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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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Autores principales: Melcher, Michael, Hodgskiss, Logan H., Mardini, Mohammad Anas, Schleper, Christa, Rittmann, Simon K.-M. R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9978112/
https://www.ncbi.nlm.nih.gov/pubmed/36876066
http://dx.doi.org/10.3389/fmicb.2023.1076342
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author Melcher, Michael
Hodgskiss, Logan H.
Mardini, Mohammad Anas
Schleper, Christa
Rittmann, Simon K.-M. R.
author_facet Melcher, Michael
Hodgskiss, Logan H.
Mardini, Mohammad Anas
Schleper, Christa
Rittmann, Simon K.-M. R.
author_sort Melcher, Michael
collection PubMed
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 (CO(2)) concentrations aiming to understand the interplay between ammonia oxidation and CO(2) 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 CO(2) 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 μ(max)) 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 D(crit). 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 μ(max). Furthermore, the obscure nature of the archaeal ammonia oxidation prevents an interpretation in the context of Monod kinetics and thus the determination of K(S). 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 pubmed-99781122023-03-03 Analysis of biomass productivity and physiology of Nitrososphaera viennensis grown in continuous culture Melcher, Michael Hodgskiss, Logan H. Mardini, Mohammad Anas Schleper, Christa Rittmann, Simon K.-M. R. Front Microbiol Microbiology 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 (CO(2)) concentrations aiming to understand the interplay between ammonia oxidation and CO(2) 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 CO(2) 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 μ(max)) 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 D(crit). 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 μ(max). Furthermore, the obscure nature of the archaeal ammonia oxidation prevents an interpretation in the context of Monod kinetics and thus the determination of K(S). 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. Frontiers Media S.A. 2023-02-16 /pmc/articles/PMC9978112/ /pubmed/36876066 http://dx.doi.org/10.3389/fmicb.2023.1076342 Text en Copyright © 2023 Melcher, Hodgskiss, Mardini, Schleper and Rittmann. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Melcher, Michael
Hodgskiss, Logan H.
Mardini, Mohammad Anas
Schleper, Christa
Rittmann, Simon K.-M. R.
Analysis of biomass productivity and physiology of Nitrososphaera viennensis grown in continuous culture
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 Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9978112/
https://www.ncbi.nlm.nih.gov/pubmed/36876066
http://dx.doi.org/10.3389/fmicb.2023.1076342
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