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...

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Autores principales:	Joshua J. Hamilton, Sarahi L. Garcia, Brittany S. Brown, Ben O. Oyserman, Francisco Moya-Flores, Stefan Bertilsson, Rex R. Malmstrom, Katrina T. Forest, Katherine D. McMahon
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	freshwater microbial ecology metabolism metagenomics metatranscriptomics physiology systems biology Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/058dcbd295894b0bba99df122766c1ca
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spelling	oai:doaj.org-article:058dcbd295894b0bba99df122766c1ca2021-12-02T18:39:33ZMetabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI10.1128/mSystems.00091-172379-5077https://doaj.org/article/058dcbd295894b0bba99df122766c1ca2017-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00091-17https://doaj.org/toc/2379-5077ABSTRACT 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. IMPORTANCE The metabolic activity of uncultivated microorganisms contributes to numerous ecosystem processes, ranging from nutrient cycling in the environment to influencing human health and disease. Advances in sequencing technology have enabled the assembly of genomes for these microorganisms, but our ability to generate reference genomes far outstrips our ability to analyze them. Common approaches to analyzing microbial metabolism require reconstructing the entirety of an organism’s metabolic pathways or performing targeted searches for genes involved in a specific process. This paper presents a third approach, in which draft metabolic reconstructions are used to identify compounds through which an organism may interact with its environment. These compounds can then guide more-intensive metabolic reconstruction efforts and can also provide new hypotheses about the specific contributions that microbes make to ecosystem-scale metabolic processes.Joshua J. HamiltonSarahi L. GarciaBrittany S. BrownBen O. OysermanFrancisco Moya-FloresStefan BertilssonRex R. MalmstromKatrina T. ForestKatherine D. McMahonAmerican Society for Microbiologyarticlefreshwater microbial ecologymetabolismmetagenomicsmetatranscriptomicsphysiologysystems biologyMicrobiologyQR1-502ENmSystems, Vol 2, Iss 4 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	freshwater microbial ecology metabolism metagenomics metatranscriptomics physiology systems biology Microbiology QR1-502
spellingShingle	freshwater microbial ecology metabolism metagenomics metatranscriptomics physiology systems biology Microbiology QR1-502 Joshua J. Hamilton Sarahi L. Garcia Brittany S. Brown Ben O. Oyserman Francisco Moya-Flores Stefan Bertilsson Rex R. Malmstrom Katrina T. Forest Katherine D. McMahon Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI
description	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 the hypothesis that members of the acI are photoheterotrophs. IMPORTANCE The metabolic activity of uncultivated microorganisms contributes to numerous ecosystem processes, ranging from nutrient cycling in the environment to influencing human health and disease. Advances in sequencing technology have enabled the assembly of genomes for these microorganisms, but our ability to generate reference genomes far outstrips our ability to analyze them. Common approaches to analyzing microbial metabolism require reconstructing the entirety of an organism’s metabolic pathways or performing targeted searches for genes involved in a specific process. This paper presents a third approach, in which draft metabolic reconstructions are used to identify compounds through which an organism may interact with its environment. These compounds can then guide more-intensive metabolic reconstruction efforts and can also provide new hypotheses about the specific contributions that microbes make to ecosystem-scale metabolic processes.
format	article
author	Joshua J. Hamilton Sarahi L. Garcia Brittany S. Brown Ben O. Oyserman Francisco Moya-Flores Stefan Bertilsson Rex R. Malmstrom Katrina T. Forest Katherine D. McMahon
author_facet	Joshua J. Hamilton Sarahi L. Garcia Brittany S. Brown Ben O. Oyserman Francisco Moya-Flores Stefan Bertilsson Rex R. Malmstrom Katrina T. Forest Katherine D. McMahon
author_sort	Joshua J. Hamilton
title	Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI
title_short	Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI
title_full	Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI
title_fullStr	Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI
title_full_unstemmed	Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI
title_sort	metabolic network analysis and metatranscriptomics reveal auxotrophies and nutrient sources of the cosmopolitan freshwater microbial lineage aci
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/058dcbd295894b0bba99df122766c1ca
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Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI

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