skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Systems level analysis of the Chlamydomonas reinhardtii metabolic network reveals variability in evolutionary co-conservation

Journal Article · · Molecular BioSystems
DOI:https://doi.org/10.1039/c6mb00237d· OSTI ID:1434909
 [1];  [2];  [1];  [3]; ORCiD logo [1];  [1];  [1];  [1];  [1];  [1];  [2];  [2];  [4];  [3];  [5];  [6]
  1. New York Univ. Abu Dhabi Institute, Abu Dhabi (United Arab Emirates)
  2. Harvard Medical School, Boston, MA (United States)
  3. Cornell Univ., Ithaca, NY (United States)
  4. Univ. of Virginia, Charlottesville, VA (United States)
  5. New York Univ. Abu Dhabi Institute, Abu Dhabi (United Arab Emirates); Harvard Medical School, Boston, MA (United States); MRC Lab. of Molecular Biology, Cambridge (United Kingdom)
  6. New York Univ. Abu Dhabi Institute, Abu Dhabi (United Arab Emirates); Harvard Medical School, Boston, MA (United States)

Metabolic networks, which are mathematical representations of organismal metabolism, are reconstructed to provide computational platforms to guide metabolic engineering experiments and explore fundamental questions on metabolism. Systems level analyses, such as interrogation of phylogenetic relationships within the network, can provide further guidance on the modification of metabolic circuitries. Chlamydomonas reinhardtii, a biofuel relevant green alga that has retained key genes with plant, animal, and protist affinities, serves as an ideal model organism to investigate the interplay between gene function and phylogenetic affinities at multiple organizational levels. Here, using detailed topological and functional analyses, coupled with transcriptomics studies on a metabolic network that we have reconstructed for C. reinhardtii, we show that network connectivity has a significant concordance with the co-conservation of genes; however, a distinction between topological and functional relationships is observable within the network. Dynamic and static modes of co-conservation were defined and observed in a subset of gene-pairs across the network topologically. In contrast, genes with predicted synthetic interactions, or genes involved in coupled reactions, show significant enrichment for both shorter and longer phylogenetic distances. Based on our results, we propose that the metabolic network of C. reinhardtii is assembled with an architecture to minimize phylogenetic profile distances topologically, while it includes an expansion of such distances for functionally interacting genes. This arrangement may increase the robustness of C. reinhardtii's network in dealing with varied environmental challenges that the species may face. As a result, the defined evolutionary constraints within the network, which identify important pairings of genes in metabolism, may offer guidance on synthetic biology approaches to optimize the production of desirable metabolites.

Research Organization:
Harvard Medical School, Boston, MA (United States). Dana-Farber Cancer Institute, Inc.
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
FG02-07ER64496
OSTI ID:
1434909
Journal Information:
Molecular BioSystems, Vol. 12, Issue 8; ISSN 1742-206X
Publisher:
Royal Society of ChemistryCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 9 works
Citation information provided by
Web of Science

References (57)

Metabolic network analysis of the causes and evolution of enzyme dispensability in yeast journal June 2004
Chemical and genomic evolution of enzyme-catalyzed reaction networks journal June 2013
Properties of Metabolic Networks: Structure versus Function journal January 2005
Correlation between structure and temperature in prokaryotic metabolic networks journal August 2007
Genome evolution reveals biochemical networks and functional modules journal December 2003
Computational Approaches for Microalgal Biofuel Optimization: A Review journal January 2014
Evolutionary Dynamics of Prokaryotic Transcriptional Regulatory Networks journal April 2006
Differential expression in RNA-seq: A matter of depth journal September 2011
Assigning protein functions by comparative genome analysis: Protein phylogenetic profiles journal April 1999
A Soluble Guanylate Cyclase Mediates Negative Signaling by Ammonium on Expression of Nitrate Reductase in Chlamydomonas journal May 2010
Functional Repurposing Revealed by Comparing S. pombe and S. cerevisiae Genetic Interactions journal June 2012
Protein function in the post-genomic era journal June 2000
Mapping and quantifying mammalian transcriptomes by RNA-Seq journal May 2008
Protein Interaction Mapping in C. elegans Using Proteins Involved in Vulval Development journal January 2000
Microalgal Metabolic Network Model Refinement through High-Throughput Functional Metabolic Profiling journal December 2014
A network perspective on the evolution of metabolism by gene duplication journal January 2007
Global organization of metabolic fluxes in the bacterium Escherichia coli journal February 2004
Metabolic network reconstruction of Chlamydomonas offers insight into light‐driven algal metabolism journal January 2011
The large-scale organization of metabolic networks journal October 2000
Annotation Transfer Between Genomes: Protein-Protein Interologs and Protein-DNA Regulogs journal May 2004
Comparative genomics and bioenergetics journal November 2001
Discovery of uncharacterized cellular systems by genome-wide analysis of functional linkages journal August 2003
Three-Dimensional Structural View of the Central Metabolic Network of Thermotoga maritima journal September 2009
Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox journal March 2007
Evidence for Dsg3 in regulating Src signaling by competing with it for binding to caveolin-1 journal March 2016
Molecular phylogeny of choanoflagellates, the sister group to Metazoa journal October 2008
Hierarchical Modularity and the Evolution of Genetic Interactomes across Species journal June 2012
Flux Coupling Analysis of Genome-Scale Metabolic Network Reconstructions journal February 2004
Network medicine: a network-based approach to human disease journal December 2010
Identification of Global Ferredoxin Interaction Networks in Chlamydomonas reinhardtii journal October 2013
Prevalent positive epistasis in Escherichia coli and Saccharomyces cerevisiae metabolic networks journal January 2010
Genome-wide functional annotation and structural verification of metabolic ORFeome of Chlamydomonas reinhardtii journal January 2011
Genome-wide expression analysis offers new insights into the origin and evolution of Physcomitrella patens stress response journal November 2015
Whole-Genome Resequencing Reveals Extensive Natural Variation in the Model Green Alga Chlamydomonas reinhardtii journal September 2015
Systems biology of SNPs journal January 2006
Environmental variability and modularity of bacterial metabolic networks journal January 2007
Conservation and Rewiring of Functional Modules Revealed by an Epistasis Map in Fission Yeast journal October 2008
Empirical fitness landscapes reveal accessible evolutionary paths journal January 2007
Evolutionary Plasticity and Innovations in Complex Metabolic Reaction Networks journal December 2009
Plant type ferredoxins and ferredoxin-dependent metabolism: Chloroplast ferredoxins journal January 2013
Coevolution to the edge of chaos: Coupled fitness landscapes, poised states, and coevolutionary avalanches journal April 1991
Modular co-evolution of metabolic networks journal January 2007
Chance and necessity in the evolution of minimal metabolic networks journal March 2006
Hierarchical thinking in network biology: the unbiased modularization of biochemical networks journal December 2004
Transcriptomic and phylogenetic analysis of a bacterial cell cycle reveals strong associations between gene co-expression and evolution journal January 2013
Evolution of metabolic network organization journal May 2010
BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks journal June 2005
The NK model of rugged fitness landscapes and its application to maturation of the immune response journal November 1989
What is flux balance analysis? journal March 2010
Midpoint redox potentials of plant and algal ferredoxins journal November 1977
Robustness–epistasis link shapes the fitness landscape of a randomly drifting protein journal November 2006
Chance and necessity: the evolution of morphological complexity and diversity journal February 2001
Constraining the metabolic genotype–phenotype relationship using a phylogeny of in silico methods journal February 2012
Evolution of Enzymes in Metabolism: A Network Perspective journal July 2002
Impacts of yeast metabolic network structure on enzyme evolution journal January 2007
Interplay Between Network Structures, Regulatory Modes and Sensing Mechanisms of Transcription Factors in the Transcriptional Regulatory Network of E. coli journal September 2007
Evolution in Mendelian Populations journal March 1931

Cited By (4)

Development of a Chlamydomonas reinhardtii metabolic network dynamic model to describe distinct phenotypes occurring at different CO 2 levels journal January 2018
Potential for Heightened Sulfur-Metabolic Capacity in Coastal Subtropical Microalgae journal January 2019
Algal Cell Factories: Approaches, Applications, and Potentials journal December 2016
The genome and phenome of the green alga Chloroidium sp. UTEX 3007 reveal adaptive traits for desert acclimatization journal June 2017