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Cultivation and Genomic Analysis of “Candidatus Nitrosocaldus islandicus,” an Obligately Thermophilic, Ammonia-Oxidizing Thaumarchaeon from a Hot Spring Biofilm in Graendalur Valley, Iceland

Ammonia-oxidizing archaea (AOA) within the phylum Thaumarchaeota are the only known aerobic ammonia oxidizers in geothermal environments. Although molecular data indicate the presence of phylogenetically diverse AOA from the Nitrosocaldus clade, group 1.1b and group 1.1a Thaumarchaeota in terrestria...

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Autores principales: Daebeler, Anne, Herbold, Craig W., Vierheilig, Julia, Sedlacek, Christopher J., Pjevac, Petra, Albertsen, Mads, Kirkegaard, Rasmus H., de la Torre, José R., Daims, Holger, Wagner, Michael
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5817080/
https://www.ncbi.nlm.nih.gov/pubmed/29491853
http://dx.doi.org/10.3389/fmicb.2018.00193
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author Daebeler, Anne
Herbold, Craig W.
Vierheilig, Julia
Sedlacek, Christopher J.
Pjevac, Petra
Albertsen, Mads
Kirkegaard, Rasmus H.
de la Torre, José R.
Daims, Holger
Wagner, Michael
author_facet Daebeler, Anne
Herbold, Craig W.
Vierheilig, Julia
Sedlacek, Christopher J.
Pjevac, Petra
Albertsen, Mads
Kirkegaard, Rasmus H.
de la Torre, José R.
Daims, Holger
Wagner, Michael
author_sort Daebeler, Anne
collection PubMed
description Ammonia-oxidizing archaea (AOA) within the phylum Thaumarchaeota are the only known aerobic ammonia oxidizers in geothermal environments. Although molecular data indicate the presence of phylogenetically diverse AOA from the Nitrosocaldus clade, group 1.1b and group 1.1a Thaumarchaeota in terrestrial high-temperature habitats, only one() enrichment culture of an AOA thriving above 50°C has been reported and functionally analyzed. In this study, we physiologically and genomically characterized a newly discovered thaumarchaeon from the deep-branching Nitrosocaldaceae family of which we have obtained a high (∼85%) enrichment from biofilm of an Icelandic hot spring (73°C). This AOA, which we provisionally refer to as “Candidatus Nitrosocaldus islandicus,” is an obligately thermophilic, aerobic chemolithoautotrophic ammonia oxidizer, which stoichiometrically converts ammonia to nitrite at temperatures between 50 and 70°C. “Ca. N. islandicus” encodes the expected repertoire of enzymes proposed to be required for archaeal ammonia oxidation, but unexpectedly lacks a nirK gene and also possesses no identifiable other enzyme for nitric oxide (NO) generation(). Nevertheless, ammonia oxidation by this AOA appears to be NO-dependent as “Ca. N. islandicus” is, like all other tested AOA, inhibited by the addition of an NO scavenger. Furthermore, comparative genomics revealed that “Ca. N. islandicus” has the potential for aromatic amino acid fermentation as its genome encodes an indolepyruvate oxidoreductase (iorAB) as well as a type 3b hydrogenase, which are not present in any other sequenced AOA. A further surprising genomic feature of this thermophilic ammonia oxidizer is the absence of DNA polymerase D genes() – one of the predominant replicative DNA polymerases in all other ammonia-oxidizing Thaumarchaeota. Collectively, our findings suggest that metabolic versatility and DNA replication might differ substantially between obligately thermophilic and other AOA.
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spelling pubmed-58170802018-02-28 Cultivation and Genomic Analysis of “Candidatus Nitrosocaldus islandicus,” an Obligately Thermophilic, Ammonia-Oxidizing Thaumarchaeon from a Hot Spring Biofilm in Graendalur Valley, Iceland Daebeler, Anne Herbold, Craig W. Vierheilig, Julia Sedlacek, Christopher J. Pjevac, Petra Albertsen, Mads Kirkegaard, Rasmus H. de la Torre, José R. Daims, Holger Wagner, Michael Front Microbiol Microbiology Ammonia-oxidizing archaea (AOA) within the phylum Thaumarchaeota are the only known aerobic ammonia oxidizers in geothermal environments. Although molecular data indicate the presence of phylogenetically diverse AOA from the Nitrosocaldus clade, group 1.1b and group 1.1a Thaumarchaeota in terrestrial high-temperature habitats, only one() enrichment culture of an AOA thriving above 50°C has been reported and functionally analyzed. In this study, we physiologically and genomically characterized a newly discovered thaumarchaeon from the deep-branching Nitrosocaldaceae family of which we have obtained a high (∼85%) enrichment from biofilm of an Icelandic hot spring (73°C). This AOA, which we provisionally refer to as “Candidatus Nitrosocaldus islandicus,” is an obligately thermophilic, aerobic chemolithoautotrophic ammonia oxidizer, which stoichiometrically converts ammonia to nitrite at temperatures between 50 and 70°C. “Ca. N. islandicus” encodes the expected repertoire of enzymes proposed to be required for archaeal ammonia oxidation, but unexpectedly lacks a nirK gene and also possesses no identifiable other enzyme for nitric oxide (NO) generation(). Nevertheless, ammonia oxidation by this AOA appears to be NO-dependent as “Ca. N. islandicus” is, like all other tested AOA, inhibited by the addition of an NO scavenger. Furthermore, comparative genomics revealed that “Ca. N. islandicus” has the potential for aromatic amino acid fermentation as its genome encodes an indolepyruvate oxidoreductase (iorAB) as well as a type 3b hydrogenase, which are not present in any other sequenced AOA. A further surprising genomic feature of this thermophilic ammonia oxidizer is the absence of DNA polymerase D genes() – one of the predominant replicative DNA polymerases in all other ammonia-oxidizing Thaumarchaeota. Collectively, our findings suggest that metabolic versatility and DNA replication might differ substantially between obligately thermophilic and other AOA. Frontiers Media S.A. 2018-02-14 /pmc/articles/PMC5817080/ /pubmed/29491853 http://dx.doi.org/10.3389/fmicb.2018.00193 Text en Copyright © 2018 Daebeler, Herbold, Vierheilig, Sedlacek, Pjevac, Albertsen, Kirkegaard, de la Torre, Daims and Wagner. http://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 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
Daebeler, Anne
Herbold, Craig W.
Vierheilig, Julia
Sedlacek, Christopher J.
Pjevac, Petra
Albertsen, Mads
Kirkegaard, Rasmus H.
de la Torre, José R.
Daims, Holger
Wagner, Michael
Cultivation and Genomic Analysis of “Candidatus Nitrosocaldus islandicus,” an Obligately Thermophilic, Ammonia-Oxidizing Thaumarchaeon from a Hot Spring Biofilm in Graendalur Valley, Iceland
title Cultivation and Genomic Analysis of “Candidatus Nitrosocaldus islandicus,” an Obligately Thermophilic, Ammonia-Oxidizing Thaumarchaeon from a Hot Spring Biofilm in Graendalur Valley, Iceland
title_full Cultivation and Genomic Analysis of “Candidatus Nitrosocaldus islandicus,” an Obligately Thermophilic, Ammonia-Oxidizing Thaumarchaeon from a Hot Spring Biofilm in Graendalur Valley, Iceland
title_fullStr Cultivation and Genomic Analysis of “Candidatus Nitrosocaldus islandicus,” an Obligately Thermophilic, Ammonia-Oxidizing Thaumarchaeon from a Hot Spring Biofilm in Graendalur Valley, Iceland
title_full_unstemmed Cultivation and Genomic Analysis of “Candidatus Nitrosocaldus islandicus,” an Obligately Thermophilic, Ammonia-Oxidizing Thaumarchaeon from a Hot Spring Biofilm in Graendalur Valley, Iceland
title_short Cultivation and Genomic Analysis of “Candidatus Nitrosocaldus islandicus,” an Obligately Thermophilic, Ammonia-Oxidizing Thaumarchaeon from a Hot Spring Biofilm in Graendalur Valley, Iceland
title_sort cultivation and genomic analysis of “candidatus nitrosocaldus islandicus,” an obligately thermophilic, ammonia-oxidizing thaumarchaeon from a hot spring biofilm in graendalur valley, iceland
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5817080/
https://www.ncbi.nlm.nih.gov/pubmed/29491853
http://dx.doi.org/10.3389/fmicb.2018.00193
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