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Title: Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI

Abstract

An explosion in the number of available genome sequences obtained through metagenomics and single-cell genomics has enabled a new view of the diversity of microbial life, yet we know surprisingly little about how microbes interact with each other or their environment. In fact, the majority of microbial species remain uncultivated, while our perception of their ecological niches is based on reconstruction of their metabolic potential. In this work, we demonstrate how the “seed set framework,” which computes the set of compounds that an organism must acquire from its environment (E. Borenstein, M. Kupiec, M. W. Feldman, and E. Ruppin, Proc Natl Acad Sci U S A 105:14482–14487, 2008, https://doi.org/10.1073/pnas.0806162105), enables computational analysis of metabolic reconstructions while providing new insights into a microbe’s metabolic capabilities, such as nutrient use and auxotrophies. We apply this framework to members of the ubiquitous freshwater actinobacterial lineage acI, confirming and extending previous experimental and genomic observations implying that acI bacteria are heterotrophs reliant on peptides and saccharides. We also present the first metatranscriptomic study of the acI lineage, revealing high expression of transport proteins and the light-harvesting protein actinorhodopsin. Putative transport proteins complement predictions of nutrients and essential metabolites while providing additional support of themore » hypothesis that members of the acI are photoheterotrophs.« less

Authors:
ORCiD logo [1]; ORCiD logo [2];  [1]; ORCiD logo [3];  [3]; ORCiD logo [4]; ORCiD logo [5];  [1]; ORCiD logo [6]
  1. Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
  2. Uppsala Univ. (Sweden). Dept. of Ecology and Genetics
  3. Univ. of Wisconsin, Madison, WI (United States). Dept. of Civil and Environmental Engineering
  4. Uppsala Univ. (Sweden). Dept. of Ecology and Genetics. Science for Life Lab.
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  6. Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology. Dept. of Civil and Environmental Engineering
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDA National Inst. of Food and Agriculture (NIFA); National Science Foundation (NSF); National Oceanic and Atmospheric Administration (NOAA) (United States)
OSTI Identifier:
1459392
Grant/Contract Number:  
AC02-05CH11231; 2016-67012-24709; WIS01789; MCB-0702395; NTL-LTER DEB-1440297; DEB-1344254; NA10OAR4170070
Resource Type:
Accepted Manuscript
Journal Name:
mSystems
Additional Journal Information:
Journal Volume: 2; Journal Issue: 4; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; freshwater microbial ecology; metabolism; metagenomics; metatranscriptomics; physiology; systems biology

Citation Formats

Hamilton, Joshua J., Garcia, Sarahi L., Brown, Brittany S., Oyserman, Ben O., Moya-Flores, Francisco, Bertilsson, Stefan, Malmstrom, Rex R., Forest, Katrina T., and McMahon, Katherine D. Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI. United States: N. p., 2017. Web. https://doi.org/10.1128/mSystems.00091-17.
Hamilton, Joshua J., Garcia, Sarahi L., Brown, Brittany S., Oyserman, Ben O., Moya-Flores, Francisco, Bertilsson, Stefan, Malmstrom, Rex R., Forest, Katrina T., & McMahon, Katherine D. Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI. United States. https://doi.org/10.1128/mSystems.00091-17
Hamilton, Joshua J., Garcia, Sarahi L., Brown, Brittany S., Oyserman, Ben O., Moya-Flores, Francisco, Bertilsson, Stefan, Malmstrom, Rex R., Forest, Katrina T., and McMahon, Katherine D. Tue . "Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI". United States. https://doi.org/10.1128/mSystems.00091-17. https://www.osti.gov/servlets/purl/1459392.
@article{osti_1459392,
title = {Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI},
author = {Hamilton, Joshua J. and Garcia, Sarahi L. and Brown, Brittany S. and Oyserman, Ben O. and Moya-Flores, Francisco and Bertilsson, Stefan and Malmstrom, Rex R. and Forest, Katrina T. and McMahon, Katherine D.},
abstractNote = {An explosion in the number of available genome sequences obtained through metagenomics and single-cell genomics has enabled a new view of the diversity of microbial life, yet we know surprisingly little about how microbes interact with each other or their environment. In fact, the majority of microbial species remain uncultivated, while our perception of their ecological niches is based on reconstruction of their metabolic potential. In this work, we demonstrate how the “seed set framework,” which computes the set of compounds that an organism must acquire from its environment (E. Borenstein, M. Kupiec, M. W. Feldman, and E. Ruppin, Proc Natl Acad Sci U S A 105:14482–14487, 2008, https://doi.org/10.1073/pnas.0806162105), enables computational analysis of metabolic reconstructions while providing new insights into a microbe’s metabolic capabilities, such as nutrient use and auxotrophies. We apply this framework to members of the ubiquitous freshwater actinobacterial lineage acI, confirming and extending previous experimental and genomic observations implying that acI bacteria are heterotrophs reliant on peptides and saccharides. We also present the first metatranscriptomic study of the acI lineage, revealing high expression of transport proteins and the light-harvesting protein actinorhodopsin. Putative transport proteins complement predictions of nutrients and essential metabolites while providing additional support of the hypothesis that members of the acI are photoheterotrophs.},
doi = {10.1128/mSystems.00091-17},
journal = {mSystems},
number = 4,
volume = 2,
place = {United States},
year = {2017},
month = {8}
}

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