Detecting Nitrous Oxide Reductase (<italic toggle="yes">nosZ</italic>) Genes in Soil Metagenomes: Method Development and Implications for the Nitrogen Cycle

ABSTRACT Microbial activities in soils, such as (incomplete) denitrification, represent major sources of nitrous oxide (N2O), a potent greenhouse gas. The key enzyme for mitigating N2O emissions is NosZ, which catalyzes N2O reduction to N2. We recently described “atypical” functional NosZ proteins e...

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Autores principales:	L. H. Orellana, L. M. Rodriguez-R, S. Higgins, J. C. Chee-Sanford, R. A. Sanford, K. M. Ritalahti, F. E. Löffler, K. T. Konstantinidis
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b00f5a3346dc4221a14210185af1294f
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spelling	oai:doaj.org-article:b00f5a3346dc4221a14210185af1294f2021-11-15T15:47:38ZDetecting Nitrous Oxide Reductase (<italic toggle="yes">nosZ</italic>) Genes in Soil Metagenomes: Method Development and Implications for the Nitrogen Cycle10.1128/mBio.01193-142150-7511https://doaj.org/article/b00f5a3346dc4221a14210185af1294f2014-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01193-14https://doaj.org/toc/2150-7511ABSTRACT Microbial activities in soils, such as (incomplete) denitrification, represent major sources of nitrous oxide (N2O), a potent greenhouse gas. The key enzyme for mitigating N2O emissions is NosZ, which catalyzes N2O reduction to N2. We recently described “atypical” functional NosZ proteins encoded by both denitrifiers and nondenitrifiers, which were missed in previous environmental surveys (R. A. Sanford et al., Proc. Natl. Acad. Sci. U. S. A. 109:19709–19714, 2012, doi:10.1073/pnas.1211238109). Here, we analyzed the abundance and diversity of both nosZ types in whole-genome shotgun metagenomes from sandy and silty loam agricultural soils that typify the U.S. Midwest corn belt. First, different search algorithms and parameters for detecting nosZ metagenomic reads were evaluated based on in silico-generated (mock) metagenomes. Using the derived cutoffs, 71 distinct alleles (95% amino acid identity level) encoding typical or atypical NosZ proteins were detected in both soil types. Remarkably, more than 70% of the total nosZ reads in both soils were classified as atypical, emphasizing that prior surveys underestimated nosZ abundance. Approximately 15% of the total nosZ reads were taxonomically related to Anaeromyxobacter, which was the most abundant genus encoding atypical NosZ-type proteins in both soil types. Further analyses revealed that atypical nosZ genes outnumbered typical nosZ genes in most publicly available soil metagenomes, underscoring their potential role in mediating N2O consumption in soils. Therefore, this study provides a bioinformatics strategy to reliably detect target genes in complex short-read metagenomes and suggests that the analysis of both typical and atypical nosZ sequences is required to understand and predict N2O flux in soils. IMPORTANCE Nitrous oxide (N2O) is a potent greenhouse gas with ozone layer destruction potential. Microbial activities control both the production and the consumption of N2O, i.e., its conversion to innocuous dinitrogen gas (N2). Until recently, consumption of N2O was attributed to bacteria encoding “typical” nitrous oxide reductase (NosZ). However, recent phylogenetic and physiological studies have shown that previously uncharacterized, functional, “atypical” NosZ proteins are encoded in genomes of diverse bacterial groups. The present study revealed that atypical nosZ genes outnumbered their typical counterparts, highlighting their potential role in N2O consumption in soils and possibly other environments. These findings advance our understanding of the diversity of microbes and functional genes involved in the nitrogen cycle and provide the means (e.g., gene sequences) to study N2O fluxes to the atmosphere and associated climate change.L. H. OrellanaL. M. Rodriguez-RS. HigginsJ. C. Chee-SanfordR. A. SanfordK. M. RitalahtiF. E. LöfflerK. T. KonstantinidisAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 3 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 L. H. Orellana L. M. Rodriguez-R S. Higgins J. C. Chee-Sanford R. A. Sanford K. M. Ritalahti F. E. Löffler K. T. Konstantinidis Detecting Nitrous Oxide Reductase (<italic toggle="yes">nosZ</italic>) Genes in Soil Metagenomes: Method Development and Implications for the Nitrogen Cycle
description	ABSTRACT Microbial activities in soils, such as (incomplete) denitrification, represent major sources of nitrous oxide (N2O), a potent greenhouse gas. The key enzyme for mitigating N2O emissions is NosZ, which catalyzes N2O reduction to N2. We recently described “atypical” functional NosZ proteins encoded by both denitrifiers and nondenitrifiers, which were missed in previous environmental surveys (R. A. Sanford et al., Proc. Natl. Acad. Sci. U. S. A. 109:19709–19714, 2012, doi:10.1073/pnas.1211238109). Here, we analyzed the abundance and diversity of both nosZ types in whole-genome shotgun metagenomes from sandy and silty loam agricultural soils that typify the U.S. Midwest corn belt. First, different search algorithms and parameters for detecting nosZ metagenomic reads were evaluated based on in silico-generated (mock) metagenomes. Using the derived cutoffs, 71 distinct alleles (95% amino acid identity level) encoding typical or atypical NosZ proteins were detected in both soil types. Remarkably, more than 70% of the total nosZ reads in both soils were classified as atypical, emphasizing that prior surveys underestimated nosZ abundance. Approximately 15% of the total nosZ reads were taxonomically related to Anaeromyxobacter, which was the most abundant genus encoding atypical NosZ-type proteins in both soil types. Further analyses revealed that atypical nosZ genes outnumbered typical nosZ genes in most publicly available soil metagenomes, underscoring their potential role in mediating N2O consumption in soils. Therefore, this study provides a bioinformatics strategy to reliably detect target genes in complex short-read metagenomes and suggests that the analysis of both typical and atypical nosZ sequences is required to understand and predict N2O flux in soils. IMPORTANCE Nitrous oxide (N2O) is a potent greenhouse gas with ozone layer destruction potential. Microbial activities control both the production and the consumption of N2O, i.e., its conversion to innocuous dinitrogen gas (N2). Until recently, consumption of N2O was attributed to bacteria encoding “typical” nitrous oxide reductase (NosZ). However, recent phylogenetic and physiological studies have shown that previously uncharacterized, functional, “atypical” NosZ proteins are encoded in genomes of diverse bacterial groups. The present study revealed that atypical nosZ genes outnumbered their typical counterparts, highlighting their potential role in N2O consumption in soils and possibly other environments. These findings advance our understanding of the diversity of microbes and functional genes involved in the nitrogen cycle and provide the means (e.g., gene sequences) to study N2O fluxes to the atmosphere and associated climate change.
format	article
author	L. H. Orellana L. M. Rodriguez-R S. Higgins J. C. Chee-Sanford R. A. Sanford K. M. Ritalahti F. E. Löffler K. T. Konstantinidis
author_facet	L. H. Orellana L. M. Rodriguez-R S. Higgins J. C. Chee-Sanford R. A. Sanford K. M. Ritalahti F. E. Löffler K. T. Konstantinidis
author_sort	L. H. Orellana
title	Detecting Nitrous Oxide Reductase (<italic toggle="yes">nosZ</italic>) Genes in Soil Metagenomes: Method Development and Implications for the Nitrogen Cycle
title_short	Detecting Nitrous Oxide Reductase (<italic toggle="yes">nosZ</italic>) Genes in Soil Metagenomes: Method Development and Implications for the Nitrogen Cycle
title_full	Detecting Nitrous Oxide Reductase (<italic toggle="yes">nosZ</italic>) Genes in Soil Metagenomes: Method Development and Implications for the Nitrogen Cycle
title_fullStr	Detecting Nitrous Oxide Reductase (<italic toggle="yes">nosZ</italic>) Genes in Soil Metagenomes: Method Development and Implications for the Nitrogen Cycle
title_full_unstemmed	Detecting Nitrous Oxide Reductase (<italic toggle="yes">nosZ</italic>) Genes in Soil Metagenomes: Method Development and Implications for the Nitrogen Cycle
title_sort	detecting nitrous oxide reductase (<italic toggle="yes">nosz</italic>) genes in soil metagenomes: method development and implications for the nitrogen cycle
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/b00f5a3346dc4221a14210185af1294f
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Detecting Nitrous Oxide Reductase (<italic toggle="yes">nosZ</italic>) Genes in Soil Metagenomes: Method Development and Implications for the Nitrogen Cycle

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