Proteomic Response of Three Marine Ammonia-Oxidizing Archaea to Hydrogen Peroxide and Their Metabolic Interactions with a Heterotrophic Alphaproteobacterium

ABSTRACT Ammonia-oxidizing archaea (AOA) play an important role in the nitrogen cycle and account for a considerable fraction of the prokaryotic plankton in the ocean. Most AOA lack the hydrogen peroxide (H2O2)-detoxifying enzyme catalase, and some AOA have been shown to grow poorly under conditions...

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Autores principales:	Barbara Bayer, Claus Pelikan, Meriel J. Bittner, Thomas Reinthaler, Martin Könneke, Gerhard J. Herndl, Pierre Offre
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Nitrosopumilus ammonia-oxidizing archaea hydrogen peroxide metabolic interactions oxidative stress proteomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8b5948d26fab4715ae6689eb0cd2cd6e
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spelling	oai:doaj.org-article:8b5948d26fab4715ae6689eb0cd2cd6e2021-12-02T19:46:18ZProteomic Response of Three Marine Ammonia-Oxidizing Archaea to Hydrogen Peroxide and Their Metabolic Interactions with a Heterotrophic Alphaproteobacterium10.1128/mSystems.00181-192379-5077https://doaj.org/article/8b5948d26fab4715ae6689eb0cd2cd6e2019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00181-19https://doaj.org/toc/2379-5077ABSTRACT Ammonia-oxidizing archaea (AOA) play an important role in the nitrogen cycle and account for a considerable fraction of the prokaryotic plankton in the ocean. Most AOA lack the hydrogen peroxide (H2O2)-detoxifying enzyme catalase, and some AOA have been shown to grow poorly under conditions of exposure to H2O2. However, differences in the degrees of H2O2 sensitivity of different AOA strains, the physiological status of AOA cells exposed to H2O2, and their molecular response to H2O2 remain poorly characterized. Further, AOA might rely on heterotrophic bacteria to detoxify H2O2, and yet the extent and variety of costs and benefits involved in these interactions remain unclear. Here, we used a proteomics approach to compare the protein profiles of three Nitrosopumilus strains grown in the presence and absence of catalase and in coculture with the heterotrophic alphaproteobacterium Oceanicaulis alexandrii. We observed that most proteins detected at a higher relative abundance in H2O2-exposed Nitrosopumilus cells had no known function in oxidative stress defense. Instead, these proteins were putatively involved in the remodeling of the extracellular matrix, which we hypothesize to be a strategy limiting the influx of H2O2 into the cells. Using RNA-stable isotope probing, we confirmed that O. alexandrii cells growing in coculture with the Nitrosopumilus strains assimilated Nitrosopumilus-derived organic carbon, suggesting that AOA could recruit H2O2-detoxifying bacteria through the release of labile organic matter. Our results contribute new insights into the response of AOA to H2O2 and highlight the potential ecological importance of their interactions with heterotrophic free-living bacteria in marine environments. IMPORTANCE Ammonia-oxidizing archaea (AOA) are the most abundant chemolithoautotrophic microorganisms in the oxygenated water column of the global ocean. Although H2O2 appears to be a universal by-product of aerobic metabolism, genes encoding the hydrogen peroxide (H2O2)-detoxifying enzyme catalase are largely absent in genomes of marine AOA. Here, we provide evidence that closely related marine AOA have different degrees of sensitivity to H2O2, which may contribute to niche differentiation between these organisms. Furthermore, our results suggest that marine AOA rely on H2O2 detoxification during periods of high metabolic activity and release organic compounds, thereby potentially attracting heterotrophic prokaryotes that provide this missing function. In summary, this report provides insights into the metabolic interactions between AOA and heterotrophic bacteria in marine environments and suggests that AOA play an important role in the biogeochemical carbon cycle by making organic carbon available for heterotrophic microorganisms.Barbara BayerClaus PelikanMeriel J. BittnerThomas ReinthalerMartin KönnekeGerhard J. HerndlPierre OffreAmerican Society for MicrobiologyarticleNitrosopumilusammonia-oxidizing archaeahydrogen peroxidemetabolic interactionsoxidative stressproteomicsMicrobiologyQR1-502ENmSystems, Vol 4, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Nitrosopumilus ammonia-oxidizing archaea hydrogen peroxide metabolic interactions oxidative stress proteomics Microbiology QR1-502
spellingShingle	Nitrosopumilus ammonia-oxidizing archaea hydrogen peroxide metabolic interactions oxidative stress proteomics Microbiology QR1-502 Barbara Bayer Claus Pelikan Meriel J. Bittner Thomas Reinthaler Martin Könneke Gerhard J. Herndl Pierre Offre Proteomic Response of Three Marine Ammonia-Oxidizing Archaea to Hydrogen Peroxide and Their Metabolic Interactions with a Heterotrophic Alphaproteobacterium
description	ABSTRACT Ammonia-oxidizing archaea (AOA) play an important role in the nitrogen cycle and account for a considerable fraction of the prokaryotic plankton in the ocean. Most AOA lack the hydrogen peroxide (H2O2)-detoxifying enzyme catalase, and some AOA have been shown to grow poorly under conditions of exposure to H2O2. However, differences in the degrees of H2O2 sensitivity of different AOA strains, the physiological status of AOA cells exposed to H2O2, and their molecular response to H2O2 remain poorly characterized. Further, AOA might rely on heterotrophic bacteria to detoxify H2O2, and yet the extent and variety of costs and benefits involved in these interactions remain unclear. Here, we used a proteomics approach to compare the protein profiles of three Nitrosopumilus strains grown in the presence and absence of catalase and in coculture with the heterotrophic alphaproteobacterium Oceanicaulis alexandrii. We observed that most proteins detected at a higher relative abundance in H2O2-exposed Nitrosopumilus cells had no known function in oxidative stress defense. Instead, these proteins were putatively involved in the remodeling of the extracellular matrix, which we hypothesize to be a strategy limiting the influx of H2O2 into the cells. Using RNA-stable isotope probing, we confirmed that O. alexandrii cells growing in coculture with the Nitrosopumilus strains assimilated Nitrosopumilus-derived organic carbon, suggesting that AOA could recruit H2O2-detoxifying bacteria through the release of labile organic matter. Our results contribute new insights into the response of AOA to H2O2 and highlight the potential ecological importance of their interactions with heterotrophic free-living bacteria in marine environments. IMPORTANCE Ammonia-oxidizing archaea (AOA) are the most abundant chemolithoautotrophic microorganisms in the oxygenated water column of the global ocean. Although H2O2 appears to be a universal by-product of aerobic metabolism, genes encoding the hydrogen peroxide (H2O2)-detoxifying enzyme catalase are largely absent in genomes of marine AOA. Here, we provide evidence that closely related marine AOA have different degrees of sensitivity to H2O2, which may contribute to niche differentiation between these organisms. Furthermore, our results suggest that marine AOA rely on H2O2 detoxification during periods of high metabolic activity and release organic compounds, thereby potentially attracting heterotrophic prokaryotes that provide this missing function. In summary, this report provides insights into the metabolic interactions between AOA and heterotrophic bacteria in marine environments and suggests that AOA play an important role in the biogeochemical carbon cycle by making organic carbon available for heterotrophic microorganisms.
format	article
author	Barbara Bayer Claus Pelikan Meriel J. Bittner Thomas Reinthaler Martin Könneke Gerhard J. Herndl Pierre Offre
author_facet	Barbara Bayer Claus Pelikan Meriel J. Bittner Thomas Reinthaler Martin Könneke Gerhard J. Herndl Pierre Offre
author_sort	Barbara Bayer
title	Proteomic Response of Three Marine Ammonia-Oxidizing Archaea to Hydrogen Peroxide and Their Metabolic Interactions with a Heterotrophic Alphaproteobacterium
title_short	Proteomic Response of Three Marine Ammonia-Oxidizing Archaea to Hydrogen Peroxide and Their Metabolic Interactions with a Heterotrophic Alphaproteobacterium
title_full	Proteomic Response of Three Marine Ammonia-Oxidizing Archaea to Hydrogen Peroxide and Their Metabolic Interactions with a Heterotrophic Alphaproteobacterium
title_fullStr	Proteomic Response of Three Marine Ammonia-Oxidizing Archaea to Hydrogen Peroxide and Their Metabolic Interactions with a Heterotrophic Alphaproteobacterium
title_full_unstemmed	Proteomic Response of Three Marine Ammonia-Oxidizing Archaea to Hydrogen Peroxide and Their Metabolic Interactions with a Heterotrophic Alphaproteobacterium
title_sort	proteomic response of three marine ammonia-oxidizing archaea to hydrogen peroxide and their metabolic interactions with a heterotrophic alphaproteobacterium
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/8b5948d26fab4715ae6689eb0cd2cd6e
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Proteomic Response of Three Marine Ammonia-Oxidizing Archaea to Hydrogen Peroxide and Their Metabolic Interactions with a Heterotrophic Alphaproteobacterium

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