DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Composition and metabolism of microbial communities in soil pores

Journal Article · · Nature Communications
ORCiD logo [1]; ORCiD logo [2];  [2];  [2];  [3]; ORCiD logo [4];  [5]
  1. Michigan State University, East Lansing, MI (United States); Michigan State University Department of Plant, Soil and Microbial Sciences
  2. Michigan State University, East Lansing, MI (United States)
  3. University of Göttingen (Germany)
  4. Michigan State University, East Lansing, MI (United States); Michigan State University, Hickory Corners, MI (United States)
  5. Helmholtz Centre for Environmental Research, Halle (Germany)

Delineation of microbial habitats within the soil matrix and characterization of their environments and metabolic processes are crucial to understand soil functioning, yet their experimental identification remains persistently limited. We combined single- and triple-energy X-ray computed microtomography with pore specific allocation of 13C labeled glucose and subsequent stable isotope probing to demonstrate how long-term disparities in vegetation history modify spatial distribution patterns of soil pore and particulate organic matter drivers of microbial habitats, and to probe bacterial communities populating such habitats. Here we show striking differences between large (30-150 µm Ø) and small (4-10 µm Ø) soil pores in (i) microbial diversity, composition, and life-strategies, (ii) responses to added substrate, (iii) metabolic pathways, and (iv) the processing and fate of labile C. We propose a microbial habitat classification concept based on biogeochemical mechanisms and localization of soil processes and also suggests interventions to mitigate the environmental consequences of agricultural management.

Research Organization:
Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF)
Grant/Contract Number:
SC0018409; AC02-06CH11357
OSTI ID:
2370491
Journal Information:
Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 15; ISSN 2041-1723
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English

References (106)

Hotspots of soil N2O emission enhanced through water absorption by plant residue journal June 2017
KEGG as a reference resource for gene and protein annotation journal October 2015
Plant diversity effects on soil microorganisms support the singular hypothesis journal February 2010
Pore distances of particulate organic matter predict N2O emissions from intact soil at moist conditions journal January 2023
Effect of plant diversity on the diversity of soil organic compounds journal February 2017
Dynamics of Microbial Growth and Coexistence on Variably Saturated Rough Surfaces journal April 2009
Standard Soil Methods for Long-Term Ecological Research book October 1999
Cover crop influence on pore size distribution and biopore dynamics: Enumerating root and soil faunal effects journal August 2022
An extraction method for measuring soil microbial biomass C journal January 1987
Strong shifts in microbial community structure are associated with increased litter input rather than temperature in High Arctic soils journal December 2020
What do we know about soil carbon destabilization? journal July 2019
Differences in soluble organic carbon chemistry in pore waters sampled from different pore size domains journal April 2017
An Improved DNA Extraction Method Using Skim Milk from Soils That Strongly Adsorb DNA journal January 2004
A Parsimony Approach to Biological Pathway Reconstruction/Inference for Genomes and Metagenomes journal August 2009
Pore architecture and particulate organic matter in soils under monoculture switchgrass and restored prairie in contrasting topography journal November 2021
The science and semantics of "soil organic matter stabilization" other March 2022
Soil-structure development including seasonal dynamics in a long-term fertilization experiment journal March 2011
Plant Diversity, soil Microbial Communities, and Ecosystem Function: are There any Links? journal August 2003
Xylanase, invertase and protease at the soil–litter interface of a loamy sand journal July 1999
microeco: an R package for data mining in microbial community ecology journal December 2020
The physical structure of soil: Determinant and consequence of trophic interactions journal September 2020
Low Pore Connectivity Increases Bacterial Diversity in Soil journal April 2010
When metagenomics meets stable-isotope probing: progress and perspectives journal April 2010
Incorporation of 13C labelled glucose into soil microorganisms of grassland: Effects of fertilizer addition and plant functional group composition journal February 2014
Analysis of Messy Data Volume 1 book March 2009
Microbial spatial footprint as a driver of soil carbon stabilization journal July 2019
Aquatic habitats and diffusion constraints affecting microbial coexistence in unsaturated porous media: MICROBIAL ACTIVITY IN UNSATURATED POROUS MEDIA journal August 2005
Microbial hotspots and hot moments in soil: Concept & review journal April 2015
Interactions among soil texture, pore structure, and labile carbon influence soil carbon gains journal November 2023
Responses of the bacterial and fungal biomass in a grassland soil to multi-year applications of dairy manure slurry and fertilizer journal April 2005
Carbon mineralisation in soil adjacent to plant residues of contrasting biochemical quality journal January 2003
Why are some microbes more ubiquitous than others? Predicting the habitat breadth of soil bacteria journal April 2014
The interaction between wheat roots and soil pores in structured field soil journal October 2020
3D geometric structures and biological activity: Application to microbial soil organic matter decomposition in pore space journal September 2008
Rhizosphere size and shape: Temporal dynamics and spatial stationarity journal August 2019
Intra-aggregate Pore Structure Influences Phylogenetic Composition of Bacterial Community in Macroaggregates journal January 2014
The role of multiple global change factors in driving soil functions and microbial biodiversity journal November 2019
Plant diversity increases soil microbial activity and soil carbon storage journal April 2015
A physiological method for the quantitative measurement of microbial biomass in soils journal January 1978
Correlative Imaging Reveals Holistic View of Soil Microenvironments journal December 2018
Quantification of soil structure based on Minkowski functions journal October 2010
BoneJ: Free and extensible bone image analysis in ImageJ journal December 2010
Central Role of the Trehalose Biosynthesis Pathway in the Pathogenesis of Human Fungal Infections: Opportunities and Challenges for Therapeutic Development journal March 2017
Soil particulate organic matter increases under perennial bioenergy crop agriculture journal October 2017
The ecology of heterogeneity: soil bacterial communities and C dynamics journal March 2020
The role of soil in regulation of climate journal August 2021
PICRUSt2 for prediction of metagenome functions journal June 2020
The microbiome structure of decomposing plant leaves in soil depends on plant species, soil pore sizes, and soil moisture content journal August 2023
Fiji: an open-source platform for biological-image analysis journal June 2012
ilastik: interactive machine learning for (bio)image analysis journal September 2019
Inputs of root-derived carbon into soil and its losses are associated with pore-size distributions journal March 2022
Theory of microbial coexistence in promoting soil–plant ecosystem health journal August 2021
Soil pH and Soil Acidity book January 1996
Spatial organization of bacterial populations in response to oxygen and carbon counter-gradients in pore networks journal February 2018
A global atlas of the dominant bacteria found in soil journal January 2018
Fungal colonization in soils with different management histories: modeling growth in three-dimensional pore volumes journal June 2011
Microscale spatiotemporal patterns of water, soil organic carbon, and enzymes in plant litter detritusphere journal October 2023
Long-term study of root biomass in a biodiversity experiment reveals shifts in diversity effects over time journal June 2014
Physical constraints affecting bacterial habitats and activity in unsaturated porous media – a review journal June 2007
Partitioning sources of CO2 emission after soil wetting using high-resolution observations and minimal models journal April 2020
Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities journal October 2009
New Approach to Measure Soil ParticulateOrganic Matter in Intact Samples Using X-ray Computed Microtomography journal January 2014
Influence of Pore Characteristics on the Fate and Distribution of Newly Added Carbon journal June 2018
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data journal April 2013
Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform journal June 2013
Biophysical processes supporting the diversity of microbial life in soil journal August 2017
Soil pore size distribution shaped not only compositions but also networks of the soil microbial community journal February 2022
Roots compact the surrounding soil depending on the structures they encounter journal November 2019
Regulation of soil organic C mineralisation at the pore scale journal February 2013
Mass‐balance approach to quantify water distribution in soils based on X‐ray computed tomography images journal July 2020
Role of Pore Size Location in Determining Bacterial Activity during Predation by Protozoa in Soil. journal January 1995
Efficient comparative phylogenetics on large trees journal October 2017
Microbial diversity affects self-organization of the soil–microbe system with consequences for function journal October 2011
Decoupling function and taxonomy in the global ocean microbiome journal September 2016
High-resolution synchrotron imaging shows that root hairs influence rhizosphere soil structure formation journal July 2017
Shifts in pore connectivity from precipitation versus groundwater rewetting increases soil carbon loss after drought journal November 2017
Carbon, nitrogen and microbial gradients induced by plant residues decomposing in soil journal December 1999
Short-term changes in the spatial distribution of microorganisms in soil aggregates as affected by glucose addition journal November 2001
Glutamate dehydrogenase and glutamine synthetase are regulated in response to nitrogen availability in Myocbacterium smegmatis journal January 2010
Effect of substrate location in soil and soil pore-water regime on carbon turnover journal January 1993
EPA-ng: Massively Parallel Evolutionary Placement of Genetic Sequences journal September 2018
Revealing pore connectivity across scales and resolutions with X‐ray CT journal April 2020
Denitrification in Soil Aggregate Analogues-Effect of Aggregate Size and Oxygen Diffusion journal April 2018
Growth Yields in Bacterial Denitrification and Nitrate Ammonification journal January 2007
Genesis and Gappa: processing, analyzing and visualizing phylogenetic (placement) data journal February 2020
Microbe-driven turnover offsets mineral-mediated storage of soil carbon under elevated CO2 journal November 2014
Respiration of 13C-Labeled Substrates Added to Soil in the Field and Subsequent 16S rRNA Gene Analysis of 13C-Labeled Soil DNA journal March 2003
Carbon acquisition ecological strategies to connect soil microbial biodiversity and carbon cycling journal February 2023
circlize implements and enhances circular visualization in R journal June 2014
Simultaneous effects of increasing levels of glucose and oxygen partial pressures on denitrification and dissimilatory nitrate reduction to ammonium in repacked soil cores journal January 1998
Micro-scale determinants of bacterial diversity in soil journal November 2013
Spectroscopy-based isotopic (δ13C) analysis for high spatial resolution of carbon exchange in the rhizosphere journal September 2022
Root phenotypes as modulators of microbial microhabitats journal September 2022
Moisture absorption by plant residue in soil journal April 2018
Understanding the joint impacts of soil architecture and microbial dynamics on soil functions: Insights derived from microscale models journal May 2022
Pore‐scale view of microbial turnover: Combining 14 C imaging, μCT and zymography after adding soluble carbon to soil pores of specific sizes journal August 2020
Modeling ecosystem-scale carbon dynamics in soil: The microbial dimension journal March 2023
Plant root exudates and rhizosphere bacterial communities shift with neighbor context journal September 2022
Manipulation of the soil pore and microbial community structure in soil mesocosm incubation studies journal February 2012
Spatial and temporal evolution of detritusphere hotspots at different soil moistures journal November 2020
Contradicting Geometrical Concepts in Pore Size Analysis Attained with Electron Microscopy and Mercury Intrusion journal December 2008
Toward an Ecological Classification of soil Bacteria journal June 2007
SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB journal November 2007
Are the microbial communities involved in glucose assimilation in paddy soils treated with different fertilization regimes for three years similar? journal March 2018
Carbon mineralisation and pore size classes in undisturbed soil cores journal January 2013
Microbial growth on partially saturated rough surfaces: Simulations in idealized roughness networks: MICROBIAL GROWTH ON ROUGH SURFACES journal February 2007