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Title: Metabolic modeling of a mutualistic microbial community

Abstract

The rate of production of methane in many environmentsdepends upon mutualistic interactions between sulfate-reducing bacteriaand methanogens. To enhance our understanding of these relationships, wetook advantage of the fully sequenced genomes of Desulfovibrio vulgarisand Methanococcus maripaludis to produce and analyze the firstmultispecies stoichiometric metabolic model. Model results were comparedto data on growth of the co-culture on lactate in the absence of sulfate.The model accurately predicted several ecologically relevantcharacteristics, including the flux of metabolites and the ratio of D.vulgaris to M. maripaludis cells during growth. In addition, the modeland our data suggested that it was possible to eliminate formate as aninterspecies electron shuttle, but hydrogen transfer was essential forsyntrophic growth. Our work demonstrated that reconstructed metabolicnetworks and stoichiometric models can serve not only to predictmetabolic fluxes and growth phenotypes of single organisms, but also tocapture growth parameters and community composition of simple bacterialcommunities.

Authors:
; ; ; ; ; ;
Publication Date:
Research Org.:
COLLABORATION - U.Washington
Sponsoring Org.:
USDOE Director. Office of Science. Biological andEnvironmental Research
OSTI Identifier:
925518
Report Number(s):
LBNL-60299
R&D Project: VGTLUW; BnR: KP1501021; TRN: US200809%%781
DOE Contract Number:
DE-AC02-05CH11231
Resource Type:
Journal Article
Resource Relation:
Journal Name: Molecular Systems Biology; Journal Volume: 3; Journal Issue: 92; Related Information: Journal Publication Date: 03/13/2007
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; COMMUNITIES; DESULFOVIBRIO; ELECTRONS; FORMATES; HYDROGEN TRANSFER; LACTATES; METABOLITES; METHANE; PRODUCTION; SIMULATION; SULFATE-REDUCING BACTERIA; Desulfovibrio flux-balance modeling interspecies hydrogentransfer Methanococcus syntrophy

Citation Formats

Stolyar, Sergey, Van Dien, Steve, Hillesland, Kristina Linnea, Pinel, Nicolas, Lie, Thomas J., Leigh, John A., and Stahl, David A.. Metabolic modeling of a mutualistic microbial community. United States: N. p., 2007. Web. doi:10.1038/msb4100131.
Stolyar, Sergey, Van Dien, Steve, Hillesland, Kristina Linnea, Pinel, Nicolas, Lie, Thomas J., Leigh, John A., & Stahl, David A.. Metabolic modeling of a mutualistic microbial community. United States. doi:10.1038/msb4100131.
Stolyar, Sergey, Van Dien, Steve, Hillesland, Kristina Linnea, Pinel, Nicolas, Lie, Thomas J., Leigh, John A., and Stahl, David A.. Tue . "Metabolic modeling of a mutualistic microbial community". United States. doi:10.1038/msb4100131.
@article{osti_925518,
title = {Metabolic modeling of a mutualistic microbial community},
author = {Stolyar, Sergey and Van Dien, Steve and Hillesland, Kristina Linnea and Pinel, Nicolas and Lie, Thomas J. and Leigh, John A. and Stahl, David A.},
abstractNote = {The rate of production of methane in many environmentsdepends upon mutualistic interactions between sulfate-reducing bacteriaand methanogens. To enhance our understanding of these relationships, wetook advantage of the fully sequenced genomes of Desulfovibrio vulgarisand Methanococcus maripaludis to produce and analyze the firstmultispecies stoichiometric metabolic model. Model results were comparedto data on growth of the co-culture on lactate in the absence of sulfate.The model accurately predicted several ecologically relevantcharacteristics, including the flux of metabolites and the ratio of D.vulgaris to M. maripaludis cells during growth. In addition, the modeland our data suggested that it was possible to eliminate formate as aninterspecies electron shuttle, but hydrogen transfer was essential forsyntrophic growth. Our work demonstrated that reconstructed metabolicnetworks and stoichiometric models can serve not only to predictmetabolic fluxes and growth phenotypes of single organisms, but also tocapture growth parameters and community composition of simple bacterialcommunities.},
doi = {10.1038/msb4100131},
journal = {Molecular Systems Biology},
number = 92,
volume = 3,
place = {United States},
year = {Tue Mar 13 00:00:00 EDT 2007},
month = {Tue Mar 13 00:00:00 EDT 2007}
}
  • Metabolic network modeling of microbial communities provides an in-depth understanding of community-wide metabolic and regulatory processes. Compared to single organism analyses, community metabolic network modeling is more complex because it needs to account for interspecies interactions. To date, most approaches focus on reconstruction of high-quality individual networks so that, when combined, they can predict community behaviors as a result of interspecies interactions. However, this conventional method becomes ineffective for communities whose members are not well characterized and cannot be experimentally interrogated in isolation. Here, we tested a new approach that uses community-level data as a critical input for the networkmore » reconstruction process. This method focuses on directly predicting interspecies metabolic interactions in a community, when axenic information is insufficient. We validated our method through the case study of a bacterial photoautotroph-heterotroph consortium that was used to provide data needed for a community-level metabolic network reconstruction. Resulting simulations provided experimentally validated predictions of how a photoautotrophic cyanobacterium supports the growth of an obligate heterotrophic species by providing organic carbon and nitrogen sources.« less
  • Most bacterial symbionts of plants are phenotypically characterized by their parasitic or matualistic relationship with the host; however, the genomic characteristics that likely discriminate mutualistic symbionts from pathogens of plants are poorly understood. This study comparatively analyzed the genomes of 54 plant-symbiontic bacteria, 27 mutualists and 27 pathogens, to discover genomic determinants of their parasitic and mutualistic nature in terms of protein family domains, KEGG orthologous groups, metabolic pathways and families of carbohydrate-active enzymes (CAZymes). We further used all bacteria with sequenced genomesl, published microarrays and transcriptomics experimental datasets, and literature to validate and to explore results of the comparison.more » The analysis revealed that genomes of mutualists are larger in size and higher in GC content and encode greater molecular, functional and metabolic diversity than the investigated genomes of pathogens. This enriched molecular and functional enzyme diversity included constructive biosynthetic signatures of CAZymes and metabolic pathways in genomes of mutualists compared with catabolic signatures dominant in the genomes of pathogens. Another discriminative characteristic of mutualists is the co-occurence of gene clusters required for the expression and function of nitrogenase and RuBisCO. Analysis of previously published experimental data indicate that nitrogen-fixing mutualists may employ Rubisco to fix CO2 not in the canonical Calvin-Benson-Basham cycle but in a novel metabolic pathway, here called Rubisco-based glycolysis , to increase efficiency of sugar utilization during the symbiosis with plants. An important discriminative characteristic of plant pathogenic bacteria is two groups of genes likely encoding effector proteins involved in host invasion and a genomic locus encoding a putative secretion system that includes a DUF1525 domain protein conserved in pathogens of plants and of other organisms. The protein belongs to the same clan of thioredoxins as the circadian clock protein kaiB found in many mutualistic symbionts and highly abundant in blood cells colonized by a human pathogen, Salmonella enterica serotype Typhi, the cause of typhoid fever.« less
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  • Communities of microorganisms control the rates of key biogeochemical cycles, and are important for biotechnology, bioremediation, and industrial microbiological processes. For this reason, we constructed a model microbial community comprised of three species dependent on trophic interactions. The three species microbial community was comprised of Clostridium cellulolyticum, Desulfovibrio vulgaris Hildenborough, and Geobacter sulfurreducens and was grown under continuous culture conditions. Cellobiose served as the carbon and energy source for C. cellulolyticum, whereas D. vulgaris and G. sulfurreducens derived carbon and energy from the metabolic products of cellobiose fermentation and were provided with sulfate and fumarate respectively as electron acceptors.