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Identification, Expression and Activity of Candidate Nitrite Reductases From Orange Beggiatoaceae, Guaymas Basin

Orange filamentous Beggiatoaceae form massive microbial mats on hydrothermal sediments in Guaymas Basin; these bacteria are considered to oxidize sulfide with nitrate and nitrite as electron acceptors. From a previously analyzed genome of an orange Beggiatoaceae filament, three candidate genes for e...

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Autores principales: Buckley, Andrew, MacGregor, Barbara, Teske, Andreas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6449678/
https://www.ncbi.nlm.nih.gov/pubmed/30984153
http://dx.doi.org/10.3389/fmicb.2019.00644
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author Buckley, Andrew
MacGregor, Barbara
Teske, Andreas
author_facet Buckley, Andrew
MacGregor, Barbara
Teske, Andreas
author_sort Buckley, Andrew
collection PubMed
description Orange filamentous Beggiatoaceae form massive microbial mats on hydrothermal sediments in Guaymas Basin; these bacteria are considered to oxidize sulfide with nitrate and nitrite as electron acceptors. From a previously analyzed genome of an orange Beggiatoaceae filament, three candidate genes for enzymes with nitrite-reducing function – an orange octaheme cytochrome, a nirS nitrite reductase, and a nitrite/tetrathionate-reducing octaheme cytochrome – were cloned and expressed in Escherichia coli. The expressed and purified orange cytochrome showed reduced nitrite-reducing activity compared to the multifunctional native protein obtained from microbial mats. The nirS gene product showed in vitro but no in-gel nitrite-reducing activity; and the nitrite/tetrathionate-reducing octaheme cytochrome was capable of reducing both nitrite and tetrathionate in vitro. Phylogenetic analysis shows that the orange Beggiatoaceae nirS, in contrast to the other candidate nitrite reductases, does not form monophyletic lineages with its counterparts in other large sulfur-oxidizing bacteria, and most likely represents a recent acquisition by lateral gene transfer. The nitrite/tetrathionate-reducing enzyme of the orange Beggiatoaceae is related to nitrite- and tetrathionate reductases harbored predominantly by Gammaproteobacteria, including obligate endosymbionts of hydrothermal vent tubeworms. Thus, the orange Guaymas Basin Beggiatoaceae have a repertoire of at least three different functional enzymes for nitrite reduction. By demonstrating the unusual diversity of enzymes with a potential role in nitrite reduction, we show that bacteria in highly dynamic, sulfide-rich hydrothermal vent habitats adapt to these conditions that usually prohibit nitrate and nitrite reduction. In the case of the orange Guaymas Beggiatoaceae, classical denitrification appears to be replaced by different multifunctional enzymes for nitrite and tetrathionate reduction; the resulting ecophysiological flexibility provides a new key to the dominance of these Beggiatoaceae in hydrothermal hot spots.
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spelling pubmed-64496782019-04-12 Identification, Expression and Activity of Candidate Nitrite Reductases From Orange Beggiatoaceae, Guaymas Basin Buckley, Andrew MacGregor, Barbara Teske, Andreas Front Microbiol Microbiology Orange filamentous Beggiatoaceae form massive microbial mats on hydrothermal sediments in Guaymas Basin; these bacteria are considered to oxidize sulfide with nitrate and nitrite as electron acceptors. From a previously analyzed genome of an orange Beggiatoaceae filament, three candidate genes for enzymes with nitrite-reducing function – an orange octaheme cytochrome, a nirS nitrite reductase, and a nitrite/tetrathionate-reducing octaheme cytochrome – were cloned and expressed in Escherichia coli. The expressed and purified orange cytochrome showed reduced nitrite-reducing activity compared to the multifunctional native protein obtained from microbial mats. The nirS gene product showed in vitro but no in-gel nitrite-reducing activity; and the nitrite/tetrathionate-reducing octaheme cytochrome was capable of reducing both nitrite and tetrathionate in vitro. Phylogenetic analysis shows that the orange Beggiatoaceae nirS, in contrast to the other candidate nitrite reductases, does not form monophyletic lineages with its counterparts in other large sulfur-oxidizing bacteria, and most likely represents a recent acquisition by lateral gene transfer. The nitrite/tetrathionate-reducing enzyme of the orange Beggiatoaceae is related to nitrite- and tetrathionate reductases harbored predominantly by Gammaproteobacteria, including obligate endosymbionts of hydrothermal vent tubeworms. Thus, the orange Guaymas Basin Beggiatoaceae have a repertoire of at least three different functional enzymes for nitrite reduction. By demonstrating the unusual diversity of enzymes with a potential role in nitrite reduction, we show that bacteria in highly dynamic, sulfide-rich hydrothermal vent habitats adapt to these conditions that usually prohibit nitrate and nitrite reduction. In the case of the orange Guaymas Beggiatoaceae, classical denitrification appears to be replaced by different multifunctional enzymes for nitrite and tetrathionate reduction; the resulting ecophysiological flexibility provides a new key to the dominance of these Beggiatoaceae in hydrothermal hot spots. Frontiers Media S.A. 2019-03-29 /pmc/articles/PMC6449678/ /pubmed/30984153 http://dx.doi.org/10.3389/fmicb.2019.00644 Text en Copyright © 2019 Buckley, MacGregor and Teske. 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(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
Buckley, Andrew
MacGregor, Barbara
Teske, Andreas
Identification, Expression and Activity of Candidate Nitrite Reductases From Orange Beggiatoaceae, Guaymas Basin
title Identification, Expression and Activity of Candidate Nitrite Reductases From Orange Beggiatoaceae, Guaymas Basin
title_full Identification, Expression and Activity of Candidate Nitrite Reductases From Orange Beggiatoaceae, Guaymas Basin
title_fullStr Identification, Expression and Activity of Candidate Nitrite Reductases From Orange Beggiatoaceae, Guaymas Basin
title_full_unstemmed Identification, Expression and Activity of Candidate Nitrite Reductases From Orange Beggiatoaceae, Guaymas Basin
title_short Identification, Expression and Activity of Candidate Nitrite Reductases From Orange Beggiatoaceae, Guaymas Basin
title_sort identification, expression and activity of candidate nitrite reductases from orange beggiatoaceae, guaymas basin
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6449678/
https://www.ncbi.nlm.nih.gov/pubmed/30984153
http://dx.doi.org/10.3389/fmicb.2019.00644
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