Formate Utilization by the Crenarchaeon <i>Desulfurococcus amylolyticus</i>

Formate is one of the key compounds of the microbial carbon and/or energy metabolism. It owes a significant contribution to various anaerobic syntrophic associations, and may become one of the energy storage compounds of modern energy biotechnology. Microbial growth on formate was demonstrated for d...

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Main Authors: Ipek Ergal, Barbara Reischl, Benedikt Hasibar, Lokeshwaran Manoharan, Aaron Zipperle, Günther Bochmann, Werner Fuchs, Simon K.-M. R. Rittmann
Format: Article
Language:English
Published: MDPI AG 2020-03-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/8/3/454
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spelling doaj-7a98541aaedf4863ad5a8007beda924a2020-11-25T01:28:23ZengMDPI AGMicroorganisms2076-26072020-03-018345410.3390/microorganisms8030454microorganisms8030454Formate Utilization by the Crenarchaeon <i>Desulfurococcus amylolyticus</i>Ipek Ergal0Barbara Reischl1Benedikt Hasibar2Lokeshwaran Manoharan3Aaron Zipperle4Günther Bochmann5Werner Fuchs6Simon K.-M. R. Rittmann7Archaea Physiology &amp; Biotechnology Group, Department of Functional and Evolutionary Ecology, Universität Wien, 1090 Wien, AustriaArchaea Physiology &amp; Biotechnology Group, Department of Functional and Evolutionary Ecology, Universität Wien, 1090 Wien, AustriaDepartment IFA Tulln, Institute for Environmental Biotechnology, University of Natural Resources and Life Sciences, 1180 Wien, AustriaArchaea Physiology &amp; Biotechnology Group, Department of Functional and Evolutionary Ecology, Universität Wien, 1090 Wien, AustriaArchaea Physiology &amp; Biotechnology Group, Department of Functional and Evolutionary Ecology, Universität Wien, 1090 Wien, AustriaDepartment IFA Tulln, Institute for Environmental Biotechnology, University of Natural Resources and Life Sciences, 1180 Wien, AustriaDepartment IFA Tulln, Institute for Environmental Biotechnology, University of Natural Resources and Life Sciences, 1180 Wien, AustriaArchaea Physiology &amp; Biotechnology Group, Department of Functional and Evolutionary Ecology, Universität Wien, 1090 Wien, AustriaFormate is one of the key compounds of the microbial carbon and/or energy metabolism. It owes a significant contribution to various anaerobic syntrophic associations, and may become one of the energy storage compounds of modern energy biotechnology. Microbial growth on formate was demonstrated for different bacteria and archaea, but not yet for species of the archaeal phylum Crenarchaeota. Here, we show that <i>Desulfurococcus amylolyticus</i> DSM 16532, an anaerobic and hyperthermophilic Crenarchaeon, metabolises formate without the production of molecular hydrogen. Growth, substrate uptake, and production kinetics on formate, glucose, and glucose/formate mixtures exhibited similar specific growth rates and similar final cell densities. A whole cell conversion experiment on formate revealed that <i>D. amylolyticus</i> converts formate into carbon dioxide, acetate, citrate, and ethanol. Using bioinformatic analysis, we examined whether one of the currently known and postulated formate utilisation pathways could be operative in <i>D. amylolyticus</i>. This analysis indicated the possibility that <i>D. amylolyticus</i> uses formaldehyde producing enzymes for the assimilation of formate. Therefore, we propose that formate might be assimilated into biomass through formaldehyde dehydrogenase and the oxidative pentose phosphate pathway. These findings shed new light on the metabolic versatility of the archaeal phylum Crenarchaeota.https://www.mdpi.com/2076-2607/8/3/454archaeacrenarchaeotaanaerobemicrobial physiologymetabolismone-carbonformaldehyde
collection DOAJ
language English
format Article
sources DOAJ
author Ipek Ergal
Barbara Reischl
Benedikt Hasibar
Lokeshwaran Manoharan
Aaron Zipperle
Günther Bochmann
Werner Fuchs
Simon K.-M. R. Rittmann
spellingShingle Ipek Ergal
Barbara Reischl
Benedikt Hasibar
Lokeshwaran Manoharan
Aaron Zipperle
Günther Bochmann
Werner Fuchs
Simon K.-M. R. Rittmann
Formate Utilization by the Crenarchaeon <i>Desulfurococcus amylolyticus</i>
Microorganisms
archaea
crenarchaeota
anaerobe
microbial physiology
metabolism
one-carbon
formaldehyde
author_facet Ipek Ergal
Barbara Reischl
Benedikt Hasibar
Lokeshwaran Manoharan
Aaron Zipperle
Günther Bochmann
Werner Fuchs
Simon K.-M. R. Rittmann
author_sort Ipek Ergal
title Formate Utilization by the Crenarchaeon <i>Desulfurococcus amylolyticus</i>
title_short Formate Utilization by the Crenarchaeon <i>Desulfurococcus amylolyticus</i>
title_full Formate Utilization by the Crenarchaeon <i>Desulfurococcus amylolyticus</i>
title_fullStr Formate Utilization by the Crenarchaeon <i>Desulfurococcus amylolyticus</i>
title_full_unstemmed Formate Utilization by the Crenarchaeon <i>Desulfurococcus amylolyticus</i>
title_sort formate utilization by the crenarchaeon <i>desulfurococcus amylolyticus</i>
publisher MDPI AG
series Microorganisms
issn 2076-2607
publishDate 2020-03-01
description Formate is one of the key compounds of the microbial carbon and/or energy metabolism. It owes a significant contribution to various anaerobic syntrophic associations, and may become one of the energy storage compounds of modern energy biotechnology. Microbial growth on formate was demonstrated for different bacteria and archaea, but not yet for species of the archaeal phylum Crenarchaeota. Here, we show that <i>Desulfurococcus amylolyticus</i> DSM 16532, an anaerobic and hyperthermophilic Crenarchaeon, metabolises formate without the production of molecular hydrogen. Growth, substrate uptake, and production kinetics on formate, glucose, and glucose/formate mixtures exhibited similar specific growth rates and similar final cell densities. A whole cell conversion experiment on formate revealed that <i>D. amylolyticus</i> converts formate into carbon dioxide, acetate, citrate, and ethanol. Using bioinformatic analysis, we examined whether one of the currently known and postulated formate utilisation pathways could be operative in <i>D. amylolyticus</i>. This analysis indicated the possibility that <i>D. amylolyticus</i> uses formaldehyde producing enzymes for the assimilation of formate. Therefore, we propose that formate might be assimilated into biomass through formaldehyde dehydrogenase and the oxidative pentose phosphate pathway. These findings shed new light on the metabolic versatility of the archaeal phylum Crenarchaeota.
topic archaea
crenarchaeota
anaerobe
microbial physiology
metabolism
one-carbon
formaldehyde
url https://www.mdpi.com/2076-2607/8/3/454
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