Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Quantitative Stable-Isotope Probing (qSIP) with Metagenomics Links Microbial Physiology and Activity to Soil Moisture in Mediterranean-Climate Grassland Ecosystems

Journal Article · · mSystems
 [1];  [1];  [2];  [3];  [3];  [4];  [3];  [4];  [4];  [2];  [1];  [1];  [2];  [1];  [5];  [1]
  1. University of California, Berkeley, CA (United States)
  2. The Ohio State University, Columbus, OH (United States)
  3. Northern Arizona University, Flagstaff, AZ (United States)
  4. Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
  5. Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); University of California, Merced, CA (United States)

The growth and physiology of soil microorganisms, which play vital roles in biogeochemical cycling, are shaped by both current and historical soil environmental conditions. Here, we developed and applied a genome-resolved metagenomic implementation of quantitative stable isotope probing (qSIP) with an H218O labeling experiment to identify actively growing soil microorganisms and their genomic capacities. qSIP enabled measurement of taxon-specific growth because isotopic incorporation into microbial DNA requires production of new genome copies. We studied three Mediterranean grassland soils across a rainfall gradient to evaluate the hypothesis that historic precipitation levels are an important factor controlling trait selection. We used qSIP-informed genome-resolved metagenomics to resolve the active subset of soil community members and identify their characteristic ecophysiological traits. Higher year-round precipitation levels correlated with higher activity and growth rates of flagellar motile microorganisms. In addition to heavily isotopically labeled bacteria, we identified abundant isotope-labeled phages, suggesting phage-induced cell lysis likely contributed to necromass production at all three sites. Further, there was a positive correlation between phage activity and the activity of putative phage hosts. Contrary to our expectations, the capacity to decompose the diverse complex carbohydrates common in soil organic matter or oxidize methanol and carbon monoxide were broadly distributed across active and inactive bacteria in all three soils, implying that these traits are not highly selected for by historical precipitation.

Research Organization:
Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Organization:
USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC52-07NA27344
OSTI ID:
2575211
Report Number(s):
LLNL--JRNL-835074
Journal Information:
mSystems, Journal Name: mSystems Journal Issue: 6 Vol. 7; ISSN 2379-5077
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (70)

Estimating taxon‐specific population dynamics in diverse microbial communities journal January 2018
tRNAscan-SE: Searching for tRNA Genes in Genomic Sequences book January 2019
Dynamics of 18O Incorporation from H 2 18O into Soil Microbial DNA journal March 2011
Soil Moisture and pH Control Relative Contributions of Fungi and Bacteria to N2O Production journal September 2014
Marine DNA Viral Macro- and Microdiversity from Pole to Pole journal May 2019
The Gut Virome Database Reveals Age-Dependent Patterns of Virome Diversity in the Human Gut journal November 2020
Microbial physiology and necromass regulate agricultural soil carbon accumulation journal December 2015
Prevalent root-derived phenolics drive shifts in microbial community composition and prime decomposition in forest soil journal June 2020
dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication journal July 2017
Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution journal September 2007
Measurement of bacterial replication rates in microbial communities journal November 2016
Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls journal November 2016
Binning metagenomic contigs by coverage and composition journal September 2014
DADA2: High-resolution sample inference from Illumina amplicon data journal May 2016
The importance of anabolism in microbial control over soil carbon storage journal July 2017
Embracing the unknown: disentangling the complexities of the soil microbiome journal August 2017
Phylogenetic conservatism of thermal traits explains dispersal limitation and genomic differentiation of Streptomyces sister-taxa journal June 2018
Bacterial contributions to delignification and lignocellulose degradation in forest soils with metagenomic and quantitative stable isotope probing journal September 2018
Quantifying population-specific growth in benthic bacterial communities under low oxygen using H218O journal February 2019
Stable isotope probing and metagenomics highlight the effect of plants on uncultured phenanthrene-degrading bacterial consortium in polluted soil journal March 2019
Niche differentiation is spatially and temporally regulated in the rhizosphere journal January 2020
Benchmarking microbial growth rate predictions from metagenomes journal September 2020
Taxon-specific microbial growth and mortality patterns reveal distinct temporal population responses to rewetting in a California grassland soil journal March 2020
Probing the active fraction of soil microbiomes using BONCAT-FACS journal June 2019
The distinction of CPR bacteria from other bacteria based on protein family content journal September 2019
Host-linked soil viral ecology along a permafrost thaw gradient 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
Scientists’ warning to humanity: microorganisms and climate change journal June 2019
Life and death in the soil microbiome: how ecological processes influence biogeochemistry journal February 2022
Genome-centric view of carbon processing in thawing permafrost journal July 2018
Phenolic acid-degrading Paraburkholderia prime decomposition in forest soil journal March 2021
The diversity and biogeography of soil bacterial communities journal January 2006
Poplar phyllosphere harbors disparate isoprene-degrading bacteria journal November 2018
Global-level population genomics reveals differential effects of geography and phylogeny on horizontal gene transfer in soil bacteria journal July 2019
Metatranscriptomic reconstruction reveals RNA viruses with the potential to shape carbon cycling in soil journal November 2019
Search and clustering orders of magnitude faster than BLAST journal August 2010
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph journal January 2015
MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets journal October 2015
WIsH: who is the host? Predicting prokaryotic hosts from metagenomic phage contigs journal July 2017
DRAM for distilling microbial metabolism to automate the curation of microbiome function journal August 2020
KEGG as a reference resource for gene and protein annotation journal October 2015
antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline journal April 2019
The ecology of heterogeneity: soil bacterial communities and C dynamics journal March 2020
Latitude delineates patterns of biogeography in terrestrial Streptomyces: Biogeography of Streptomyces journal July 2016
Taxonomic patterns in the nitrogen assimilation of soil prokaryotes: Nitrogen assimilation of soil prokaryotes journal March 2018
Microbes drive global soil nitrogen mineralization and availability journal January 2019
A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems: Global soil microbial biomass C, N and P journal December 2012
A Predator Unmasked: Life Cycle of Bdellovibrio bacteriovorus from a Genomic Perspective journal January 2004
A global atlas of the dominant bacteria found in soil journal January 2018
Quantitative Microbial Ecology through Stable Isotope Probing journal August 2015
Microbial rRNA Synthesis and Growth Compared through Quantitative Stable Isotope Probing with H 2 18 O journal February 2018
Relationship between Desiccation and Exopolysaccharide Production in a Soil Pseudomonas sp journal January 1992
The Functional Significance of Bacterial Predators journal April 2021
Stable-Isotope-Informed, Genome-Resolved Metagenomics Uncovers Potential Cross-Kingdom Interactions in Rhizosphere Soil journal October 2021
Measurement Error and Resolution in Quantitative Stable Isotope Probing: Implications for Experimental Design journal August 2020
Metagenomics and Quantitative Stable Isotope Probing Offer Insights into Metabolism of Polycyclic Aromatic Hydrocarbon Degraders in Chronically Polluted Seawater journal June 2021
Viruses in Soil Ecosystems: An Unknown Quantity Within an Unexplored Territory journal September 2017
Prodigal: prokaryotic gene recognition and translation initiation site identification journal March 2010
Simulating metagenomic stable isotope probing datasets with MetaSIPSim journal January 2020
Stable isotope informed genome-resolved metagenomics reveals that Saccharibacteria utilize microbially-processed plant-derived carbon journal July 2018
MetaWRAP—a flexible pipeline for genome-resolved metagenomic data analysis journal September 2018
Active virus-host interactions at sub-freezing temperatures in Arctic peat soil journal October 2021
Minnesota peat viromes reveal terrestrial and aquatic niche partitioning for local and global viral populations journal November 2021
A Parsimony Approach to Biological Pathway Reconstruction/Inference for Genomes and Metagenomes journal August 2009
A systematic pipeline for classifying bacterial operons reveals the evolutionary landscape of biofilm machineries journal April 2020
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data journal April 2013
Distance-Based Redundancy Analysis: Testing Multispecies Responses in Multifactorial Ecological Experiments journal February 1999
Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone journal January 2016
MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies journal January 2019
VirSorter: mining viral signal from microbial genomic data journal January 2015

Similar Records

The Microbial Ecology of Nutrient Feedbacks in Soil
Technical Report · Sun Nov 16 23:00:00 EST 2025 · OSTI ID:3003128

Related Subjects