skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Exometabolite niche partitioning among sympatric soil bacteria

Abstract

© 2015 Macmillan Publishers Limited. All rights reserved. Soils are arguably the most microbially diverse ecosystems. Physicochemical properties have been associated with the maintenance of this diversity. Yet, the role of microbial substrate specialization is largely unexplored since substrate utilization studies have focused on simple substrates, not the complex mixtures representative of the soil environment. Here we examine the exometabolite composition of desert biological soil crusts (biocrusts) and the substrate preferences of seven biocrust isolates. The biocrust's main primary producer releases a diverse array of metabolites, and isolates of physically associated taxa use unique subsets of the complex metabolite pool. Individual isolates use only 13-26% of available metabolites, with only 2 out of 470 used by all and 40% not used by any. An extension of this approach to a mesophilic soil environment also reveals high levels of microbial substrate specialization. These results suggest that exometabolite niche partitioning may be an important factor in the maintenance of microbial diversity.

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [7];  [6];  [4];  [4];  [7]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Climate and Ecosystems Sciences Division; Univ. of California, Berkeley, CA (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division; Arizona State Univ., Mesa, AZ (United States)
  4. Arizona State Univ., Mesa, AZ (United States)
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Climate and Ecosystems Sciences Division; Vrije Univ., Amsterdam (Netherlands)
  6. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Climate and Ecosystems Sciences Division
  7. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division; DOE Joint Genome Institute, Walnut Creek, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1256039
Alternate Identifier(s):
OSTI ID: 1513785
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Baran, Richard, Brodie, Eoin L., Mayberry-Lewis, Jazmine, Hummel, Eric, Da Rocha, Ulisses Nunes, Chakraborty, Romy, Bowen, Benjamin P., Karaoz, Ulas, Cadillo-Quiroz, Hinsby, Garcia-Pichel, Ferran, and Northen, Trent R. Exometabolite niche partitioning among sympatric soil bacteria. United States: N. p., 2015. Web. https://doi.org/10.1038/ncomms9289.
Baran, Richard, Brodie, Eoin L., Mayberry-Lewis, Jazmine, Hummel, Eric, Da Rocha, Ulisses Nunes, Chakraborty, Romy, Bowen, Benjamin P., Karaoz, Ulas, Cadillo-Quiroz, Hinsby, Garcia-Pichel, Ferran, & Northen, Trent R. Exometabolite niche partitioning among sympatric soil bacteria. United States. https://doi.org/10.1038/ncomms9289
Baran, Richard, Brodie, Eoin L., Mayberry-Lewis, Jazmine, Hummel, Eric, Da Rocha, Ulisses Nunes, Chakraborty, Romy, Bowen, Benjamin P., Karaoz, Ulas, Cadillo-Quiroz, Hinsby, Garcia-Pichel, Ferran, and Northen, Trent R. Tue . "Exometabolite niche partitioning among sympatric soil bacteria". United States. https://doi.org/10.1038/ncomms9289. https://www.osti.gov/servlets/purl/1256039.
@article{osti_1256039,
title = {Exometabolite niche partitioning among sympatric soil bacteria},
author = {Baran, Richard and Brodie, Eoin L. and Mayberry-Lewis, Jazmine and Hummel, Eric and Da Rocha, Ulisses Nunes and Chakraborty, Romy and Bowen, Benjamin P. and Karaoz, Ulas and Cadillo-Quiroz, Hinsby and Garcia-Pichel, Ferran and Northen, Trent R.},
abstractNote = {© 2015 Macmillan Publishers Limited. All rights reserved. Soils are arguably the most microbially diverse ecosystems. Physicochemical properties have been associated with the maintenance of this diversity. Yet, the role of microbial substrate specialization is largely unexplored since substrate utilization studies have focused on simple substrates, not the complex mixtures representative of the soil environment. Here we examine the exometabolite composition of desert biological soil crusts (biocrusts) and the substrate preferences of seven biocrust isolates. The biocrust's main primary producer releases a diverse array of metabolites, and isolates of physically associated taxa use unique subsets of the complex metabolite pool. Individual isolates use only 13-26% of available metabolites, with only 2 out of 470 used by all and 40% not used by any. An extension of this approach to a mesophilic soil environment also reveals high levels of microbial substrate specialization. These results suggest that exometabolite niche partitioning may be an important factor in the maintenance of microbial diversity.},
doi = {10.1038/ncomms9289},
journal = {Nature Communications},
number = ,
volume = 6,
place = {United States},
year = {2015},
month = {9}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 19 works
Citation information provided by
Web of Science

Figures / Tables:

Figure 1 Figure 1: Two scenarios for substrate preferences in sympatric soil bacteria. (a) Metabolites have a weak effect in supporting diversity due to substrate generalism among heterotrophs. (b) Metabolite diversity contributes to niche differentiation and supports diversity due to strong substrate preferences among heterotrophs.

Save / Share:

Works referenced in this record:

Reduction of (per)chlorate by a novel organism isolated from paper mill waste
journal, August 1999


Microbial competition
journal, August 1981


Phylogenetic and Morphological Diversity of Cyanobacteria in Soil Desert Crusts from the Colorado Plateau
journal, April 2001


Metabolic Footprinting of Mutant Libraries to Map Metabolite Utilization to Genotype
journal, October 2012

  • Baran, Richard; Bowen, Benjamin P.; Price, Morgan N.
  • ACS Chemical Biology, Vol. 8, Issue 1
  • DOI: 10.1021/cb300477w

Untargeted metabolic footprinting reveals a surprising breadth of metabolite uptake and release by Synechococcus sp. PCC 7002
journal, January 2011

  • Baran, Richard; Bowen, Benjamin P.; Northen, Trent R.
  • Molecular BioSystems, Vol. 7, Issue 12
  • DOI: 10.1039/c1mb05196b

Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages
journal, July 2014


Nutrient requirements for growth of the extreme oligotroph ‘Candidatus Pelagibacter ubique’ HTCC1062 on a defined medium
journal, October 2012

  • Carini, Paul; Steindler, Laura; Beszteri, Sara
  • The ISME Journal, Vol. 7, Issue 3
  • DOI: 10.1038/ismej.2012.122

Metabolite Identification in Synechococcus sp. PCC 7002 Using Untargeted Stable Isotope Assisted Metabolite Profiling
journal, November 2010

  • Baran, Richard; Bowen, Benjamin P.; Bouskill, Nicholas J.
  • Analytical Chemistry, Vol. 82, Issue 21
  • DOI: 10.1021/ac1020112

Temperature Drives the Continental-Scale Distribution of Key Microbes in Topsoil Communities
journal, June 2013

  • Garcia-Pichel, Ferran; Loza, Virginia; Marusenko, Yevgeniy
  • Science, Vol. 340, Issue 6140
  • DOI: 10.1126/science.1236404

Nutritional flexibility of oligotrophic and copiotrophic Antarctic bacteria with respect to organic substrates
journal, January 1989


Growing Unculturable Bacteria
journal, June 2012


Hydration dynamics promote bacterial coexistence on rough surfaces
journal, October 2012


The world at your feet: desert biological soil crusts
journal, May 2003


MassBank: a public repository for sharing mass spectral data for life sciences
journal, July 2010

  • Horai, Hisayuki; Arita, Masanori; Kanaya, Shigehiko
  • Journal of Mass Spectrometry, Vol. 45, Issue 7
  • DOI: 10.1002/jms.1777

Biogeographic patterns in ocean microbes emerge in a neutral agent-based model
journal, September 2014


Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients
journal, December 2011

  • Fierer, Noah; Lauber, Christian L.; Ramirez, Kelly S.
  • The ISME Journal, Vol. 6, Issue 5
  • DOI: 10.1038/ismej.2011.159

Untangling Genomes from Metagenomes: Revealing an Uncultured Class of Marine Euryarchaeota
journal, February 2012


Genome of the Cyanobacterium Microcoleus vaginatusFGP-2, a Photosynthetic Ecosystem Engineer of Arid Land Soil Biocrusts Worldwide
journal, June 2011

  • Starkenburg, S. R.; Reitenga, K. G.; Freitas, T.
  • Journal of Bacteriology, Vol. 193, Issue 17
  • DOI: 10.1128/JB.05138-11

Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009

  • Schloss, P. D.; Westcott, S. L.; Ryabin, T.
  • Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
  • DOI: 10.1128/AEM.01541-09

High Rate of Uptake of Organic Nitrogen Compounds by Prochlorococcus Cyanobacteria as a Key to Their Dominance in Oligotrophic Oceanic Waters
journal, February 2003


Metabolic footprinting and systems biology: the medium is the message
journal, June 2005

  • Kell, Douglas B.; Brown, Marie; Davey, Hazel M.
  • Nature Reviews Microbiology, Vol. 3, Issue 7
  • DOI: 10.1038/nrmicro1177

The Competitive Exclusion Principle
journal, April 1960


Spatial and Resource Factors Influencing High Microbial Diversity in Soil
journal, January 2002


Dormancy contributes to the maintenance of microbial diversity
journal, March 2010

  • Jones, S. E.; Lennon, J. T.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 13
  • DOI: 10.1073/pnas.0912765107

The Use of Carbon Substrate Utilization Patterns in Environmental and Ecological Microbiology
journal, March 1998

  • Konopka, A.; Oliver, L.; Jr., R. F. Turco,
  • Microbial Ecology, Vol. 35, Issue 2
  • DOI: 10.1007/s002489900065

Exometabolomics and MSI: deconstructing how cells interact to transform their small molecule environment
journal, August 2015


Functional Genomics of Novel Secondary Metabolites from Diverse Cyanobacteria Using Untargeted Metabolomics
journal, September 2013

  • Baran, Richard; Ivanova, Natalia; Jose, Nick
  • Marine Drugs, Vol. 11, Issue 10
  • DOI: 10.3390/md11103617

Closely related phytoplankton species produce similar suites of dissolved organic matter
journal, March 2014

  • Becker, Jamie W.; Berube, Paul M.; Follett, Christopher L.
  • Frontiers in Microbiology, Vol. 5
  • DOI: 10.3389/fmicb.2014.00111

Robust Automated Mass Spectra Interpretation and Chemical Formula Calculation Using Mixed Integer Linear Programming
journal, September 2013

  • Baran, Richard; Northen, Trent R.
  • Analytical Chemistry, Vol. 85, Issue 20
  • DOI: 10.1021/ac402180c

Phenotype MicroArrays for High-Throughput Phenotypic Testing and Assay of Gene Function
journal, July 2001


Persistence of soil organic matter as an ecosystem property
journal, October 2011

  • Schmidt, Michael W. I.; Torn, Margaret S.; Abiven, Samuel
  • Nature, Vol. 478, Issue 7367
  • DOI: 10.1038/nature10386

Dynamic cyanobacterial response to hydration and dehydration in a desert biological soil crust
journal, June 2013

  • Rajeev, Lara; da Rocha, Ulisses Nunes; Klitgord, Niels
  • The ISME Journal, Vol. 7, Issue 11
  • DOI: 10.1038/ismej.2013.83

Relevance of ammonium oxidation within biological soil crust communities
journal, January 2005


UPARSE: highly accurate OTU sequences from microbial amplicon reads
journal, August 2013


Resource Partitioning and Sympatric Differentiation Among Closely Related Bacterioplankton
journal, May 2008


Molecular biology of cyanobacterial salt acclimation
journal, January 2011


The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012

  • Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1219

Export of nitrogenous compounds due to incomplete cycling within biological soil crusts of arid lands
journal, March 2007


METLIN: A Metabolite Mass Spectral Database
journal, January 2005


A Hydration-Based Biophysical Index for the Onset of Soil Microbial Coexistence
journal, November 2012


Differential Growth Responses of Soil Bacterial Taxa to Carbon Substrates of Varying Chemical Recalcitrance
journal, January 2011

  • Goldfarb, Katherine C.; Karaoz, Ulas; Hanson, China A.
  • Frontiers in Microbiology, Vol. 2
  • DOI: 10.3389/fmicb.2011.00094

The diversity and biogeography of soil bacterial communities
journal, January 2006

  • Fierer, N.; Jackson, R. B.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 3
  • DOI: 10.1073/pnas.0507535103

Isolation of a significant fraction of non-phototroph diversity from a desert Biological Soil Crust
journal, April 2015

  • Nunes da Rocha, Ulisses; Cadillo-Quiroz, Hinsby; Karaoz, Ulas
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.00277

Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012

  • Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
  • The ISME Journal, Vol. 6, Issue 8
  • DOI: 10.1038/ismej.2012.8

The Community and Phylogenetic Diversity of Biological Soil Crusts in the Colorado Plateau Studied by Molecular Fingerprinting and Intensive Cultivation
journal, May 2006

  • Gundlapally, Sathyanarayana Reddy; Garcia-Pichel, Ferran
  • Microbial Ecology, Vol. 52, Issue 2
  • DOI: 10.1007/s00248-006-9011-6

From Enzymatic Adaptation to Allosteric Transitions
journal, October 1966


Strategies of Mixed Substrate Utilization in Microorganisms [and Discussion]
journal, June 1982

  • Harder, W.; Dijkhuizen, L.; Postgate, J. R.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 297, Issue 1088
  • DOI: 10.1098/rstb.1982.0055

Cyanobacteria produce high levels of ergothioneine
journal, December 2011


Characterization of a Pseudomonas sp. Capable of Aniline Degradation in the Presence of Secondary Carbon Sources †
journal, January 1989


Physiological Diversity and Distributions of Heterotrophic Bacteria in Deep Cretaceous Sediments of the Atlantic Coastal Plain
journal, January 1991

  • Fredrickson, James K.; Balkwill, David L.; Zachara, John M.
  • Applied and Environmental Microbiology, Vol. 57, Issue 2
  • DOI: 10.1128/AEM.57.2.402-411.1991

Observations on the Distinction Between Oligotrophic and Eutrophic Marine Bacteria
journal, January 1984


Purification and properties of unicellular blue-green algae (order Chroococcales).
journal, January 1971


A new medium for the enumeration and subculture of bacteria from potable water.
journal, January 1985


The World at Your Feet: Desert Biological Soil Crusts
journal, May 2003

  • Belnap, Jayne
  • Frontiers in Ecology and the Environment, Vol. 1, Issue 4
  • DOI: 10.2307/3868062

From enzymatic adaptation to allosteric transitions
journal, July 2003


Analysis of immune, microbiota and metabolome maturation in infants in a clinical trial of Lactobacillus paracasei CBA L74-fermented formula
journal, June 2020


    Works referencing / citing this record:

    Applying community ecological theory to maximize productivity of cultivated biocrusts
    journal, August 2017

    • Bowker, Matthew A.; Antoninka, Anita J.; Durham, Rebecca A.
    • Ecological Applications, Vol. 27, Issue 6
    • DOI: 10.1002/eap.1582

    Plant selection initiates alternative successional trajectories in the soil microbial community after disturbance
    journal, March 2019

    • Duhamel, Marie; Wan, Joe; Bogar, Laura M.
    • Ecological Monographs, Vol. 89, Issue 3
    • DOI: 10.1002/ecm.1367

    Biological soil crusts: diminutive communities of potential global importance
    journal, March 2017

    • Ferrenberg, Scott; Tucker, Colin L.; Reed, Sasha C.
    • Frontiers in Ecology and the Environment, Vol. 15, Issue 3
    • DOI: 10.1002/fee.1469

    Biocrust morphology is linked to marked differences in microbial community composition
    journal, October 2017

    • Chilton, Angela M.; Neilan, Brett A.; Eldridge, David J.
    • Plant and Soil, Vol. 429, Issue 1-2
    • DOI: 10.1007/s11104-017-3442-3

    Assessing the influence of soil abiotic and biotic factors on Nostoc commune inoculation success
    journal, August 2019


    Biphasic cellular adaptations and ecological implications of Alteromonas macleodii degrading a mixture of algal polysaccharides
    journal, August 2018


    Predicting metabolic adaptation from networks of mutational paths
    journal, September 2017


    Linking soil biology and chemistry in biological soil crust using isolate exometabolomics
    journal, January 2018


    Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly
    journal, March 2018


    Learning representations of microbe–metabolite interactions
    journal, November 2019

    • Morton, James T.; Aksenov, Alexander A.; Nothias, Louis Felix
    • Nature Methods, Vol. 16, Issue 12
    • DOI: 10.1038/s41592-019-0616-3

    Mixed-Cropping Between Field Pea Varieties Alters Root Bacterial and Fungal Communities
    journal, November 2019


    Metabolic division of labor in microbial systems
    journal, February 2018

    • Tsoi, Ryan; Wu, Feilun; Zhang, Carolyn
    • Proceedings of the National Academy of Sciences, Vol. 115, Issue 10
    • DOI: 10.1073/pnas.1716888115

    Altering biocrusts for an altered climate
    journal, February 2016

    • Young, Kristina E.; Grover, Henry S.; Bowker, Matthew A.
    • New Phytologist, Vol. 210, Issue 1
    • DOI: 10.1111/nph.13910

    Biochar-stimulated plant performance is strongly linked to microbial diversity and metabolic potential in the rhizosphere
    journal, October 2016

    • Kolton, Max; Graber, Ellen R.; Tsehansky, Ludmila
    • New Phytologist, Vol. 213, Issue 3
    • DOI: 10.1111/nph.14253

    Biocrust-forming mosses mitigate the impact of aridity on soil microbial communities in drylands: observational evidence from three continents
    journal, April 2018

    • Delgado-Baquerizo, Manuel; Maestre, Fernando T.; Eldridge, David J.
    • New Phytologist, Vol. 220, Issue 3
    • DOI: 10.1111/nph.15120

    Nursing biocrusts: isolation, cultivation, and fitness test of indigenous cyanobacteria: Nursing biocrust cyanobacteria
    journal, January 2019

    • Giraldo-Silva, Ana; Nelson, Corey; Barger, Nichole N.
    • Restoration Ecology, Vol. 27, Issue 4
    • DOI: 10.1111/rec.12920

    Biofilms 2018: a Diversity of Microbes and Mechanisms
    journal, February 2019

    • Fuqua, Clay; Filloux, Alain; Ghigo, Jean-Marc
    • Journal of Bacteriology, Vol. 201, Issue 18
    • DOI: 10.1128/jb.00118-19

    Large Blooms of Bacillales ( Firmicutes ) Underlie the Response to Wetting of Cyanobacterial Biocrusts at Various Stages of Maturity
    journal, March 2018

    • Karaoz, Ulas; Couradeau, Estelle; da Rocha, Ulisses Nunes
    • mBio, Vol. 9, Issue 2
    • DOI: 10.1128/mbio.01366-16

    Effects of Spatial Variability and Relic DNA Removal on the Detection of Temporal Dynamics in Soil Microbial Communities
    journal, January 2020

    • Carini, Paul; Delgado-Baquerizo, Manuel; Hinckley, Eve-Lyn S.
    • mBio, Vol. 11, Issue 1
    • DOI: 10.1128/mbio.02776-19

    Dynamic substrate preferences predict metabolic properties of a simple microbial consortium
    journal, January 2017


    Combining multiple functional annotation tools increases coverage of metabolic annotation
    journal, December 2018


    Web of microbes (WoM): a curated microbial exometabolomics database for linking chemistry and microbes
    journal, September 2018


    Belowground Response to Drought in a Tropical Forest Soil. II. Change in Microbial Function Impacts Carbon Composition
    journal, March 2016


    Microbial Group Dynamics in Plant Rhizospheres and Their Implications on Nutrient Cycling
    journal, July 2018


    Challenges and Approaches in Microbiome Research: From Fundamental to Applied
    journal, August 2018


    Mind the Gap: Mapping Mass Spectral Databases in Genome-Scale Metabolic Networks Reveals Poorly Covered Areas
    journal, September 2018

    • Frainay, Clément; Schymanski, Emma; Neumann, Steffen
    • Metabolites, Vol. 8, Issue 3
    • DOI: 10.3390/metabo8030051

    Wet season cyanobacterial N enrichment highly correlated with species richness and Nostoc in the northern Australian savannah
    journal, January 2018

    • Williams, Wendy; Büdel, Burkhard; Williams, Stephen
    • Biogeosciences, Vol. 15, Issue 7
    • DOI: 10.5194/bg-15-2149-2018

    Multilab EcoFAB study shows highly reproducible physiology and depletion of soil metabolites by a model grass
    journal, January 2019

    • Sasse, Joelle; Kant, Josefine; Cole, Benjamin J.
    • New Phytologist, Vol. 222, Issue 2
    • DOI: 10.1111/nph.15662

      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.