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Title: Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla

Abstract

Cultivation-independent surveys of microbial diversity have revealed many bacterial phyla that lack cultured representatives. These lineages, referred to as candidate phyla, have been detected across many environments. Here, we deeply sequenced microbial communities from acetate-stimulated aquifer sediment to recover the complete and essentially complete genomes of single representatives of the candidate phyla SR1, WWE3, TM7, and OD1. All four of these genomes are very small, 0.7 to 1.2 Mbp, and have large inventories of novel proteins. Additionally, all lack identifiable biosynthetic pathways for several key metabolites. The SR1 genome uses the UGA codon to encode glycine, and the same codon is very rare in the OD1 genome, suggesting that the OD1 organism could also transition to alternate coding. Interestingly, the relative abundance of the members of SR1 increased with the appearance of sulfide in groundwater, a pattern mirrored by a member of the phylumTenericutes. All four genomes encode type IV pili, which may be involved in interorganism interaction. On the basis of these results and other recently published research, metabolic dependence on other organisms may be widely distributed across multiple bacterial candidate phyla. Few or no genomic sequences exist for members of the numerous bacterial phyla lacking cultivated representatives, making itmore » difficult to assess their roles in the environment. This paper presents three complete and one essentially complete genomes of members of four candidate phyla, documents consistently small genome size, and predicts metabolic capabilities on the basis of gene content. These metagenomic analyses expand our view of a lifestyle apparently common across these candidate phyla.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1]
  1. Univ. of California, Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1511374
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 4; Journal Issue: 5; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Kantor, Rose S., Wrighton, Kelly C., Handley, Kim M., Sharon, Itai, Hug, Laura A., Castelle, Cindy J., Thomas, Brian C., Banfield, Jillian F., Brune, Andreas, and Giovannoni, Stephen J. Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla. United States: N. p., 2013. Web. doi:10.1128/mBio.00708-13.
Kantor, Rose S., Wrighton, Kelly C., Handley, Kim M., Sharon, Itai, Hug, Laura A., Castelle, Cindy J., Thomas, Brian C., Banfield, Jillian F., Brune, Andreas, & Giovannoni, Stephen J. Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla. United States. https://doi.org/10.1128/mBio.00708-13
Kantor, Rose S., Wrighton, Kelly C., Handley, Kim M., Sharon, Itai, Hug, Laura A., Castelle, Cindy J., Thomas, Brian C., Banfield, Jillian F., Brune, Andreas, and Giovannoni, Stephen J. Tue . "Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla". United States. https://doi.org/10.1128/mBio.00708-13. https://www.osti.gov/servlets/purl/1511374.
@article{osti_1511374,
title = {Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla},
author = {Kantor, Rose S. and Wrighton, Kelly C. and Handley, Kim M. and Sharon, Itai and Hug, Laura A. and Castelle, Cindy J. and Thomas, Brian C. and Banfield, Jillian F. and Brune, Andreas and Giovannoni, Stephen J.},
abstractNote = {Cultivation-independent surveys of microbial diversity have revealed many bacterial phyla that lack cultured representatives. These lineages, referred to as candidate phyla, have been detected across many environments. Here, we deeply sequenced microbial communities from acetate-stimulated aquifer sediment to recover the complete and essentially complete genomes of single representatives of the candidate phyla SR1, WWE3, TM7, and OD1. All four of these genomes are very small, 0.7 to 1.2 Mbp, and have large inventories of novel proteins. Additionally, all lack identifiable biosynthetic pathways for several key metabolites. The SR1 genome uses the UGA codon to encode glycine, and the same codon is very rare in the OD1 genome, suggesting that the OD1 organism could also transition to alternate coding. Interestingly, the relative abundance of the members of SR1 increased with the appearance of sulfide in groundwater, a pattern mirrored by a member of the phylumTenericutes. All four genomes encode type IV pili, which may be involved in interorganism interaction. On the basis of these results and other recently published research, metabolic dependence on other organisms may be widely distributed across multiple bacterial candidate phyla. Few or no genomic sequences exist for members of the numerous bacterial phyla lacking cultivated representatives, making it difficult to assess their roles in the environment. This paper presents three complete and one essentially complete genomes of members of four candidate phyla, documents consistently small genome size, and predicts metabolic capabilities on the basis of gene content. These metagenomic analyses expand our view of a lifestyle apparently common across these candidate phyla.},
doi = {10.1128/mBio.00708-13},
journal = {mBio (Online)},
number = 5,
volume = 4,
place = {United States},
year = {Tue Oct 22 00:00:00 EDT 2013},
month = {Tue Oct 22 00:00:00 EDT 2013}
}

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Cited by: 211 works
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Figures / Tables:

FIG 1 FIG 1: Complete and nearly complete genomes from four CP (RAAC1 to RAAC4) were reconstructed. (Left) Phylogeny of selected CP based on 16S rRNA genes. The maximum-likelihood tree shown was constructed from an alignment containing 111 taxa and 1,565 unambiguously aligned positions. Bootstrap values of >80% are displayed as filledmore » circles (for accession numbers, see Fig. S1 in the supplemental material). Also noted are previously sequenced partial and complete genomes for related members of the CP for which full-length 16S rRNA gene sequences were available (8, 10, 12, 19, 20, 22). (Right) ESOMs made by using differential coverage across the 14 sediment columns confirmed genome binning.« less

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Genomic Description of ‘Candidatus Abyssubacteria,’ a Novel Subsurface Lineage Within the Candidate Phylum Hydrogenedentes
journal, August 2018


Impact of single-cell genomics and metagenomics on the emerging view of extremophile “microbial dark matter”
journal, August 2014

  • Hedlund, Brian P.; Dodsworth, Jeremy A.; Murugapiran, Senthil K.
  • Extremophiles, Vol. 18, Issue 5
  • DOI: 10.1007/s00792-014-0664-7

Gifted microbes for genome mining and natural product discovery
journal, August 2016


Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer
journal, March 2014

  • Wrighton, Kelly C.; Castelle, Cindy J.; Wilkins, Michael J.
  • The ISME Journal, Vol. 8, Issue 7
  • DOI: 10.1038/ismej.2013.249

Aquifer environment selects for microbial species cohorts in sediment and groundwater
journal, February 2015

  • Hug, Laura A.; Thomas, Brian C.; Brown, Christopher T.
  • The ISME Journal, Vol. 9, Issue 8
  • DOI: 10.1038/ismej.2015.2

Major bacterial lineages are essentially devoid of CRISPR-Cas viral defence systems
journal, February 2016

  • Burstein, David; Sun, Christine L.; Brown, Christopher T.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms10613

Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system
journal, October 2016

  • Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms13219

Recent advances in genomic DNA sequencing of microbial species from single cells
journal, August 2014

  • Lasken, Roger S.; McLean, Jeffrey S.
  • Nature Reviews Genetics, Vol. 15, Issue 9
  • DOI: 10.1038/nrg3785

Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations
journal, September 2018

  • Castelle, Cindy J.; Brown, Christopher T.; Anantharaman, Karthik
  • Nature Reviews Microbiology, Vol. 16, Issue 10
  • DOI: 10.1038/s41579-018-0076-2

Single sample resolution of rare microbial dark matter in a marine invertebrate metagenome
journal, September 2016

  • Miller, Ian J.; Weyna, Theodore R.; Fong, Stephen S.
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep34362

Unusual respiratory capacity and nitrogen metabolism in a Parcubacterium (OD1) of the Candidate Phyla Radiation
journal, January 2017

  • Castelle, Cindy J.; Brown, Christopher T.; Thomas, Brian C.
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep40101

Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle
journal, December 2014

  • He, Xuesong; McLean, Jeffrey S.; Edlund, Anna
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 1
  • DOI: 10.1073/pnas.1419038112

Novel approaches in function-driven single-cell genomics
journal, June 2017


The complete genome sequence for putative H 2 - and S-oxidizer C andidatus Sulfuricurvum sp., assembled de novo from an aquifer-derived metagenome : Complete genome of
journal, April 2014

  • Handley, Kim M.; Bartels, Daniela; O'Loughlin, Edward J.
  • Environmental Microbiology, Vol. 16, Issue 11
  • DOI: 10.1111/1462-2920.12453

Identification and Resolution of Microdiversity through Metagenomic Sequencing of Parallel Consortia
journal, October 2015

  • Nelson, William C.; Maezato, Yukari; Wu, Yu-Wei
  • Applied and Environmental Microbiology, Vol. 82, Issue 1
  • DOI: 10.1128/AEM.02274-15

The Prodigal Compound: Return of Ribosyl 1,5-Bisphosphate as an Important Player in Metabolism
journal, December 2018

  • Hove-Jensen, Bjarne; Brodersen, Ditlev E.; Manav, M. Cemre
  • Microbiology and Molecular Biology Reviews, Vol. 83, Issue 1
  • DOI: 10.1128/mmbr.00040-18

Insights Obtained by Culturing Saccharibacteria With Their Bacterial Hosts
journal, February 2020


Recovering complete and draft population genomes from metagenome datasets
journal, March 2016


Comparison of faecal microbiota in Blastocystis-positive and Blastocystis-negative irritable bowel syndrome patients
journal, August 2016


A metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments
journal, September 2018

  • Vavourakis, Charlotte D.; Andrei, Adrian-Stefan; Mehrshad, Maliheh
  • Microbiome, Vol. 6, Issue 1
  • DOI: 10.1186/s40168-018-0548-7

S-layers at second glance? Altiarchaeal grappling hooks (hami) resemble archaeal S-layer proteins in structure and sequence
journal, June 2015

  • Perras, Alexandra K.; Daum, Bertram; Ziegler, Christine
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.00543

Fungi Contribute Critical but Spatially Varying Roles in Nitrogen and Carbon Cycling in Acid Mine Drainage
journal, March 2016

  • Mosier, Annika C.; Miller, Christopher S.; Frischkorn, Kyle R.
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.00238

A Small Number of Low-abundance Bacteria Dominate Plant Species-specific Responses during Rhizosphere Colonization
journal, May 2017


Single-Cell Genomics Reveals a Diverse Metabolic Potential of Uncultivated Desulfatiglans-Related Deltaproteobacteria Widely Distributed in Marine Sediment
journal, September 2018


Phylogenetic clustering of small low nucleic acid-content bacteria across diverse freshwater ecosystems
text, January 2018


Microbial communities across a hillslope‐riparian transect shaped by proximity to the stream, groundwater table, and weathered bedrock
journal, May 2019

  • Lavy, Adi; McGrath, David Geller; Matheus Carnevali, Paula B.
  • Ecology and Evolution, Vol. 9, Issue 12
  • DOI: 10.1002/ece3.5254

Genome-reconstruction for eukaryotes from complex natural microbial communities
journal, March 2018

  • West, Patrick T.; Probst, Alexander J.; Grigoriev, Igor V.
  • Genome Research, Vol. 28, Issue 4
  • DOI: 10.1101/gr.228429.117

Metagenomic analysis of microbial community and function involved in cd-contaminated soil
journal, February 2018


The rise of diversity in metabolic platforms across the Candidate Phyla Radiation
journal, June 2020

  • Jaffe, Alexander L.; Castelle, Cindy J.; Matheus Carnevali, Paula B.
  • BMC Biology, Vol. 18, Issue 1
  • DOI: 10.1186/s12915-020-00804-5

Metabolic network percolation quantifies biosynthetic capabilities across the human oral microbiome
journal, June 2019

  • Bernstein, David B.; Dewhirst, Floyd E.; Segrè, Daniel
  • eLife, Vol. 8
  • DOI: 10.7554/elife.39733

Cohesion: a method for quantifying the connectivity of microbial communities
journal, July 2017

  • Herren, Cristina M.; McMahon, Katherine D.
  • The ISME Journal, Vol. 11, Issue 11
  • DOI: 10.1038/ismej.2017.91

Microbial diversity in European alpine permafrost and active layers
text, January 2016


Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.