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:
-
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Climate and Ecosystems Sciences Division; Univ. of California, Berkeley, CA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division; Arizona State Univ., Mesa, AZ (United States)
- Arizona State Univ., Mesa, AZ (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Climate and Ecosystems Sciences Division; Vrije Univ., Amsterdam (Netherlands)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Climate and Ecosystems Sciences Division
- 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 Laboratory (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. doi: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}
}
Web of Science
Figures / Tables:

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- Sergaki, Chrysi; Lagunas, Beatriz; Lidbury, Ian
- Frontiers in Plant Science, Vol. 9
Using Maximum Entropy Production to Describe Microbial Biogeochemistry Over Time and Space in a Meromictic Pond
journal, October 2018
- Vallino, Joseph J.; Huber, Julie A.
- Frontiers in Environmental Science, Vol. 6
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
Spatial segregation of the biological soil crust microbiome around its foundational cyanobacterium, Microcoleus vaginatus, and the formation of a nitrogen-fixing cyanosphere
journal, April 2019
- Couradeau, Estelle; Giraldo-Silva, Ana; De Martini, Francesca
- Microbiome, Vol. 7, Issue 1
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
Biphasic cellular adaptations and ecological implications of Alteromonas macleodii degrading a mixture of algal polysaccharides
journal, August 2018
- Koch, Hanna; Dürwald, Alexandra; Schweder, Thomas
- The ISME Journal, Vol. 13, Issue 1
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
Challenges and Approaches in Microbiome Research: From Fundamental to Applied
journal, August 2018
- Sergaki, Chrysi; Lagunas, Beatriz; Lidbury, Ian
- Frontiers in Plant Science, Vol. 9
Web of microbes (WoM): a curated microbial exometabolomics database for linking chemistry and microbes
journal, September 2018
- Kosina, Suzanne M.; Greiner, Annette M.; Lau, Rebecca K.
- BMC Microbiology, Vol. 18, Issue 1
Altering biocrusts for an altered climate
journal, February 2016
- Young, Kristina E.; Grover, Henry S.; Bowker, Matthew A.
- New Phytologist, Vol. 210, Issue 1
Combining multiple functional annotation tools increases coverage of metabolic annotation
journal, December 2018
- Griesemer, Marc; Kimbrel, Jeffrey A.; Zhou, Carol E.
- BMC Genomics, Vol. 19, Issue 1
Predicting metabolic adaptation from networks of mutational paths
journal, September 2017
- Josephides, Christos; Swain, Peter S.
- Nature Communications, Vol. 8, Issue 1
Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly
journal, March 2018
- Zhalnina, Kateryna; Louie, Katherine B.; Hao, Zhao
- Nature Microbiology, Vol. 3, Issue 4
Nitrogen fixation in a non-heterocystous cyanobacterial mat from a mountain river
journal, August 2016
- Berrendero, Esther; Valiente, Eduardo Fernández; Perona, Elvira
- Scientific Reports, Vol. 6, Issue 1
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
Combining multiple functional annotation tools increases coverage of metabolic annotation
journal, December 2018
- Griesemer, Marc; Kimbrel, Jeffrey A.; Zhou, Carol E.
- BMC Genomics, Vol. 19, Issue 1
Mixed-Cropping Between Field Pea Varieties Alters Root Bacterial and Fungal Communities
journal, November 2019
- Horner, Anthony; Browett, Samuel S.; Antwis, Rachael E.
- Scientific Reports, Vol. 9, Issue 1
Belowground Response to Drought in a Tropical Forest Soil. II. Change in Microbial Function Impacts Carbon Composition
journal, March 2016
- Bouskill, Nicholas J.; Wood, Tana E.; Baran, Richard
- Frontiers in Microbiology, Vol. 7
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
Assessing the influence of soil abiotic and biotic factors on Nostoc commune inoculation success
journal, August 2019
- Roncero-Ramos, B.; Román, J. R.; Rodríguez-Caballero, E.
- Plant and Soil, Vol. 444, Issue 1-2
Microbial Group Dynamics in Plant Rhizospheres and Their Implications on Nutrient Cycling
journal, July 2018
- Garcia, Joshua; Kao-Kniffin, Jenny
- Frontiers in Microbiology, Vol. 9
Characterization of a nifH-Harboring Bacterial Community in the Soil-Limited Gotjawal Forest
journal, August 2019
- Lee, Tae Kwon; Han, Il; Kim, Min Sung
- Frontiers in Microbiology, Vol. 10
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
Linking soil biology and chemistry in biological soil crust using isolate exometabolomics
journal, January 2018
- Swenson, Tami L.; Karaoz, Ulas; Swenson, Joel M.
- Nature Communications, Vol. 9, Issue 1
Polyphasic evaluation of key cyanobacteria in biocrusts from the most arid region in Europe
journal, January 2019
- Roncero-Ramos, Beatriz; Muñoz-Martín, M. Ángeles; Chamizo, Sonia
- PeerJ, Vol. 7
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
Belowground Response to Drought in a Tropical Forest Soil. II. Change in Microbial Function Impacts Carbon Composition
journal, March 2016
- Bouskill, Nicholas J.; Wood, Tana E.; Baran, Richard
- Frontiers in Microbiology, Vol. 7
Learning representations of microbe–metabolite interactions
journal, November 2019
- Morton, James T.; Aksenov, Alexander A.; Nothias, Louis Felix
- Nature Methods, Vol. 16, Issue 12
Yeast Creates a Niche for Symbiotic Lactic Acid Bacteria through Nitrogen Overflow
journal, October 2017
- Ponomarova, Olga; Gabrielli, Natalia; Sévin, Daniel C.
- Cell Systems, Vol. 5, Issue 4
Microbial Group Dynamics in Plant Rhizospheres and Their Implications on Nutrient Cycling
journal, July 2018
- Garcia, Joshua; Kao-Kniffin, Jenny
- Frontiers in Microbiology, Vol. 9
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
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