Diverse uncultivated ultra-small bacterial cells in groundwater

Luef, Birgit; Frischkorn, Kyle R.; Wrighton, Kelly C.; Holman, Hoi-Ying N.; Birarda, Giovanni; Thomas, Brian C.; Singh, Andrea; Williams, Kenneth H.; Siegerist, Cristina E.; Tringe, Susannah G.; Downing, Kenneth H.; Comolli, Luis R.; Banfield, Jillian F.

doi:10.1038/ncomms7372

Title: Diverse uncultivated ultra-small bacterial cells in groundwater

Journal Article · 27 February 2015 · Nature Communications

DOI: https://doi.org/10.1038/ncomms7372 · OSTI ID:1512171

Luef, Birgit ^[1]; Frischkorn, Kyle R. ^[1]; Wrighton, Kelly C. ^[1]; Holman, Hoi-Ying N. ^[2]; Birarda, Giovanni ^[2]; Thomas, Brian C. ^[1]; Singh, Andrea ^[1]; Williams, Kenneth H. ^[3]; Siegerist, Cristina E. ^[1];

^[4]; Downing, Kenneth H. ^[5]; Comolli, Luis R. ^[5]; Banfield, Jillian F. ^[6]

Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Ecology Dept.
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Geophysics Dept., Earth Sciences Division
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Structural Biology and Imaging Dept., Life Sciences Division
Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Geophysics Dept., Earth Sciences Division; Univ. of California, Berkeley, CA (United States). Dept. of Environmental Science, Policy and Management

Bacteria from phyla lacking cultivated representatives are widespread in natural systems and some have very small genomes. Here we test the hypothesis that these cells are small and thus might be enriched by filtration for coupled genomic and ultrastructural characterization. Metagenomic analysis of groundwater that passed through a ~0.2-μm filter reveals a wide diversity of bacteria from the WWE3, OP11 and OD1 candidate phyla. Cryogenic transmission electron microscopy demonstrates that, despite morphological variation, cells consistently have small cell size (0.009±0.002 μm3). Ultrastructural features potentially related to cell and genome size minimization include tightly packed spirals inferred to be DNA, few densely packed ribosomes and a variety of pili-like structures that might enable inter-organism interactions that compensate for biosynthetic capacities inferred to be missing from genomic data. The results suggest that extremely small cell size is associated with these relatively common, yet little known organisms.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1512171

Journal Information:: Nature Communications, Vol. 6, Issue 1; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 240 works

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Lipid analysis of CO2-rich subsurface aquifers suggests an autotrophy-based deep biosphere with lysolipids enriched in CPR bacteria Probst, Alexander J.; Elling, Felix J.; Castelle, Cindy J. The ISME Journal, Vol. 14, Issue 6 https://doi.org/10.1038/s41396-020-0624-4	journal	March 2020
Major bacterial lineages are essentially devoid of CRISPR-Cas viral defence systems Burstein, David; Sun, Christine L.; Brown, Christopher T. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10613	journal	February 2016
Analysis of five complete genome sequences for members of the class Peribacteria in the recently recognized Peregrinibacteria bacterial phylum Anantharaman, Karthik; Brown, Christopher T.; Burstein, David PeerJ, Vol. 4 https://doi.org/10.7717/peerj.1607	journal	January 2016
Highly divergent ancient gene families in metagenomic samples are compatible with additional divisions of life Lopez, Philippe; Halary, Sébastien; Bapteste, Eric Biology Direct, Vol. 10, Issue 1 https://doi.org/10.1186/s13062-015-0092-3	journal	October 2015
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13219	journal	October 2016
Uncultivated microbes in need of their own taxonomy Konstantinidis, Konstantinos T.; Rosselló-Móra, Ramon; Amann, Rudolf The ISME Journal, Vol. 11, Issue 11 https://doi.org/10.1038/ismej.2017.113	journal	July 2017
Drivers of Bacterial Maintenance and Minimal Energy Requirements Kempes, Christopher P.; van Bodegom, Peter M.; Wolpert, David Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00031	journal	January 2017
Carbon Fixation by Marine Ultrasmall Prokaryotes Lannes, Romain; Olsson-Francis, Karen; Lopez, Philippe Genome Biology and Evolution, Vol. 11, Issue 4 https://doi.org/10.1093/gbe/evz050	journal	March 2019
Changes in the Drinking Water Microbiome: Effects of Water Treatments Along the Flow of Two Drinking Water Treatment Plants in a Urbanized Area, Milan (Italy) Bruno, Antonia; Sandionigi, Anna; Bernasconi, Marzia Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02557	journal	October 2018
Melanosomes and ancient coloration re-examined: A response to Vinther 2015 (DOI 10.1002/bies.201500018) Schweitzer, Mary H.; Lindgren, Johan; Moyer, Alison E. BioEssays, Vol. 37, Issue 11 https://doi.org/10.1002/bies.201500061	journal	October 2015
Nano-Sized and Filterable Bacteria and Archaea: Biodiversity and Function Ghuneim, Lydia-Ann J.; Jones, David L.; Golyshin, Peter N. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01971	journal	August 2018
Genomic signatures and co‐occurrence patterns of the ultra‐small Saccharimonadia (phylum CPR/Patescibacteria) suggest a symbiotic lifestyle Lemos, Leandro N.; Medeiros, Julliane D.; Dini‐Andreote, Francisco Molecular Ecology, Vol. 28, Issue 18 https://doi.org/10.1111/mec.15208	journal	September 2019
Human age and skin physiology shape diversity and abundance of Archaea on skin Moissl-Eichinger, Christine; Probst, Alexander J.; Birarda, Giovanni Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-04197-4	journal	June 2017
Members of the Candidate Phyla Radiation are functionally differentiated by carbon- and nitrogen-cycling capabilities Danczak, R. E.; Johnston, M. D.; Kenah, C. Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0331-1	journal	September 2017
Insights Obtained by Culturing Saccharibacteria With Their Bacterial Hosts Bor, B.; Collins, A. J.; Murugkar, P. P. Journal of Dental Research, Vol. 99, Issue 6 https://doi.org/10.1177/0022034520905792	journal	February 2020
Highly divergent ancient gene families in metagenomic samples are compatible with additional divisions of life Lopez, Philippe; Halary, Sébastien; Bapteste, Eric Biology Direct, Vol. 10, Issue 1 https://doi.org/10.1186/s13062-015-0092-3	journal	October 2015
Rare Microbial Taxa Emerge When Communities Collide: Freshwater and Marine Microbiome Responses to Experimental Seawater Intrusion Rocca, Jennifer D.; Simonin, Marie; Wright, Justin P. bioRxiv https://doi.org/10.1101/550756	posted_content	February 2019
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13219	journal	October 2016
Evolutionary tradeoffs in cellular composition across diverse bacteria Kempes, Christopher P.; Wang, Lawrence; Amend, Jan P. The ISME Journal, Vol. 10, Issue 9 https://doi.org/10.1038/ismej.2016.21	journal	April 2016
Single-cell genomics of co-sorted Nanoarchaeota suggests novel putative host associations and diversification of proteins involved in symbiosis Jarett, Jessica K.; Nayfach, Stephen; Podar, Mircea Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0539-8	journal	September 2018
Unusual biology across a group comprising more than 15% of domain Bacteria Brown, Christopher T.; Hug, Laura A.; Thomas, Brian C. Nature, Vol. 523, Issue 7559 https://doi.org/10.1038/nature14486	journal	June 2015
Minimum information about an uncultivated virus genome (MIUVIG) Roux, Simon; Adriaenssens, Evelien M.; Dutilh, Bas E. ETH Zurich https://doi.org/10.3929/ethz-b-000315358	text	January 2019
Nano-Sized and Filterable Bacteria and Archaea: Biodiversity and Function Ghuneim, Lydia-Ann J.; Jones, David L.; Golyshin, Peter N. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01971	journal	August 2018
Candidate Phyla Radiation Roizmanbacteria From Hot Springs Have Novel and Unexpectedly Abundant CRISPR-Cas Systems Chen, Lin-Xing; Al-Shayeb, Basem; Méheust, Raphaël Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00928	journal	May 2019
Members of the Candidate Phyla Radiation are functionally differentiated by carbon- and nitrogen-cycling capabilities Danczak, R. E.; Johnston, M. D.; Kenah, C. Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0331-1	journal	September 2017
From cultured to uncultured genome sequences: metagenomics and modeling microbial ecosystems Garza, Daniel R.; Dutilh, Bas E. Cellular and Molecular Life Sciences, Vol. 72, Issue 22 https://doi.org/10.1007/s00018-015-2004-1	journal	August 2015
Abundance and Distribution of Microbial Cells and Viruses in an Alluvial Aquifer Pan, Donald; Nolan, Jason; Williams, Kenneth H. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01199	journal	July 2017
Critical biogeochemical functions in the subsurface are associated with bacteria from new phyla and little studied lineages: N- and C-cycling organisms in the subsurface Hug, Laura A.; Thomas, Brian C.; Sharon, Itai Environmental Microbiology, Vol. 18, Issue 1 https://doi.org/10.1111/1462-2920.12930	journal	July 2015
Microbial metagenomes from three aquifers in the Fennoscandian shield terrestrial deep biosphere reveal metabolic partitioning among populations Wu, Xiaofen; Holmfeldt, Karin; Hubalek, Valerie The ISME Journal, Vol. 10, Issue 5 https://doi.org/10.1038/ismej.2015.185	journal	October 2015
Ultrastructure of compacted DNA in cyanobacteria by high-voltage cryo-electron tomography Murata, Kazuyoshi; Hagiwara, Sayuri; Kimori, Yoshitaka Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep34934	journal	October 2016
Measurement of bacterial replication rates in microbial communities Brown, Christopher T.; Olm, Matthew R.; Thomas, Brian C. Nature Biotechnology, Vol. 34, Issue 12 https://doi.org/10.1038/nbt.3704	journal	November 2016
Exaggerated expectations in ancient starch research and the need for new taphonomic and authenticity criteria Mercader, Julio; Akeju, Tolutope; Brown, Melisa FACETS, Vol. 3, Issue 1 https://doi.org/10.1139/facets-2017-0126	journal	January 2018
Quorum Sensing Modulates the Epibiotic-Parasitic Relationship Between Actinomyces odontolyticus and Its Saccharibacteria epibiont, a Nanosynbacter lyticus Strain, TM7x Bedree, Joseph K.; Bor, Batbileg; Cen, Lujia Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02049	journal	September 2018
Characterisation of a stable laboratory co-culture of acidophilic nanoorganisms Krause, Susanne; Bremges, Andreas; Münch, Philipp C. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-03315-6	journal	June 2017
Aquifer environment selects for microbial species cohorts in sediment and groundwater Hug, Laura A.; Thomas, Brian C.; Brown, Christopher T. The ISME Journal, Vol. 9, Issue 8 https://doi.org/10.1038/ismej.2015.2	journal	February 2015
Drivers of Bacterial Maintenance and Minimal Energy Requirements Kempes, Christopher P.; van Bodegom, Peter M.; Wolpert, David Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00031	journal	January 2017
Macrocyclic peptide-based inhibition and imaging of hepatocyte growth factor Sakai, Katsuya; Passioura, Toby; Sato, Hiroki Nature Chemical Biology, Vol. 15, Issue 6 https://doi.org/10.1038/s41589-019-0285-7	journal	May 2019
Aedes spp. and Their Microbiota: A Review Scolari, Francesca; Casiraghi, Maurizio; Bonizzoni, Mariangela Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02036	journal	September 2019
High reactivity of deep biota under anthropogenic CO2 injection into basalt Trias, Rosalia; Ménez, Bénédicte; le Campion, Paul Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01288-8	journal	October 2017
Ultrastructure of compacted DNA in cyanobacteria by high-voltage cryo-electron tomography Murata, Kazuyoshi; Hagiwara, Sayuri; Kimori, Yoshitaka Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep34934	journal	October 2016
Microbial metagenomes from three aquifers in the Fennoscandian shield terrestrial deep biosphere reveal metabolic partitioning among populations Wu, Xiaofen; Holmfeldt, Karin; Hubalek, Valerie The ISME Journal, Vol. 10, Issue 5 https://doi.org/10.1038/ismej.2015.185	journal	October 2015
Growth promotion and inhibition induced by interactions of groundwater bacteria Geesink, Patricia; Tyc, Olaf; Küsel, Kirsten FEMS Microbiology Ecology, Vol. 94, Issue 11 https://doi.org/10.1093/femsec/fiy164	journal	August 2018
Abundance and Distribution of Microbial Cells and Viruses in an Alluvial Aquifer Pan, Donald; Nolan, Jason; Williams, Kenneth H. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01199	journal	July 2017
Phylogenetic clustering of small low nucleic acid-content bacteria across diverse freshwater ecosystems Proctor, Caitlin R.; Besmer, Michael D.; Langenegger, Timon ETH Zurich https://doi.org/10.3929/ethz-b-000242996	text	January 2018
Genome-resolved metagenomics identifies genetic mobility, metabolic interactions, and unexpected diversity in perchlorate-reducing communities Barnum, Tyler P.; Figueroa, Israel A.; Carlström, Charlotte I. The ISME Journal, Vol. 12, Issue 6 https://doi.org/10.1038/s41396-018-0081-5	journal	February 2018
Comparative Genomics of Candidate Phylum TM6 Suggests That Parasitism Is Widespread and Ancestral in This Lineage Yeoh, Yun Kit; Sekiguchi, Yuji; Parks, Donovan H. Molecular Biology and Evolution, Vol. 33, Issue 4 https://doi.org/10.1093/molbev/msv281	journal	November 2015
The distinction of CPR bacteria from other bacteria based on protein family content Méheust, Raphaël; Burstein, David; Castelle, Cindy J. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12171-z	journal	September 2019
Accurate and complete genomes from metagenomes Chen, Lin-Xing; Anantharaman, Karthik; Shaiber, Alon Genome Research, Vol. 30, Issue 3 https://doi.org/10.1101/gr.258640.119	journal	March 2020
On the translocation of bacteria and their lipopolysaccharides between blood and peripheral locations in chronic, inflammatory diseases: the central roles of LPS and LPS-induced cell death Kell, Douglas B.; Pretorius, Etheresia Integrative Biology, Vol. 7, Issue 11 https://doi.org/10.1039/c5ib00158g	journal	September 2015
Sizing up the bacterial cell cycle Willis, Lisa; Huang, Kerwyn Casey Nature Reviews Microbiology, Vol. 15, Issue 10 https://doi.org/10.1038/nrmicro.2017.79	journal	August 2017
Bottled aqua incognita: microbiota assembly and dissolved organic matter diversity in natural mineral waters Lesaulnier, Celine C.; Herbold, Craig W.; Pelikan, Claus Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0344-9	journal	September 2017
Additional file 1 of Genome-centric metagenomics reveals the host-driven dynamics and ecological role of CPR bacteria in an activated sludge system Wang, Yulin; Zhang, Yulin; Hu, Yu figshare https://doi.org/10.6084/m9.figshare.22619041	dataset	January 2023