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Title: Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone

Abstract

Annually, half of all plant-derived carbon is added to soil where it is microbially respired to CO 2. However, understanding of the microbiology of this process is limited because most culture-independent methods cannot link metabolic processes to the organisms present, and this link to causative agents is necessary to predict the results of perturbations on the system. We collected soil samples at two sub-root depths (10–20 cm and 30–40 cm) before and after a rainfall-driven nutrient perturbation event in a Northern California grassland that experiences a Mediterranean climate. From ten samples, we reconstructed 198 metagenome-assembled genomes that represent all major phylotypes. We also quantified 6,835 proteins and 175 metabolites and showed that after the rain event the concentrations of many sugars and amino acids approach zero at the base of the soil profile. Unexpectedly, the genomes of novel members of the Gemmatimonadetes and Candidate Phylum Rokubacteria phyla encode pathways for methylotrophy. We infer that these abundant organisms contribute substantially to carbon turnover in the soil, given that methylotrophy proteins were among the most abundant proteins in the proteome. Previously undescribed Bathyarchaeota and Thermoplasmatales archaea are abundant in deeper soil horizons and are inferred to contribute appreciably to aromatic amino acid degradation. Manymore » of the other bacteria appear to breakdown other components of plant biomass, as evidenced by the prevalence of various sugar and amino acid transporters and corresponding hydrolyzing machinery in the proteome. Overall, our work provides organism-resolved insight into the spatial distribution of bacteria and archaea whose activities combine to degrade plant-derived organics, limiting the transport of methanol, amino acids and sugars into underlying weathered rock. Finally, the new insights into the soil carbon cycle during an intense period of carbon turnover, including biogeochemical roles to previously little known soil microbes, were made possible via the combination of metagenomics, proteomics, and metabolomics.« less

Authors:
 [1];  [2];  [3];  [1];  [1];  [1];  [2];  [4];  [1];  [5];  [3];  [2];  [6]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Sciences
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. Univ. of California, Santa Cruz, CA (United States). Dept. of Ecology and Evolutionary Biology
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  6. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1354646
Alternate Identifier(s):
OSTI ID: 1378973
Grant/Contract Number:  
AC05-00OR22725; AC02-05CH11231
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
PeerJ
Additional Journal Information:
Journal Volume: 4; Journal ID: ISSN 2167-8359
Publisher:
PeerJ Inc.
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES

Citation Formats

Butterfield, Cristina N., Li, Zhou, Andeer, Peter F., Spaulding, Susan, Thomas, Brian C., Singh, Andrea, Hettich, Robert L., Suttle, Kenwyn B., Probst, Alexander J., Tringe, Susannah G., Northen, Trent, Pan, Chongle, and Banfield, Jillian F. Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone. United States: N. p., 2016. Web. doi:10.7717/peerj.2687.
Butterfield, Cristina N., Li, Zhou, Andeer, Peter F., Spaulding, Susan, Thomas, Brian C., Singh, Andrea, Hettich, Robert L., Suttle, Kenwyn B., Probst, Alexander J., Tringe, Susannah G., Northen, Trent, Pan, Chongle, & Banfield, Jillian F. Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone. United States. doi:10.7717/peerj.2687.
Butterfield, Cristina N., Li, Zhou, Andeer, Peter F., Spaulding, Susan, Thomas, Brian C., Singh, Andrea, Hettich, Robert L., Suttle, Kenwyn B., Probst, Alexander J., Tringe, Susannah G., Northen, Trent, Pan, Chongle, and Banfield, Jillian F. Tue . "Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone". United States. doi:10.7717/peerj.2687. https://www.osti.gov/servlets/purl/1354646.
@article{osti_1354646,
title = {Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone},
author = {Butterfield, Cristina N. and Li, Zhou and Andeer, Peter F. and Spaulding, Susan and Thomas, Brian C. and Singh, Andrea and Hettich, Robert L. and Suttle, Kenwyn B. and Probst, Alexander J. and Tringe, Susannah G. and Northen, Trent and Pan, Chongle and Banfield, Jillian F.},
abstractNote = {Annually, half of all plant-derived carbon is added to soil where it is microbially respired to CO2. However, understanding of the microbiology of this process is limited because most culture-independent methods cannot link metabolic processes to the organisms present, and this link to causative agents is necessary to predict the results of perturbations on the system. We collected soil samples at two sub-root depths (10–20 cm and 30–40 cm) before and after a rainfall-driven nutrient perturbation event in a Northern California grassland that experiences a Mediterranean climate. From ten samples, we reconstructed 198 metagenome-assembled genomes that represent all major phylotypes. We also quantified 6,835 proteins and 175 metabolites and showed that after the rain event the concentrations of many sugars and amino acids approach zero at the base of the soil profile. Unexpectedly, the genomes of novel members of the Gemmatimonadetes and Candidate Phylum Rokubacteria phyla encode pathways for methylotrophy. We infer that these abundant organisms contribute substantially to carbon turnover in the soil, given that methylotrophy proteins were among the most abundant proteins in the proteome. Previously undescribed Bathyarchaeota and Thermoplasmatales archaea are abundant in deeper soil horizons and are inferred to contribute appreciably to aromatic amino acid degradation. Many of the other bacteria appear to breakdown other components of plant biomass, as evidenced by the prevalence of various sugar and amino acid transporters and corresponding hydrolyzing machinery in the proteome. Overall, our work provides organism-resolved insight into the spatial distribution of bacteria and archaea whose activities combine to degrade plant-derived organics, limiting the transport of methanol, amino acids and sugars into underlying weathered rock. Finally, the new insights into the soil carbon cycle during an intense period of carbon turnover, including biogeochemical roles to previously little known soil microbes, were made possible via the combination of metagenomics, proteomics, and metabolomics.},
doi = {10.7717/peerj.2687},
journal = {PeerJ},
number = ,
volume = 4,
place = {United States},
year = {Tue Nov 08 00:00:00 EST 2016},
month = {Tue Nov 08 00:00:00 EST 2016}
}

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Cited by: 6 works
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Works referenced in this record:

Search and clustering orders of magnitude faster than BLAST
journal, August 2010


MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340