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Title: Impact of spatial organization on a novel auxotrophic interaction among soil microbes

Abstract

Here, a key prerequisite to achieve a deeper understanding of microbial communities and to engineer synthetic ones is to identify the individual metabolic interactions among key species and how these interactions are affected by different environmental factors. Deciphering the physiological basis of species–species and species–environment interactions in spatially organized environments requires reductionist approaches using ecologically and functionally relevant species. To this end, we focus here on a defined system to study the metabolic interactions in a spatial context among the plant-beneficial endophytic fungus Serendipita indica, and the soil-dwelling model bacterium Bacillus subtilis. Focusing on the growth dynamics of S. indica under defined conditions, we identified an auxotrophy in this organism for thiamine, which is a key co-factor for essential reactions in the central carbon metabolism. We found that S. indica growth is restored in thiamine-free media, when co-cultured with B. subtilis. The success of this auxotrophic interaction, however, was dependent on the spatial and temporal organization of the system; the beneficial impact of B. subtilis was only visible when its inoculation was separated from that of S. indica either in time or space. These findings describe a key auxotrophic interaction in the soil among organisms that are shown to bemore » important for plant ecosystem functioning, and point to the potential importance of spatial and temporal organization for the success of auxotrophic interactions. These points can be particularly important for engineering of minimal functional synthetic communities as plant seed treatments and for vertical farming under defined conditions.« less

Authors:
 [1];  [1]; ORCiD logo [2];  [1];  [1];  [1]; ORCiD logo [1]
  1. The Univ. of Warwick, Coventry (United Kingdom)
  2. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Publication Date:
Research Org.:
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE Laboratory Directed Research and Development (LDRD) Program
OSTI Identifier:
1434433
Report Number(s):
LA-UR-18-21554
Journal ID: ISSN 1751-7362
Grant/Contract Number:  
AC52-06NA25396
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 12; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biological Science; Auxotrophy; soil microbial communities; Serendipita indica; Bacillus subtilis; endophytic fungi; thiamine; vitamins; metabolic interaction; precision farming

Citation Formats

Jiang, Xue, ZerfaB, Christian, Feng, Song, Eichmann, Ruth, Asally, Munehiro, Schafer, Patrick, and Soyer, Orkun S. Impact of spatial organization on a novel auxotrophic interaction among soil microbes. United States: N. p., 2018. Web. doi:10.1038/s41396-018-0095-z.
Jiang, Xue, ZerfaB, Christian, Feng, Song, Eichmann, Ruth, Asally, Munehiro, Schafer, Patrick, & Soyer, Orkun S. Impact of spatial organization on a novel auxotrophic interaction among soil microbes. United States. doi:10.1038/s41396-018-0095-z.
Jiang, Xue, ZerfaB, Christian, Feng, Song, Eichmann, Ruth, Asally, Munehiro, Schafer, Patrick, and Soyer, Orkun S. Fri . "Impact of spatial organization on a novel auxotrophic interaction among soil microbes". United States. doi:10.1038/s41396-018-0095-z. https://www.osti.gov/servlets/purl/1434433.
@article{osti_1434433,
title = {Impact of spatial organization on a novel auxotrophic interaction among soil microbes},
author = {Jiang, Xue and ZerfaB, Christian and Feng, Song and Eichmann, Ruth and Asally, Munehiro and Schafer, Patrick and Soyer, Orkun S.},
abstractNote = {Here, a key prerequisite to achieve a deeper understanding of microbial communities and to engineer synthetic ones is to identify the individual metabolic interactions among key species and how these interactions are affected by different environmental factors. Deciphering the physiological basis of species–species and species–environment interactions in spatially organized environments requires reductionist approaches using ecologically and functionally relevant species. To this end, we focus here on a defined system to study the metabolic interactions in a spatial context among the plant-beneficial endophytic fungus Serendipita indica, and the soil-dwelling model bacterium Bacillus subtilis. Focusing on the growth dynamics of S. indica under defined conditions, we identified an auxotrophy in this organism for thiamine, which is a key co-factor for essential reactions in the central carbon metabolism. We found that S. indica growth is restored in thiamine-free media, when co-cultured with B. subtilis. The success of this auxotrophic interaction, however, was dependent on the spatial and temporal organization of the system; the beneficial impact of B. subtilis was only visible when its inoculation was separated from that of S. indica either in time or space. These findings describe a key auxotrophic interaction in the soil among organisms that are shown to be important for plant ecosystem functioning, and point to the potential importance of spatial and temporal organization for the success of auxotrophic interactions. These points can be particularly important for engineering of minimal functional synthetic communities as plant seed treatments and for vertical farming under defined conditions.},
doi = {10.1038/s41396-018-0095-z},
journal = {The ISME Journal},
number = ,
volume = 12,
place = {United States},
year = {2018},
month = {3}
}

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    Works referencing / citing this record:

    Better together: engineering and application of microbial symbioses
    journal, December 2015


    Metabolic modelling in a dynamic evolutionary framework predicts adaptive diversification of bacteria in a long-term evolution experiment
    journal, August 2016

    • Großkopf, Tobias; Consuegra, Jessika; Gaffé, Joël
    • BMC Evolutionary Biology, Vol. 16, Issue 1
    • DOI: 10.1186/s12862-016-0733-x

    Arbuscular mycorrhiza and soil nitrogen cycling
    journal, March 2012


    Environmental pH modulation by pathogenic fungi as a strategy to conquer the host
    journal, February 2017


    Rapid HPLC Measurement of Thiamine and Its Phosphate Esters in Whole Blood
    journal, March 2008


    Plant root-microbe communication in shaping root microbiomes
    journal, January 2016

    • Lareen, Andrew; Burton, Frances; Schäfer, Patrick
    • Plant Molecular Biology, Vol. 90, Issue 6
    • DOI: 10.1007/s11103-015-0417-8

    Engineering microbial communities using thermodynamic principles and electrical interfaces
    journal, April 2018


    Plant and microbial strategies to improve the phosphorus efficiency of agriculture
    journal, September 2011


    Sebacinales – one thousand and one interactions with land plants
    journal, February 2016

    • Weiß, Michael; Waller, Frank; Zuccaro, Alga
    • New Phytologist, Vol. 211, Issue 1
    • DOI: 10.1111/nph.13977

    Bacillus subtilis isolated from the human gastrointestinal tract
    journal, March 2009


    Genetic drift opposes mutualism during spatial population expansion
    journal, January 2014

    • Muller, M. J. I.; Neugeboren, B. I.; Nelson, D. R.
    • Proceedings of the National Academy of Sciences, Vol. 111, Issue 3
    • DOI: 10.1073/pnas.1313285111

    Endophytic Life Strategies Decoded by Genome and Transcriptome Analyses of the Mutualistic Root Symbiont Piriformospora indica
    journal, October 2011


    Underlying mechanisms for syntrophic metabolism of essential enzyme cofactors in microbial communities
    journal, February 2017

    • Romine, Margaret F.; Rodionov, Dmitry A.; Maezato, Yukari
    • The ISME Journal, Vol. 11, Issue 6
    • DOI: 10.1038/ismej.2017.2

    Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria
    journal, November 2013


    Fungal—bacterial interactions: a mixed bag of mingling microbes
    journal, August 2006


    Engineering ecosystems and synthetic ecologies
    journal, January 2012

    • Mee, Michael T.; Wang, Harris H.
    • Molecular BioSystems, Vol. 8, Issue 10
    • DOI: 10.1039/c2mb25133g

    Piriformospora indica promotes adventitious root formation in cuttings
    journal, May 2007


    Metabolic origins of spatial organization in the tumor microenvironment
    journal, February 2017

    • Carmona-Fontaine, Carlos; Deforet, Maxime; Akkari, Leila
    • Proceedings of the National Academy of Sciences, Vol. 114, Issue 11
    • DOI: 10.1073/pnas.1700600114

    Proline auxotrophy in Sinorhizobium meliloti results in a plant-specific symbiotic phenotype
    journal, December 2015

    • Zamani, Maryam; Finan, Turlough M.; Cowie, Alison
    • Microbiology, Vol. 161, Issue 12
    • DOI: 10.1099/mic.0.000182

    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

    Challenges in microbial ecology: building predictive understanding of community function and dynamics
    journal, March 2016

    • Widder, Stefanie; Allen, Rosalind J.; Pfeiffer, Thomas
    • The ISME Journal, Vol. 10, Issue 11
    • DOI: 10.1038/ismej.2016.45

    Decoding molecular interactions in microbial communities
    journal, July 2016

    • Abreu, Nicole A.; Taga, Michiko E.
    • FEMS Microbiology Reviews, Vol. 40, Issue 5
    • DOI: 10.1093/femsre/fuw019

    Widespread decay of vitamin-related pathways: coincidence or consequence?
    journal, August 2013

    • Helliwell, Katherine E.; Wheeler, Glen L.; Smith, Alison G.
    • Trends in Genetics, Vol. 29, Issue 8
    • DOI: 10.1016/j.tig.2013.03.003

    Cell-to-cell heterogeneity emerges as consequence of metabolic cooperation in a synthetic yeast community
    journal, July 2016

    • Campbell, Kate; Vowinckel, Jakob; Ralser, Markus
    • Biotechnology Journal, Vol. 11, Issue 9
    • DOI: 10.1002/biot.201500301

    Structure and Functions of the Bacterial Microbiota of Plants
    journal, April 2013


    Piriformospora indica-a mutualistic basidiomycete with an exceptionally large plant host range: Mutualistic root symbiosis
    journal, November 2011


    Engineering microbial consortia for controllable outputs
    journal, March 2016

    • Lindemann, Stephen R.; Bernstein, Hans C.; Song, Hyun-Seob
    • The ISME Journal, Vol. 10, Issue 9
    • DOI: 10.1038/ismej.2016.26

    Temporal and spatial constraints on community assembly during microbial colonization of wood in seawater
    journal, April 2015

    • Kalenitchenko, Dimitri; Fagervold, Sonja K.; Pruski, Audrey M.
    • The ISME Journal, Vol. 9, Issue 12
    • DOI: 10.1038/ismej.2015.61

    Niche engineering demonstrates a latent capacity for fungal-algal mutualism
    journal, July 2014


    The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield
    journal, September 2005

    • Waller, F.; Achatz, B.; Baltruschat, H.
    • Proceedings of the National Academy of Sciences, Vol. 102, Issue 38
    • DOI: 10.1073/pnas.0504423102

    Morphological optimization for access to dual oxidants in biofilms
    journal, December 2013

    • Kempes, C. P.; Okegbe, C.; Mears-Clarke, Z.
    • Proceedings of the National Academy of Sciences, Vol. 111, Issue 1
    • DOI: 10.1073/pnas.1315521110

    Saccharomyces cerevisiae THI4p is a suicide thiamine thiazole synthase
    journal, October 2011

    • Chatterjee, Abhishek; Abeydeera, N. Dinuka; Bale, Shridhar
    • Nature, Vol. 478, Issue 7370
    • DOI: 10.1038/nature10503

    Thi20, a remarkable enzyme from Saccharomyces cerevisiae with dual thiamin biosynthetic and degradation activities
    journal, August 2005


    The Microbial Engines That Drive Earth's Biogeochemical Cycles
    journal, May 2008


    A new thiamin salvage pathway
    journal, July 2007

    • Jenkins, Amy Haas; Schyns, Ghislain; Potot, Sébastien
    • Nature Chemical Biology, Vol. 3, Issue 8
    • DOI: 10.1038/nchembio.2007.13

    SubtiWiki--a comprehensive community resource for the model organism Bacillus subtilis
    journal, November 2011

    • Mader, U.; Schmeisky, A. G.; Florez, L. A.
    • Nucleic Acids Research, Vol. 40, Issue D1
    • DOI: 10.1093/nar/gkr923

    MUSCLE: multiple sequence alignment with high accuracy and high throughput
    journal, March 2004

    • Edgar, R. C.
    • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
    • DOI: 10.1093/nar/gkh340

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