Unusual Metabolism and Hypervariation in the Genome of a Gracilibacterium (BD1-5) from an Oil-Degrading Community

ABSTRACT The candidate phyla radiation (CPR) comprises a large monophyletic group of bacterial lineages known almost exclusively based on genomes obtained using cultivation-independent methods. Within the CPR, Gracilibacteria (BD1-5) are particularly poorly understood due to undersampling and the in...

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Autores principales:	Christian M. K. Sieber, Blair G. Paul, Cindy J. Castelle, Ping Hu, Susannah G. Tringe, David L. Valentine, Gary L. Andersen, Jillian F. Banfield
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	BD1-5 CPR candidate phyla radiation genomes from metagenomes gracilibacteria surface proteins Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/09bed20fa5fe4743a01df2d9cf72f9a1
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spelling	oai:doaj.org-article:09bed20fa5fe4743a01df2d9cf72f9a12021-11-15T15:54:45ZUnusual Metabolism and Hypervariation in the Genome of a Gracilibacterium (BD1-5) from an Oil-Degrading Community10.1128/mBio.02128-192150-7511https://doaj.org/article/09bed20fa5fe4743a01df2d9cf72f9a12019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02128-19https://doaj.org/toc/2150-7511ABSTRACT The candidate phyla radiation (CPR) comprises a large monophyletic group of bacterial lineages known almost exclusively based on genomes obtained using cultivation-independent methods. Within the CPR, Gracilibacteria (BD1-5) are particularly poorly understood due to undersampling and the inherent fragmented nature of available genomes. Here, we report the first closed, curated genome of a gracilibacterium from an enrichment experiment inoculated from the Gulf of Mexico and designed to investigate hydrocarbon degradation. The gracilibacterium rose in abundance after the community switched to dominance by Colwellia. Notably, we predict that this gracilibacterium completely lacks glycolysis, the pentose phosphate and Entner-Doudoroff pathways. It appears to acquire pyruvate, acetyl coenzyme A (acetyl-CoA), and oxaloacetate via degradation of externally derived citrate, malate, and amino acids and may use compound interconversion and oxidoreductases to generate and recycle reductive power. The initial genome assembly was fragmented in an unusual gene that is hypervariable within a repeat region. Such extreme local variation is rare but characteristic of genes that confer traits under pressure to diversify within a population. Notably, the four major repeated 9-mer nucleotide sequences all generate a proline-threonine-aspartic acid (PTD) repeat. The genome of an abundant Colwellia psychrerythraea population has a large extracellular protein that also contains the repeated PTD motif. Although we do not know the host for the BD1-5 cell, the high relative abundance of the C. psychrerythraea population and the shared surface protein repeat may indicate an association between these bacteria. IMPORTANCE CPR bacteria are generally predicted to be symbionts due to their extensive biosynthetic deficits. Although monophyletic, they are not monolithic in terms of their lifestyles. The organism described here appears to have evolved an unusual metabolic platform not reliant on glucose or pentose sugars. Its biology appears to be centered around bacterial host-derived compounds and/or cell detritus. Amino acids likely provide building blocks for nucleic acids, peptidoglycan, and protein synthesis. We resolved an unusual repeat region that would be invisible without genome curation. The nucleotide sequence is apparently under strong diversifying selection, but the amino acid sequence is under stabilizing selection. The amino acid repeat also occurs in a surface protein of a coexisting bacterium, suggesting colocation and possibly interdependence.Christian M. K. SieberBlair G. PaulCindy J. CastellePing HuSusannah G. TringeDavid L. ValentineGary L. AndersenJillian F. BanfieldAmerican Society for MicrobiologyarticleBD1-5CPRcandidate phyla radiationgenomes from metagenomesgracilibacteriasurface proteinsMicrobiologyQR1-502ENmBio, Vol 10, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	BD1-5 CPR candidate phyla radiation genomes from metagenomes gracilibacteria surface proteins Microbiology QR1-502
spellingShingle	BD1-5 CPR candidate phyla radiation genomes from metagenomes gracilibacteria surface proteins Microbiology QR1-502 Christian M. K. Sieber Blair G. Paul Cindy J. Castelle Ping Hu Susannah G. Tringe David L. Valentine Gary L. Andersen Jillian F. Banfield Unusual Metabolism and Hypervariation in the Genome of a Gracilibacterium (BD1-5) from an Oil-Degrading Community
description	ABSTRACT The candidate phyla radiation (CPR) comprises a large monophyletic group of bacterial lineages known almost exclusively based on genomes obtained using cultivation-independent methods. Within the CPR, Gracilibacteria (BD1-5) are particularly poorly understood due to undersampling and the inherent fragmented nature of available genomes. Here, we report the first closed, curated genome of a gracilibacterium from an enrichment experiment inoculated from the Gulf of Mexico and designed to investigate hydrocarbon degradation. The gracilibacterium rose in abundance after the community switched to dominance by Colwellia. Notably, we predict that this gracilibacterium completely lacks glycolysis, the pentose phosphate and Entner-Doudoroff pathways. It appears to acquire pyruvate, acetyl coenzyme A (acetyl-CoA), and oxaloacetate via degradation of externally derived citrate, malate, and amino acids and may use compound interconversion and oxidoreductases to generate and recycle reductive power. The initial genome assembly was fragmented in an unusual gene that is hypervariable within a repeat region. Such extreme local variation is rare but characteristic of genes that confer traits under pressure to diversify within a population. Notably, the four major repeated 9-mer nucleotide sequences all generate a proline-threonine-aspartic acid (PTD) repeat. The genome of an abundant Colwellia psychrerythraea population has a large extracellular protein that also contains the repeated PTD motif. Although we do not know the host for the BD1-5 cell, the high relative abundance of the C. psychrerythraea population and the shared surface protein repeat may indicate an association between these bacteria. IMPORTANCE CPR bacteria are generally predicted to be symbionts due to their extensive biosynthetic deficits. Although monophyletic, they are not monolithic in terms of their lifestyles. The organism described here appears to have evolved an unusual metabolic platform not reliant on glucose or pentose sugars. Its biology appears to be centered around bacterial host-derived compounds and/or cell detritus. Amino acids likely provide building blocks for nucleic acids, peptidoglycan, and protein synthesis. We resolved an unusual repeat region that would be invisible without genome curation. The nucleotide sequence is apparently under strong diversifying selection, but the amino acid sequence is under stabilizing selection. The amino acid repeat also occurs in a surface protein of a coexisting bacterium, suggesting colocation and possibly interdependence.
format	article
author	Christian M. K. Sieber Blair G. Paul Cindy J. Castelle Ping Hu Susannah G. Tringe David L. Valentine Gary L. Andersen Jillian F. Banfield
author_facet	Christian M. K. Sieber Blair G. Paul Cindy J. Castelle Ping Hu Susannah G. Tringe David L. Valentine Gary L. Andersen Jillian F. Banfield
author_sort	Christian M. K. Sieber
title	Unusual Metabolism and Hypervariation in the Genome of a Gracilibacterium (BD1-5) from an Oil-Degrading Community
title_short	Unusual Metabolism and Hypervariation in the Genome of a Gracilibacterium (BD1-5) from an Oil-Degrading Community
title_full	Unusual Metabolism and Hypervariation in the Genome of a Gracilibacterium (BD1-5) from an Oil-Degrading Community
title_fullStr	Unusual Metabolism and Hypervariation in the Genome of a Gracilibacterium (BD1-5) from an Oil-Degrading Community
title_full_unstemmed	Unusual Metabolism and Hypervariation in the Genome of a Gracilibacterium (BD1-5) from an Oil-Degrading Community
title_sort	unusual metabolism and hypervariation in the genome of a gracilibacterium (bd1-5) from an oil-degrading community
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/09bed20fa5fe4743a01df2d9cf72f9a1
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Unusual Metabolism and Hypervariation in the Genome of a Gracilibacterium (BD1-5) from an Oil-Degrading Community

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