Holger Daims; Yang Liu; Craig W. Herbold; Petra Pjevac; Jih Gaw Lin; Meng Li; Ji Dong Gu

doi:10.1128/mBio.03175-19

Activity and metabolic versatility of complete ammonia oxidizers in full-scale wastewater treatment systems

Yuchun Yang, Holger Daims, Yang Liu, Craig W. Herbold, Petra Pjevac, Jih Gaw Lin, Meng Li, Ji Dong Gu^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

65 Scopus citations

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 ecophysi-ological versatility could make comammox Nitrospira an interesting target for optimizing nitrification in current and future bioreactor configurations.

Original language	English
Article number	e03175-19
Journal	mBio
Volume	11
Issue number	2
DOIs	https://doi.org/10.1128/mBio.03175-19
State	Published - 2020
Externally published	Yes

Keywords

Comammox nitrospira
Cyanase
Full-scale WWTPs
Homoacetate fermentation
Metabolic versatility

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10.1128/mBio.03175-19

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title = "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 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 ecophysi-ological versatility could make comammox Nitrospira an interesting target for optimizing nitrification in current and future bioreactor configurations.",

keywords = "Comammox nitrospira, Cyanase, Full-scale WWTPs, Homoacetate fermentation, Metabolic versatility",

author = "Yuchun Yang and Holger Daims and Yang Liu and Herbold, {Craig W.} and Petra Pjevac and Lin, {Jih Gaw} and Meng Li and Gu, {Ji Dong}",

note = "Publisher Copyright: {\textcopyright} 2020 Yang et al.",

year = "2020",

doi = "10.1128/mBio.03175-19",

language = "英语",

volume = "11",

journal = "mBio",

issn = "2161-2129",

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T1 - Activity and metabolic versatility of complete ammonia oxidizers in full-scale wastewater treatment systems

AU - Yang, Yuchun

AU - Daims, Holger

AU - Liu, Yang

AU - Herbold, Craig W.

AU - Pjevac, Petra

AU - Lin, Jih Gaw

AU - Li, Meng

AU - Gu, Ji Dong

PY - 2020

Y1 - 2020

N2 - 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 ecophysi-ological versatility could make comammox Nitrospira an interesting target for optimizing nitrification in current and future bioreactor configurations.

AB - 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 ecophysi-ological versatility could make comammox Nitrospira an interesting target for optimizing nitrification in current and future bioreactor configurations.

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KW - Cyanase

KW - Full-scale WWTPs

KW - Homoacetate fermentation

KW - Metabolic versatility

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DO - 10.1128/mBio.03175-19

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AN - SCOPUS:85082019209

SN - 2161-2129

VL - 11

JO - mBio

JF - mBio

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M1 - e03175-19

ER -

Activity and metabolic versatility of complete ammonia oxidizers in full-scale wastewater treatment systems

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Keywords

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