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Title: Soil Candidate Phyla Radiation Bacteria Encode Components of Aerobic Metabolism and Co-occur with Nanoarchaea in the Rare Biosphere of Rhizosphere Grassland Communities

Journal Article · · mSystems
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]; ORCiD logo [3]; ORCiD logo [4]; ;
  1. Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, California, USA
  2. Nuclear and Chemical Sciences Division, Lawrence Livermore National Laboratory, Livermore, California, USA
  3. Department of Environmental Science, Policy, and Management, University of California, Berkeley, Berkeley, California, USA, Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, California, USA
  4. Department of Environmental Science, Policy, and Management, University of California, Berkeley, Berkeley, California, USA, Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, California, USA, Chan Zuckerberg Biohub, San Francisco, California, USA, Innovative Genomics Institute, University of California, Berkeley, Berkeley, California, USA

Candidate Phyla Radiation (CPR) bacteria and nanoarchaea populate most ecosystems but are rarely detected in soil. We concentrated particles of less than 0.2 μm in size from grassland soil, enabling targeted metagenomic analysis of these organisms, which are almost totally unexplored in largely oxic environments such as soil. We recovered a diversity of CPR bacterial and some archaeal sequences but no sequences from other cellular organisms. The sampled sequences include Doudnabacteria (SM2F11) and Pacearchaeota, organisms rarely reported in soil, as well as Saccharibacteria, Parcubacteria, and Microgenomates. CPR and archaea of the phyla Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, and Nanohaloarchaeota (DPANN) were enriched 100- to 1,000-fold compared to that in bulk soil, in which we estimate each of these organisms comprises approximately 1 to 100 cells per gram of soil. Like most CPR and DPANN sequenced to date, we predict these microorganisms live symbiotic anaerobic lifestyles. However, Saccharibacteria, Parcubacteria, and Doudnabacteria genomes sampled here also harbor ubiquinol oxidase operons that may have been acquired from other bacteria, likely during adaptation to aerobic soil environments. We conclude that CPR bacteria and DPANN archaea are part of the rare soil biosphere and harbor unique metabolic platforms that potentially evolved to live symbiotically under relatively oxic conditions.

Research Organization:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Laboratory Directed Research and Development (LDRD) Program; National Institutes of Health (NIH)
Grant/Contract Number:
SCW1678; AC52-07NA27344; SC0020163; SC0016247; AC02-05CH11231; 18-ERD-041; DP2AI117984
OSTI ID:
1813894
Alternate ID(s):
OSTI ID: 1834749; OSTI ID: 1860646
Report Number(s):
LLNL-JRNL-814549; e01205-20
Journal Information:
mSystems, Journal Name: mSystems Vol. 6 Journal Issue: 4; ISSN 2379-5077
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (24)

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Microbial communities across a hillslope‐riparian transect shaped by proximity to the stream, groundwater table, and weathered bedrock journal May 2019
New Biological Insights Into How Deforestation in Amazonia Affects Soil Microbial Communities Using Metagenomics and Metagenome-Assembled Genomes journal July 2018
Mediterranean grassland soil C–N compound turnover is dependent on rainfall and depth, and is mediated by genomically divergent microorganisms journal May 2019
Estimates of viral abundance in soils are strongly influenced by extraction and enumeration methods journal February 2013
Genome-resolved metagenomics reveals site-specific diversity of episymbiotic CPR bacteria and DPANN archaea in groundwater ecosystems journal January 2021
Bacterial Secondary Metabolite Biosynthetic Potential in Soil Varies with Phylum, Depth, and Vegetation Type journal June 2020
The rise of diversity in metabolic platforms across the Candidate Phyla Radiation journal June 2020
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Complementary Metagenomic Approaches Improve Reconstruction of Microbial Diversity in a Forest Soil journal April 2020
Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale journal May 2021
Socially mediated induction and suppression of antibiosis during bacterial coexistence journal July 2015
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Impact of spatial organization on a novel auxotrophic interaction among soil microbes journal March 2018
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Stable isotope informed genome-resolved metagenomics reveals that Saccharibacteria utilize microbially-processed plant-derived carbon journal July 2018
Exploring Viral Diversity in a Unique South African Soil Habitat journal January 2018
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Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations journal September 2018
Genetic and functional diversity of ubiquitous DNA viruses in selected Chinese agricultural soils journal March 2017
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