Analysis of biomass productivity and physiology of Nitrososphaera viennensis grown in continuous culture

Microbial ammonia oxidation is the first and usually rate limiting step in nitrification and is therefore an important step in the global nitrogen cycle. Ammonia-oxidizing archaea (AOA) play an important role in nitrification. Here, we report a comprehensive analysis of biomass productivity and the...

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Main Authors: Michael Melcher, Logan H. Hodgskiss, Mohammad Anas Mardini, Christa Schleper, Simon K.-M. R. Rittmann
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1076342/full
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author Michael Melcher
Logan H. Hodgskiss
Mohammad Anas Mardini
Christa Schleper
Simon K.-M. R. Rittmann
Simon K.-M. R. Rittmann
Simon K.-M. R. Rittmann
author_facet Michael Melcher
Logan H. Hodgskiss
Mohammad Anas Mardini
Christa Schleper
Simon K.-M. R. Rittmann
Simon K.-M. R. Rittmann
Simon K.-M. R. Rittmann
author_sort Michael Melcher
collection DOAJ
description Microbial ammonia oxidation is the first and usually rate limiting step in nitrification and is therefore an important step in the global nitrogen cycle. Ammonia-oxidizing archaea (AOA) play an important role in nitrification. Here, we report a comprehensive analysis of biomass productivity and the physiological response of Nitrososphaera viennensis to different ammonium and carbon dioxide (CO2) concentrations aiming to understand the interplay between ammonia oxidation and CO2 fixation of N. viennensis. The experiments were performed in closed batch in serum bottles as well as in batch, fed-batch, and continuous culture in bioreactors. A reduced specific growth rate (μ) of N. viennensis was observed in batch systems in bioreactors. By increasing CO2 gassing μ could be increased to rates comparable to that of closed batch systems. Furthermore, at a high dilution rate (D) in continuous culture (≥ 0.7 of μmax) the biomass to ammonium yield (Y(X/NH3)) increased up to 81.7% compared to batch cultures. In continuous culture, biofilm formation at higher D prevented the determination of Dcrit. Due to changes in Y(X/NH3) and due to biofilm, nitrite concentration becomes an unreliable proxy for the cell number in continuous cultures at D towards μmax. Furthermore, the obscure nature of the archaeal ammonia oxidation prevents an interpretation in the context of Monod kinetics and thus the determination of KS. Our findings indicate that the physiological response of N. viennensis might be regulated with different enzymatic make-ups, according to the ammonium catalysis rate. We reveal novel insights into the physiology of N. viennensis that are important for biomass production and the biomass yield of AOA. Moreover, our study has implications to the field of archaea biology and microbial ecology by showing that bioprocess technology and quantitative analysis can be applied to decipher environmental factors affecting the physiology and productivity of AOA.
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spelling doaj.art-6d050059bb694df6a8083dcb9088b2af2023-02-16T07:47:20ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-02-011410.3389/fmicb.2023.10763421076342Analysis of biomass productivity and physiology of Nitrososphaera viennensis grown in continuous cultureMichael Melcher0Logan H. Hodgskiss1Mohammad Anas Mardini2Christa Schleper3Simon K.-M. R. Rittmann4Simon K.-M. R. Rittmann5Simon K.-M. R. Rittmann6Archaea Biology and Ecogenomics Division, Department of Functional and Evolutionary Ecology, University of Vienna, Vienna, AustriaArchaea Biology and Ecogenomics Division, Department of Functional and Evolutionary Ecology, University of Vienna, Vienna, AustriaArchaea Biology and Ecogenomics Division, Department of Functional and Evolutionary Ecology, University of Vienna, Vienna, AustriaArchaea Biology and Ecogenomics Division, Department of Functional and Evolutionary Ecology, University of Vienna, Vienna, AustriaArchaea Biology and Ecogenomics Division, Department of Functional and Evolutionary Ecology, University of Vienna, Vienna, AustriaArkeon GmbH, Tulln a.d. Donau, AustriaArchaea Physiology & Biotechnology Group, Department of Functional and Evolutionary Ecology, University of Vienna, Vienna, AustriaMicrobial ammonia oxidation is the first and usually rate limiting step in nitrification and is therefore an important step in the global nitrogen cycle. Ammonia-oxidizing archaea (AOA) play an important role in nitrification. Here, we report a comprehensive analysis of biomass productivity and the physiological response of Nitrososphaera viennensis to different ammonium and carbon dioxide (CO2) concentrations aiming to understand the interplay between ammonia oxidation and CO2 fixation of N. viennensis. The experiments were performed in closed batch in serum bottles as well as in batch, fed-batch, and continuous culture in bioreactors. A reduced specific growth rate (μ) of N. viennensis was observed in batch systems in bioreactors. By increasing CO2 gassing μ could be increased to rates comparable to that of closed batch systems. Furthermore, at a high dilution rate (D) in continuous culture (≥ 0.7 of μmax) the biomass to ammonium yield (Y(X/NH3)) increased up to 81.7% compared to batch cultures. In continuous culture, biofilm formation at higher D prevented the determination of Dcrit. Due to changes in Y(X/NH3) and due to biofilm, nitrite concentration becomes an unreliable proxy for the cell number in continuous cultures at D towards μmax. Furthermore, the obscure nature of the archaeal ammonia oxidation prevents an interpretation in the context of Monod kinetics and thus the determination of KS. Our findings indicate that the physiological response of N. viennensis might be regulated with different enzymatic make-ups, according to the ammonium catalysis rate. We reveal novel insights into the physiology of N. viennensis that are important for biomass production and the biomass yield of AOA. Moreover, our study has implications to the field of archaea biology and microbial ecology by showing that bioprocess technology and quantitative analysis can be applied to decipher environmental factors affecting the physiology and productivity of AOA.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1076342/fullarchaeabioreactorclosed batchbatchfed-batchchemostat
spellingShingle Michael Melcher
Logan H. Hodgskiss
Mohammad Anas Mardini
Christa Schleper
Simon K.-M. R. Rittmann
Simon K.-M. R. Rittmann
Simon K.-M. R. Rittmann
Analysis of biomass productivity and physiology of Nitrososphaera viennensis grown in continuous culture
Frontiers in Microbiology
archaea
bioreactor
closed batch
batch
fed-batch
chemostat
title Analysis of biomass productivity and physiology of Nitrososphaera viennensis grown in continuous culture
title_full Analysis of biomass productivity and physiology of Nitrososphaera viennensis grown in continuous culture
title_fullStr Analysis of biomass productivity and physiology of Nitrososphaera viennensis grown in continuous culture
title_full_unstemmed Analysis of biomass productivity and physiology of Nitrososphaera viennensis grown in continuous culture
title_short Analysis of biomass productivity and physiology of Nitrososphaera viennensis grown in continuous culture
title_sort analysis of biomass productivity and physiology of nitrososphaera viennensis grown in continuous culture
topic archaea
bioreactor
closed batch
batch
fed-batch
chemostat
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1076342/full
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