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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 Laboratory (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. https://doi.org/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. https://doi.org/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 = {Fri Mar 23 00:00:00 EDT 2018},
month = {Fri Mar 23 00:00:00 EDT 2018}
}

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Decoding molecular interactions in microbial communities
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Insights into the Evolution of Vitamin B12 Auxotrophy from Sequenced Algal Genomes
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Oxygen Profiles in, and in the Agar Beneath, Colonies of Bacillus Cereus, Staphylococcus Albus and Escherichia Coli
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Proline auxotrophy in Sinorhizobium meliloti results in a plant-specific symbiotic phenotype
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Broad-Spectrum Suppression of Innate Immunity Is Required for Colonization of Arabidopsis Roots by the Fungus Piriformospora indica
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The Microbial Engines That Drive Earth's Biogeochemical Cycles
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The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss
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Works referencing / citing this record:

Genome and evolution of the arbuscular mycorrhizal fungus Diversispora epigaea (formerly Glomus versiforme ) and its bacterial endosymbionts
journal, October 2018

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Disentangling strictly self-serving mutations from win-win mutations in a mutualistic microbial community
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Manganese Oxide Biomineralization Provides Protection against Nitrite Toxicity in a Cell-Density-Dependent Manner
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Uncovering and resolving challenges of quantitative modeling in a simplified community of interacting cells
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A riboswitch gives rise to multi-generational phenotypic heterogeneity in an auxotrophic bacterium
text, January 2020