Metabolic modeling of endosymbiont genome reduction on a temporal scale

A fundamental challenge in Systems Biology is whether a cell‐scale metabolic model can predict patterns of genome evolution by realistically accounting for associated biochemical constraints. Here, we study the order in which genes are lost in an in silico evolutionary process, leading from the metabolic network of Eschericia coli to that of the endosymbiont Buchnera aphidicola. We examine how this order correlates with the order by which the genes were actually lost, as estimated from a phylogenetic reconstruction. By optimizing this correlation across the space of potential growth and biomass conditions, we compute an upper bound estimate on the model's prediction accuracy (R=0.54). The model's network‐based predictive ability outperforms predictions obtained using genomic features of individual genes, reflecting the effect of selection imposed by metabolic stoichiometric constraints. Thus, while the timing of gene loss might be expected to be a completely stochastic evolutionary process, remarkably, we find that metabolic considerations, on their own, make a marked 40% contribution to determining when such losses occur.

[1]  J. Neyman.  MOLECULAR STUDIES OF EVOLUTION: A SOURCE OF NOVEL STATISTICAL PROBLEMS* , 1971 .

[2]  N. Moran,et al.  Molecular Interactions between Bacterial Symbionts and Their Hosts , 2006, Cell.

[3]  N. Moran,et al.  50 Million Years of Genomic Stasis in Endosymbiotic Bacteria , 2002, Science.

[4]  S. Oliver,et al.  Chance and necessity in the evolution of minimal metabolic networks , 2006, Nature.

[5]  D. Sankoff.  Minimal Mutation Trees of Sequences , 1975 .

[6]  C. D. Gelatt,et al.  Optimization by Simulated Annealing , 1983, Science.

[7]  T. Jukes.  CHAPTER 24 – Evolution of Protein Molecules , 1969 .

[8]  U. Gophna,et al.  Reconstructing ancestral gene content by coevolution. , 2010, Genome research.

[9]  Paulien Hogeweg,et al.  Metabolic adaptation after whole genome duplication. , 2009, Molecular biology and evolution.

[10]  Phat L Tran,et al.  Metabolic Complementarity and Genomics of the Dual Bacterial Symbiosis of Sharpshooters , 2006, PLoS biology.

[11]  Chi-Yung Lai,et al.  Amplification of trpEG: adaptation of Buchnera aphidicola to an endosymbiotic association with aphids. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[12]  B. Snel,et al.  Toward Automatic Reconstruction of a Highly Resolved Tree of Life , 2006, Science.

[13]  Ziheng Yang,et al.  PAML: a program package for phylogenetic analysis by maximum likelihood , 1997, Comput. Appl. Biosci..

[14]  L. Wernisch,et al.  Solving the riddle of codon usage preferences: a test for translational selection. , 2004, Nucleic acids research.

[15]  Alfonso Valencia,et al.  Modular organization in the reductive evolution of protein-protein interaction networks , 2007, Genome Biology.

[16]  N. Moran,et al.  Bacterial endosymbionts in animals. , 2000, Current opinion in microbiology.

[17]  A. Moya,et al.  Genome size reduction through multiple events of gene disintegration in Buchnera APS. , 2001, Trends in genetics : TIG.

[18]  Andrés Moya,et al.  Extreme genome reduction in Buchnera spp.: Toward the minimal genome needed for symbiotic life , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[19]  M. Hattori,et al.  Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS , 2000, Nature.

[20]  Kenneth J. Kauffman,et al.  Advances in flux balance analysis. , 2003, Current opinion in biotechnology.

[21]  Bernhard O. Palsson,et al.  Matrix Formalism to Describe Functional States of Transcriptional Regulatory Systems , 2006, PLoS Comput. Biol..

[22]  Bas E Dutilh,et al.  Asymmetric relationships between proteins shape genome evolution , 2009, Genome Biology.

[23]  Adam M. Feist,et al.  Reconstruction of biochemical networks in microorganisms , 2009, Nature Reviews Microbiology.

[24]  N. Moran,et al.  A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[25]  S. Jeffery.  Evolution of Protein Molecules , 1979 .

[26]  N. Moran,et al.  The process of genome shrinkage in the obligate symbiont Buchnera aphidicola , 2001, Genome Biology.

[27]  A. Douglas,et al.  Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. , 1998, Annual review of entomology.

[28]  N. Moran,et al.  Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. , 1995, Annual review of microbiology.

[29]  Darren A. Natale,et al.  The COG database: an updated version includes eukaryotes , 2003, BMC Bioinformatics.

[30]  B. Palsson,et al.  Genome-scale models of microbial cells: evaluating the consequences of constraints , 2004, Nature Reviews Microbiology.

[31]  Laurent Duret,et al.  Differential retention of metabolic genes following whole-genome duplication. , 2009, Molecular biology and evolution.

[32]  B. Palsson,et al.  Metabolic Flux Balancing: Basic Concepts, Scientific and Practical Use , 1994, Bio/Technology.

[33]  Igor Goryanin,et al.  A fragile metabolic network adapted for cooperation in the symbiotic bacterium Buchnera aphidicola , 2009, BMC Systems Biology.

[34]  Eytan Ruppin,et al.  Translation efficiency is determined by both codon bias and folding energy , 2010, Proceedings of the National Academy of Sciences.

[35]  P. Sharp,et al.  The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications. , 1987, Nucleic acids research.

[36]  Adam M. Feist,et al.  A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information , 2007, Molecular systems biology.

[37]  Jason A. Papin,et al.  Applications of genome-scale metabolic reconstructions , 2009, Molecular systems biology.

[38]  N. Moran,et al.  Bacterial Genes in the Aphid Genome: Absence of Functional Gene Transfer from Buchnera to Its Host , 2010, PLoS genetics.

[39]  Ludovic Cottret,et al.  Systemic analysis of the symbiotic function of Buchnera aphidicola, the primary endosymbiont of the pea aphid Acyrthosiphon pisum. , 2009, Comptes rendus biologies.

[40]  Markus J. Herrgård,et al.  Integrating high-throughput and computational data elucidates bacterial networks , 2004, Nature.

[41]  A. Douglas.  Symbiotic microorganisms: untapped resources for insect pest control. , 2007, Trends in biotechnology.

[42]  A. Moya,et al.  Tempo and mode of early gene loss in endosymbiotic bacteria from insects , 2006, BMC Evolutionary Biology.

[43]  W. Fitch.  Toward Defining the Course of Evolution: Minimum Change for a Specific Tree Topology , 1971 .

[44]  D. Fell,et al.  Fat synthesis in adipose tissue. An examination of stoichiometric constraints. , 1986, The Biochemical journal.

[45]  N. Moran,et al.  The Dynamics and Time Scale of Ongoing Genomic Erosion in Symbiotic Bacteria , 2009, Science.

[46]  C. Pál,et al.  Adaptive evolution of bacterial metabolic networks by horizontal gene transfer , 2005, Nature Genetics.

[47]  B. Palsson,et al.  An expanded genome-scale model of Escherichia coli K-12 (iJR904 GSM/GPR) , 2003, Genome Biology.

[48]  Alfonso Valencia,et al.  Reductive genome evolution in Buchnera aphidicola , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[49]  C. Schilling,et al.  Flux coupling analysis of genome-scale metabolic network reconstructions. , 2004, Genome research.

[50]  Hidemi Watanabe,et al.  Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia , 2002, Nature Genetics.

[51]  E. Ruppin,et al.  Multiple knockout analysis of genetic robustness in the yeast metabolic network , 2006, Nature Genetics.