Homoacetogenesis in Deep-Sea <italic toggle="yes">Chloroflexi</italic>, as Inferred by Single-Cell Genomics, Provides a Link to Reductive Dehalogenation in Terrestrial <italic toggle="yes">Dehalococcoidetes</italic>

ABSTRACT The deep marine subsurface is one of the largest unexplored biospheres on Earth and is widely inhabited by members of the phylum Chloroflexi. In this report, we investigated genomes of single cells obtained from deep-sea sediments of the Peruvian Margin, which are enriched in such Chlorofle...

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Autores principales:	Holly L. Sewell, Anne-Kristin Kaster, Alfred M. Spormann
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	anaerobic benzoate oxidation Anaerolineae homoacetogenesis benzoyl-CoA reductase Dehalococcoidia Wood-Ljungdahl pathway Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/24af694dbb21431fb83438247e953d8a
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spelling	oai:doaj.org-article:24af694dbb21431fb83438247e953d8a2021-11-15T15:51:55ZHomoacetogenesis in Deep-Sea <italic toggle="yes">Chloroflexi</italic>, as Inferred by Single-Cell Genomics, Provides a Link to Reductive Dehalogenation in Terrestrial <italic toggle="yes">Dehalococcoidetes</italic>10.1128/mBio.02022-172150-7511https://doaj.org/article/24af694dbb21431fb83438247e953d8a2017-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02022-17https://doaj.org/toc/2150-7511ABSTRACT The deep marine subsurface is one of the largest unexplored biospheres on Earth and is widely inhabited by members of the phylum Chloroflexi. In this report, we investigated genomes of single cells obtained from deep-sea sediments of the Peruvian Margin, which are enriched in such Chloroflexi. 16S rRNA gene sequence analysis placed two of these single-cell-derived genomes (DscP3 and Dsc4) in a clade of subphylum I Chloroflexi which were previously recovered from deep-sea sediment in the Okinawa Trough and a third (DscP2-2) as a member of the previously reported DscP2 population from Peruvian Margin site 1230. The presence of genes encoding enzymes of a complete Wood-Ljungdahl pathway, glycolysis/gluconeogenesis, a Rhodobacter nitrogen fixation (Rnf) complex, glyosyltransferases, and formate dehydrogenases in the single-cell genomes of DscP3 and Dsc4 and the presence of an NADH-dependent reduced ferredoxin:NADP oxidoreductase (Nfn) and Rnf in the genome of DscP2-2 imply a homoacetogenic lifestyle of these abundant marine Chloroflexi. We also report here the first complete pathway for anaerobic benzoate oxidation to acetyl coenzyme A (CoA) in the phylum Chloroflexi (DscP3 and Dsc4), including a class I benzoyl-CoA reductase. Of remarkable evolutionary significance, we discovered a gene encoding a formate dehydrogenase (FdnI) with reciprocal closest identity to the formate dehydrogenase-like protein (complex iron-sulfur molybdoenzyme [CISM], DET0187) of terrestrial Dehalococcoides/Dehalogenimonas spp. This formate dehydrogenase-like protein has been shown to lack formate dehydrogenase activity in Dehalococcoides/Dehalogenimonas spp. and is instead hypothesized to couple HupL hydrogenase to a reductive dehalogenase in the catabolic reductive dehalogenation pathway. This finding of a close functional homologue provides an important missing link for understanding the origin and the metabolic core of terrestrial Dehalococcoides/Dehalogenimonas spp. and of reductive dehalogenation, as well as the biology of abundant deep-sea Chloroflexi. IMPORTANCE The deep marine subsurface is one of the largest unexplored biospheres on Earth and is widely inhabited by members of the phylum Chloroflexi. In this report, we investigated genomes of single cells obtained from deep-sea sediments and provide evidence for a homacetogenic lifestyle of these abundant marine Chloroflexi. Moreover, genome signature and key metabolic genes indicate an evolutionary relationship between these deep-sea sediment microbes and terrestrial, reductively dehalogenating Dehalococcoides.Holly L. SewellAnne-Kristin KasterAlfred M. SpormannAmerican Society for Microbiologyarticleanaerobic benzoate oxidationAnaerolineaehomoacetogenesisbenzoyl-CoA reductaseDehalococcoidiaWood-Ljungdahl pathwayMicrobiologyQR1-502ENmBio, Vol 8, Iss 6 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	anaerobic benzoate oxidation Anaerolineae homoacetogenesis benzoyl-CoA reductase Dehalococcoidia Wood-Ljungdahl pathway Microbiology QR1-502
spellingShingle	anaerobic benzoate oxidation Anaerolineae homoacetogenesis benzoyl-CoA reductase Dehalococcoidia Wood-Ljungdahl pathway Microbiology QR1-502 Holly L. Sewell Anne-Kristin Kaster Alfred M. Spormann Homoacetogenesis in Deep-Sea <italic toggle="yes">Chloroflexi</italic>, as Inferred by Single-Cell Genomics, Provides a Link to Reductive Dehalogenation in Terrestrial <italic toggle="yes">Dehalococcoidetes</italic>
description	ABSTRACT The deep marine subsurface is one of the largest unexplored biospheres on Earth and is widely inhabited by members of the phylum Chloroflexi. In this report, we investigated genomes of single cells obtained from deep-sea sediments of the Peruvian Margin, which are enriched in such Chloroflexi. 16S rRNA gene sequence analysis placed two of these single-cell-derived genomes (DscP3 and Dsc4) in a clade of subphylum I Chloroflexi which were previously recovered from deep-sea sediment in the Okinawa Trough and a third (DscP2-2) as a member of the previously reported DscP2 population from Peruvian Margin site 1230. The presence of genes encoding enzymes of a complete Wood-Ljungdahl pathway, glycolysis/gluconeogenesis, a Rhodobacter nitrogen fixation (Rnf) complex, glyosyltransferases, and formate dehydrogenases in the single-cell genomes of DscP3 and Dsc4 and the presence of an NADH-dependent reduced ferredoxin:NADP oxidoreductase (Nfn) and Rnf in the genome of DscP2-2 imply a homoacetogenic lifestyle of these abundant marine Chloroflexi. We also report here the first complete pathway for anaerobic benzoate oxidation to acetyl coenzyme A (CoA) in the phylum Chloroflexi (DscP3 and Dsc4), including a class I benzoyl-CoA reductase. Of remarkable evolutionary significance, we discovered a gene encoding a formate dehydrogenase (FdnI) with reciprocal closest identity to the formate dehydrogenase-like protein (complex iron-sulfur molybdoenzyme [CISM], DET0187) of terrestrial Dehalococcoides/Dehalogenimonas spp. This formate dehydrogenase-like protein has been shown to lack formate dehydrogenase activity in Dehalococcoides/Dehalogenimonas spp. and is instead hypothesized to couple HupL hydrogenase to a reductive dehalogenase in the catabolic reductive dehalogenation pathway. This finding of a close functional homologue provides an important missing link for understanding the origin and the metabolic core of terrestrial Dehalococcoides/Dehalogenimonas spp. and of reductive dehalogenation, as well as the biology of abundant deep-sea Chloroflexi. IMPORTANCE The deep marine subsurface is one of the largest unexplored biospheres on Earth and is widely inhabited by members of the phylum Chloroflexi. In this report, we investigated genomes of single cells obtained from deep-sea sediments and provide evidence for a homacetogenic lifestyle of these abundant marine Chloroflexi. Moreover, genome signature and key metabolic genes indicate an evolutionary relationship between these deep-sea sediment microbes and terrestrial, reductively dehalogenating Dehalococcoides.
format	article
author	Holly L. Sewell Anne-Kristin Kaster Alfred M. Spormann
author_facet	Holly L. Sewell Anne-Kristin Kaster Alfred M. Spormann
author_sort	Holly L. Sewell
title	Homoacetogenesis in Deep-Sea <italic toggle="yes">Chloroflexi</italic>, as Inferred by Single-Cell Genomics, Provides a Link to Reductive Dehalogenation in Terrestrial <italic toggle="yes">Dehalococcoidetes</italic>
title_short	Homoacetogenesis in Deep-Sea <italic toggle="yes">Chloroflexi</italic>, as Inferred by Single-Cell Genomics, Provides a Link to Reductive Dehalogenation in Terrestrial <italic toggle="yes">Dehalococcoidetes</italic>
title_full	Homoacetogenesis in Deep-Sea <italic toggle="yes">Chloroflexi</italic>, as Inferred by Single-Cell Genomics, Provides a Link to Reductive Dehalogenation in Terrestrial <italic toggle="yes">Dehalococcoidetes</italic>
title_fullStr	Homoacetogenesis in Deep-Sea <italic toggle="yes">Chloroflexi</italic>, as Inferred by Single-Cell Genomics, Provides a Link to Reductive Dehalogenation in Terrestrial <italic toggle="yes">Dehalococcoidetes</italic>
title_full_unstemmed	Homoacetogenesis in Deep-Sea <italic toggle="yes">Chloroflexi</italic>, as Inferred by Single-Cell Genomics, Provides a Link to Reductive Dehalogenation in Terrestrial <italic toggle="yes">Dehalococcoidetes</italic>
title_sort	homoacetogenesis in deep-sea <italic toggle="yes">chloroflexi</italic>, as inferred by single-cell genomics, provides a link to reductive dehalogenation in terrestrial <italic toggle="yes">dehalococcoidetes</italic>
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/24af694dbb21431fb83438247e953d8a
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Homoacetogenesis in Deep-Sea <italic toggle="yes">Chloroflexi</italic>, as Inferred by Single-Cell Genomics, Provides a Link to Reductive Dehalogenation in Terrestrial <italic toggle="yes">Dehalococcoidetes</italic>

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