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Title: 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 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 byColwellia. 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 abundantColwellia psychrerythraeapopulation has a large extracellular protein that also contains the repeated PTD motif. Althoughmore » we do not know the host for the BD1-5 cell, the high relative abundance of theC. psychrerythraeapopulation and the shared surface protein repeat may indicate an association between these bacteria. 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. Finally, the amino acid repeat also occurs in a surface protein of a coexisting bacterium, suggesting colocation and possibly interdependence.« less

Authors:
ORCiD logo [1];  [2];  [3];  [4];  [5];  [2];  [6];  [3];  [7]
  1. Univ. of California, Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  2. Univ. of California, Santa Barbara, CA (United States)
  3. Univ. of California, Berkeley, CA (United States)
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); St. Mary's College of California, Moraga, CA (United States)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  6. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
  7. VA Palo Alto Health Care System, Livermore, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Institutes of Health (NIH)
OSTI Identifier:
1581335
Grant/Contract Number:  
AC02-05CH11231; SC10010566; 5R01AI092531
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 10; Journal Issue: 6; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; BD1-5; CPR; candidate phyla radiation; genomes from metagenomes; gracilibacteria; surface proteins

Citation Formats

Sieber, Christian M. K., Paul, Blair G., Castelle, Cindy J., Hu, Ping, Tringe, Susannah G., Valentine, David L., Andersen, Gary L., Banfield, Jillian F., and Relman, David A. Unusual Metabolism and Hypervariation in the Genome of a Gracilibacterium (BD1-5) from an Oil-Degrading Community. United States: N. p., 2019. Web. doi:10.1128/mBio.02128-19.
Sieber, Christian M. K., Paul, Blair G., Castelle, Cindy J., Hu, Ping, Tringe, Susannah G., Valentine, David L., Andersen, Gary L., Banfield, Jillian F., & Relman, David A. Unusual Metabolism and Hypervariation in the Genome of a Gracilibacterium (BD1-5) from an Oil-Degrading Community. United States. doi:10.1128/mBio.02128-19.
Sieber, Christian M. K., Paul, Blair G., Castelle, Cindy J., Hu, Ping, Tringe, Susannah G., Valentine, David L., Andersen, Gary L., Banfield, Jillian F., and Relman, David A. Tue . "Unusual Metabolism and Hypervariation in the Genome of a Gracilibacterium (BD1-5) from an Oil-Degrading Community". United States. doi:10.1128/mBio.02128-19. https://www.osti.gov/servlets/purl/1581335.
@article{osti_1581335,
title = {Unusual Metabolism and Hypervariation in the Genome of a Gracilibacterium (BD1-5) from an Oil-Degrading Community},
author = {Sieber, Christian M. K. and Paul, Blair G. and Castelle, Cindy J. and Hu, Ping and Tringe, Susannah G. and Valentine, David L. and Andersen, Gary L. and Banfield, Jillian F. and Relman, David A.},
abstractNote = {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 byColwellia. 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 abundantColwellia psychrerythraeapopulation 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 theC. psychrerythraeapopulation and the shared surface protein repeat may indicate an association between these bacteria. 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. Finally, the amino acid repeat also occurs in a surface protein of a coexisting bacterium, suggesting colocation and possibly interdependence.},
doi = {10.1128/mBio.02128-19},
journal = {mBio (Online)},
number = 6,
volume = 10,
place = {United States},
year = {2019},
month = {11}
}

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