Genome-Guided Identification of Organohalide-Respiring <italic toggle="yes">Deltaproteobacteria</italic> from the Marine Environment

ABSTRACT Organohalide compounds are widespread in the environment as a result of both anthropogenic activities and natural production. The marine environment, in particular, is a major reservoir of organohalides, and reductive dehalogenation is thought to be an important process in the overall cycli...

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Autores principales:	Jie Liu, Max M. Häggblom
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Deltaproteobacteria anaerobes marine organohalide respiration Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8a18401df2134ee8926939b8eb30033c
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spelling	oai:doaj.org-article:8a18401df2134ee8926939b8eb30033c2021-11-15T15:52:18ZGenome-Guided Identification of Organohalide-Respiring <italic toggle="yes">Deltaproteobacteria</italic> from the Marine Environment10.1128/mBio.02471-182150-7511https://doaj.org/article/8a18401df2134ee8926939b8eb30033c2018-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02471-18https://doaj.org/toc/2150-7511ABSTRACT Organohalide compounds are widespread in the environment as a result of both anthropogenic activities and natural production. The marine environment, in particular, is a major reservoir of organohalides, and reductive dehalogenation is thought to be an important process in the overall cycling of these compounds. Deltaproteobacteria are important members of the marine microbiota with diverse metabolic capacities, and reductive dehalogenation has been observed in some Deltaproteobacteria. In this study, a comprehensive survey of Deltaproteobacteria genomes revealed that approximately 10% contain reductive dehalogenase (RDase) genes, which are found within a common gene neighborhood. The dehalogenating potential of select RDase A-containing Deltaproteobacteria and their gene expression were experimentally verified. Three Deltaproteobacteria strains isolated from marine environments representing diverse species, Halodesulfovibrio marinisediminis, Desulfuromusa kysingii, and Desulfovibrio bizertensis, were shown to reductively dehalogenate bromophenols and utilize them as terminal electron acceptors in organohalide respiration. Their debrominating activity was not inhibited by sulfate or elemental sulfur, and these species are either sulfate- or sulfur-reducing bacteria. The analysis of RDase A gene transcripts indicated significant upregulation induced by 2,6-dibromophenol. This study extends our knowledge of the phylogenetic diversity of organohalide-respiring bacteria and their functional RDase A gene diversity. The identification of reductive dehalogenase genes in diverse Deltaproteobacteria and confirmation of their organohalide-respiring capability suggest that Deltaproteobacteria play an important role in natural organohalide cycling. IMPORTANCE The marine environment is a major reservoir for both anthropogenic and natural organohalides, and reductive dehalogenation is thought to be an important process in the overall cycling of these compounds. Here we demonstrate that the capacity of organohalide respiration appears to be widely distributed in members of marine Deltaproteobacteria. The identification of reductive dehalogenase genes in diverse Deltaproteobacteria and the confirmation of their dehalogenating activity through functional assays and transcript analysis in select isolates extend our knowledge of organohalide-respiring Deltaproteobacteria diversity. The presence of functional reductive dehalogenase genes in diverse Deltaproteobacteria implies that they may play an important role in organohalide respiration in the environment.Jie LiuMax M. HäggblomAmerican Society for MicrobiologyarticleDeltaproteobacteriaanaerobesmarineorganohalide respirationMicrobiologyQR1-502ENmBio, Vol 9, Iss 6 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Deltaproteobacteria anaerobes marine organohalide respiration Microbiology QR1-502
spellingShingle	Deltaproteobacteria anaerobes marine organohalide respiration Microbiology QR1-502 Jie Liu Max M. Häggblom Genome-Guided Identification of Organohalide-Respiring <italic toggle="yes">Deltaproteobacteria</italic> from the Marine Environment
description	ABSTRACT Organohalide compounds are widespread in the environment as a result of both anthropogenic activities and natural production. The marine environment, in particular, is a major reservoir of organohalides, and reductive dehalogenation is thought to be an important process in the overall cycling of these compounds. Deltaproteobacteria are important members of the marine microbiota with diverse metabolic capacities, and reductive dehalogenation has been observed in some Deltaproteobacteria. In this study, a comprehensive survey of Deltaproteobacteria genomes revealed that approximately 10% contain reductive dehalogenase (RDase) genes, which are found within a common gene neighborhood. The dehalogenating potential of select RDase A-containing Deltaproteobacteria and their gene expression were experimentally verified. Three Deltaproteobacteria strains isolated from marine environments representing diverse species, Halodesulfovibrio marinisediminis, Desulfuromusa kysingii, and Desulfovibrio bizertensis, were shown to reductively dehalogenate bromophenols and utilize them as terminal electron acceptors in organohalide respiration. Their debrominating activity was not inhibited by sulfate or elemental sulfur, and these species are either sulfate- or sulfur-reducing bacteria. The analysis of RDase A gene transcripts indicated significant upregulation induced by 2,6-dibromophenol. This study extends our knowledge of the phylogenetic diversity of organohalide-respiring bacteria and their functional RDase A gene diversity. The identification of reductive dehalogenase genes in diverse Deltaproteobacteria and confirmation of their organohalide-respiring capability suggest that Deltaproteobacteria play an important role in natural organohalide cycling. IMPORTANCE The marine environment is a major reservoir for both anthropogenic and natural organohalides, and reductive dehalogenation is thought to be an important process in the overall cycling of these compounds. Here we demonstrate that the capacity of organohalide respiration appears to be widely distributed in members of marine Deltaproteobacteria. The identification of reductive dehalogenase genes in diverse Deltaproteobacteria and the confirmation of their dehalogenating activity through functional assays and transcript analysis in select isolates extend our knowledge of organohalide-respiring Deltaproteobacteria diversity. The presence of functional reductive dehalogenase genes in diverse Deltaproteobacteria implies that they may play an important role in organohalide respiration in the environment.
format	article
author	Jie Liu Max M. Häggblom
author_facet	Jie Liu Max M. Häggblom
author_sort	Jie Liu
title	Genome-Guided Identification of Organohalide-Respiring <italic toggle="yes">Deltaproteobacteria</italic> from the Marine Environment
title_short	Genome-Guided Identification of Organohalide-Respiring <italic toggle="yes">Deltaproteobacteria</italic> from the Marine Environment
title_full	Genome-Guided Identification of Organohalide-Respiring <italic toggle="yes">Deltaproteobacteria</italic> from the Marine Environment
title_fullStr	Genome-Guided Identification of Organohalide-Respiring <italic toggle="yes">Deltaproteobacteria</italic> from the Marine Environment
title_full_unstemmed	Genome-Guided Identification of Organohalide-Respiring <italic toggle="yes">Deltaproteobacteria</italic> from the Marine Environment
title_sort	genome-guided identification of organohalide-respiring <italic toggle="yes">deltaproteobacteria</italic> from the marine environment
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/8a18401df2134ee8926939b8eb30033c
work_keys_str_mv	AT jieliu genomeguidedidentificationoforganohaliderespiringitalictoggleyesdeltaproteobacteriaitalicfromthemarineenvironment AT maxmhaggblom genomeguidedidentificationoforganohaliderespiringitalictoggleyesdeltaproteobacteriaitalicfromthemarineenvironment
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Genome-Guided Identification of Organohalide-Respiring <italic toggle="yes">Deltaproteobacteria</italic> from the Marine Environment

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