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Title: Networks of energetic and metabolic interactions define dynamics in microbial communities

Microorganisms form diverse communities that have a profound impact on the environment and human health. Recent technological advances have enabled elucidation of community diversity at high resolution. Investigation of microbial communities has revealed that they often contain multiple members with complementing and seemingly redundant metabolic capabilities. An understanding of the communal impacts of redundant metabolic capabilities is currently lacking; specifically, it is not known whether metabolic redundancy will foster competition or motivate cooperation. By investigating methanogenic populations, we identified the multidimensional interspecies interactions that define composition and dynamics within syntrophic communities that play a key role in the global carbon cycle. Species-specific genomes were extracted from metagenomic data using differential coverage binning. We then used metabolic modeling leveraging metatranscriptomic information to reveal and quantify a complex intertwined system of syntrophic relationships. Our results show that amino acid auxotrophies create additional interdependencies that define community composition and control carbon and energy flux through the system while simultaneously contributing to overall community robustness. Strategic use of antimicrobials further reinforces this intricate interspecies network. Collectively, our study reveals the multidimensional interactions in syntrophic communities that promote high species richness and bolster community stability during environmental perturbations.
Authors:
 [1] ;  [1] ;  [1] ;  [1]
  1. Univ. of California, San Diego, CA (United States). Dept. of Bioengineering
Publication Date:
Grant/Contract Number:
AC02-05CH11231; P30 NS047101; SC0004485; SC0004917
Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 112; Journal Issue: 50; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Research Org:
Univ. of California, San Diego, CA (United States)
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Scientific User Facilities Division
Contributing Orgs:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; microbial communities; microbiome; interspecies interactions; methanogens; metabolic modeling
OSTI Identifier:
1235185
Alternate Identifier(s):
OSTI ID: 1469098

Embree, Mallory, Liu, Joanne K., Al-Bassam, Mahmoud M., and Zengler, Karsten. Networks of energetic and metabolic interactions define dynamics in microbial communities. United States: N. p., Web. doi:10.1073/pnas.1506034112.
Embree, Mallory, Liu, Joanne K., Al-Bassam, Mahmoud M., & Zengler, Karsten. Networks of energetic and metabolic interactions define dynamics in microbial communities. United States. doi:10.1073/pnas.1506034112.
Embree, Mallory, Liu, Joanne K., Al-Bassam, Mahmoud M., and Zengler, Karsten. 2015. "Networks of energetic and metabolic interactions define dynamics in microbial communities". United States. doi:10.1073/pnas.1506034112.
@article{osti_1235185,
title = {Networks of energetic and metabolic interactions define dynamics in microbial communities},
author = {Embree, Mallory and Liu, Joanne K. and Al-Bassam, Mahmoud M. and Zengler, Karsten},
abstractNote = {Microorganisms form diverse communities that have a profound impact on the environment and human health. Recent technological advances have enabled elucidation of community diversity at high resolution. Investigation of microbial communities has revealed that they often contain multiple members with complementing and seemingly redundant metabolic capabilities. An understanding of the communal impacts of redundant metabolic capabilities is currently lacking; specifically, it is not known whether metabolic redundancy will foster competition or motivate cooperation. By investigating methanogenic populations, we identified the multidimensional interspecies interactions that define composition and dynamics within syntrophic communities that play a key role in the global carbon cycle. Species-specific genomes were extracted from metagenomic data using differential coverage binning. We then used metabolic modeling leveraging metatranscriptomic information to reveal and quantify a complex intertwined system of syntrophic relationships. Our results show that amino acid auxotrophies create additional interdependencies that define community composition and control carbon and energy flux through the system while simultaneously contributing to overall community robustness. Strategic use of antimicrobials further reinforces this intricate interspecies network. Collectively, our study reveals the multidimensional interactions in syntrophic communities that promote high species richness and bolster community stability during environmental perturbations.},
doi = {10.1073/pnas.1506034112},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 50,
volume = 112,
place = {United States},
year = {2015},
month = {11}
}