Exometabolite niche partitioning among sympatric soil bacteria

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.

doi:10.1038/ncomms9289

Title: Exometabolite niche partitioning among sympatric soil bacteria

Journal Article · 22 September 2015 · Nature Communications

DOI: https://doi.org/10.1038/ncomms9289 · OSTI ID:1256039

Baran, Richard ^[1]; Brodie, Eoin L. ^[2]; Mayberry-Lewis, Jazmine ^[3]; Hummel, Eric ^[4]; Da Rocha, Ulisses Nunes ^[5]; Chakraborty, Romy ^[6]; Bowen, Benjamin P. ^[7]; Karaoz, Ulas ^[6]; Cadillo-Quiroz, Hinsby ^[4]; Garcia-Pichel, Ferran ^[4]; Northen, Trent R. ^[7]

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)

© 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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1256039

Alternate ID(s):: OSTI ID: 1513785

Journal Information:: Nature Communications, Vol. 6; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 124 works

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Recent advances in the role of plant metabolites in shaping the root microbiome Jacoby, Richard P.; Chen, Li; Schwier, Melina F1000Research, Vol. 9 https://doi.org/10.12688/f1000research.21796.1	journal	January 2020
Multi-taxon inventory reveals highly consistent biodiversity responses to ecospace variation Brunbjerg, Ane Kirstine; Bruun, Hans Henrik; Dalby, Lars Oikos https://doi.org/10.1101/807321	journal	October 2019
Plant selection initiates alternative successional trajectories in the soil microbial community after disturbance Duhamel, Marie; Wan, Joe; Bogar, Laura M. Ecological Monographs, Vol. 89, Issue 3 https://doi.org/10.1002/ecm.1367	journal	March 2019
Emergent simplicity in microbial community assembly Goldford, Joshua E.; Lu, Nanxi; Bajić, Djordje Science, Vol. 361, Issue 6401 https://doi.org/10.1126/science.aat1168	journal	August 2018
Linking soil biology and chemistry in biological soil crust using isolate exometabolomics Swenson, Tami L.; Karaoz, Ulas; Swenson, Joel M. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-017-02356-9	journal	January 2018
Exogenous Nitrogen Addition Reduced the Temperature Sensitivity of Microbial Respiration without Altering the Microbial Community Composition Wei, Hui; Chen, Xiaomei; He, Jinhong Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02382	journal	December 2017
Biocrust morphology is linked to marked differences in microbial community composition Chilton, Angela M.; Neilan, Brett A.; Eldridge, David J. Plant and Soil, Vol. 429, Issue 1-2 https://doi.org/10.1007/s11104-017-3442-3	journal	October 2017
Dynamic substrate preferences predict metabolic properties of a simple microbial consortium Erbilgin, Onur; Bowen, Benjamin P.; Kosina, Suzanne M. BMC Bioinformatics, Vol. 18, Issue 1 https://doi.org/10.1186/s12859-017-1478-2	journal	January 2017
Applying community ecological theory to maximize productivity of cultivated biocrusts Bowker, Matthew A.; Antoninka, Anita J.; Durham, Rebecca A. Ecological Applications, Vol. 27, Issue 6 https://doi.org/10.1002/eap.1582	journal	August 2017
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Dynamic substrate preferences predict metabolic properties of a simple microbial consortium Erbilgin, Onur; Bowen, Benjamin P.; Kosina, Suzanne M. BMC Bioinformatics, Vol. 18, Issue 1 https://doi.org/10.1186/s12859-017-1478-2	journal	January 2017
Spatial segregation of the biological soil crust microbiome around its foundational cyanobacterium, Microcoleus vaginatus, and the formation of a nitrogen-fixing cyanosphere Couradeau, Estelle; Giraldo-Silva, Ana; De Martini, Francesca Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0661-2	journal	April 2019
Multi‐taxon inventory reveals highly consistent biodiversity responses to ecospace variation Brunbjerg, Ane Kirstine; Bruun, Hans Henrik; Dalby, Lars Oikos, Vol. 129, Issue 9 https://doi.org/10.1111/oik.07145	journal	June 2020
Challenges and Approaches in Microbiome Research: From Fundamental to Applied Sergaki, Chrysi; Lagunas, Beatriz; Lidbury, Ian Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01205	journal	August 2018
Using Maximum Entropy Production to Describe Microbial Biogeochemistry Over Time and Space in a Meromictic Pond Vallino, Joseph J.; Huber, Julie A. Frontiers in Environmental Science, Vol. 6 https://doi.org/10.3389/fenvs.2018.00100	journal	October 2018
Nursing biocrusts: isolation, cultivation, and fitness test of indigenous cyanobacteria: Nursing biocrust cyanobacteria Giraldo-Silva, Ana; Nelson, Corey; Barger, Nichole N. Restoration Ecology, Vol. 27, Issue 4 https://doi.org/10.1111/rec.12920	journal	January 2019
Using maximum entropy production to describe microbial biogeochemistry over time and space in a meromictic pond Vallino, Joseph J.; Huber, Julie A. Frontiers in Environmental Science https://doi.org/10.1101/266346	posted_content	February 2018
Spatial segregation of the biological soil crust microbiome around its foundational cyanobacterium, Microcoleus vaginatus, and the formation of a nitrogen-fixing cyanosphere Couradeau, Estelle; Giraldo-Silva, Ana; De Martini, Francesca Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0661-2	journal	April 2019
Multilab EcoFAB study shows highly reproducible physiology and depletion of soil metabolites by a model grass Sasse, Joelle; Kant, Josefine; Cole, Benjamin J. New Phytologist, Vol. 222, Issue 2 https://doi.org/10.1111/nph.15662	journal	January 2019
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Altering biocrusts for an altered climate Young, Kristina E.; Grover, Henry S.; Bowker, Matthew A. New Phytologist, Vol. 210, Issue 1 https://doi.org/10.1111/nph.13910	journal	February 2016
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Predicting metabolic adaptation from networks of mutational paths Josephides, Christos; Swain, Peter S. Nature Communications https://doi.org/10.1101/115170	journal	March 2017
Predicting metabolic adaptation from networks of mutational paths Josephides, Christos; Swain, Peter S. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00828-6	journal	September 2017
Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly Zhalnina, Kateryna; Louie, Katherine B.; Hao, Zhao Nature Microbiology, Vol. 3, Issue 4 https://doi.org/10.1038/s41564-018-0129-3	journal	March 2018
Nitrogen fixation in a non-heterocystous cyanobacterial mat from a mountain river Berrendero, Esther; Valiente, Eduardo Fernández; Perona, Elvira Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep30920	journal	August 2016
Wet season cyanobacterial N enrichment highly correlated with species richness and Nostoc in the northern Australian savannah Williams, Wendy; Büdel, Burkhard; Williams, Stephen Biogeosciences, Vol. 15, Issue 7 https://doi.org/10.5194/bg-15-2149-2018	journal	January 2018
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Mixed-Cropping Between Field Pea Varieties Alters Root Bacterial and Fungal Communities Horner, Anthony; Browett, Samuel S.; Antwis, Rachael E. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-53342-8	journal	November 2019
Belowground Response to Drought in a Tropical Forest Soil. II. Change in Microbial Function Impacts Carbon Composition Bouskill, Nicholas J.; Wood, Tana E.; Baran, Richard Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00323	journal	March 2016
Biological soil crusts: diminutive communities of potential global importance Ferrenberg, Scott; Tucker, Colin L.; Reed, Sasha C. Frontiers in Ecology and the Environment, Vol. 15, Issue 3 https://doi.org/10.1002/fee.1469	journal	March 2017
Assessing the influence of soil abiotic and biotic factors on Nostoc commune inoculation success Roncero-Ramos, B.; Román, J. R.; Rodríguez-Caballero, E. Plant and Soil, Vol. 444, Issue 1-2 https://doi.org/10.1007/s11104-019-04239-y	journal	August 2019
Microbial Group Dynamics in Plant Rhizospheres and Their Implications on Nutrient Cycling Garcia, Joshua; Kao-Kniffin, Jenny Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01516	journal	July 2018
Characterization of a nifH-Harboring Bacterial Community in the Soil-Limited Gotjawal Forest Lee, Tae Kwon; Han, Il; Kim, Min Sung Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01858	journal	August 2019
Mind the Gap: Mapping Mass Spectral Databases in Genome-Scale Metabolic Networks Reveals Poorly Covered Areas Frainay, Clément; Schymanski, Emma; Neumann, Steffen Metabolites, Vol. 8, Issue 3 https://doi.org/10.3390/metabo8030051	journal	September 2018
Linking soil biology and chemistry in biological soil crust using isolate exometabolomics Swenson, Tami L.; Karaoz, Ulas; Swenson, Joel M. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-017-02356-9	journal	January 2018
Polyphasic evaluation of key cyanobacteria in biocrusts from the most arid region in Europe Roncero-Ramos, Beatriz; Muñoz-Martín, M. Ángeles; Chamizo, Sonia PeerJ, Vol. 7 https://doi.org/10.7717/peerj.6169	journal	January 2019
Biofilms 2018: a Diversity of Microbes and Mechanisms Fuqua, Clay; Filloux, Alain; Ghigo, Jean-Marc Journal of Bacteriology, Vol. 201, Issue 18 https://doi.org/10.1128/jb.00118-19	journal	February 2019
Belowground Response to Drought in a Tropical Forest Soil. II. Change in Microbial Function Impacts Carbon Composition Bouskill, Nicholas J.; Wood, Tana E.; Baran, Richard Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00323	journal	March 2016
Learning representations of microbe–metabolite interactions Morton, James T.; Aksenov, Alexander A.; Nothias, Louis Felix Nature Methods, Vol. 16, Issue 12 https://doi.org/10.1038/s41592-019-0616-3	journal	November 2019
Yeast Creates a Niche for Symbiotic Lactic Acid Bacteria through Nitrogen Overflow Ponomarova, Olga; Gabrielli, Natalia; Sévin, Daniel C. Cell Systems, Vol. 5, Issue 4 https://doi.org/10.1016/j.cels.2017.09.002	journal	October 2017
Patterns and Controls on Nitrogen Cycling of Biological Soil Crusts Barger, Nichole N.; Weber, Bettina; Garcia-Pichel, Ferran Biological Soil Crusts: An Organizing Principle in Drylands https://doi.org/10.1007/978-3-319-30214-0_14	book	January 2016
Microbial Group Dynamics in Plant Rhizospheres and Their Implications on Nutrient Cycling Garcia, Joshua; Kao-Kniffin, Jenny Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01516	journal	July 2018
Effects of Spatial Variability and Relic DNA Removal on the Detection of Temporal Dynamics in Soil Microbial Communities Carini, Paul; Delgado-Baquerizo, Manuel; Hinckley, Eve-Lyn S. mBio, Vol. 11, Issue 1 https://doi.org/10.1128/mbio.02776-19	journal	January 2020