Metabolic networks of Sodalis glossinidius: A systems biology approach to reductive evolution

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Belda, Eugeni ^a,b,c   Silva, Francisco J ^a,b   Peretó, Juli ^a,b   Moya, Andrés ^a,b  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITY OF VALENCIA   (Spain)

^c CENTRE NATIONAL DE SÉQUENÇAGE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIUM; BUCHNERA APHIDICOLA; CONTROLLED STUDY; ECOLOGY; ENDOSYMBIOSIS; ENVIRONMENTAL FACTOR; ESCHERICHIA COLI; EVOLUTION; GENE INACTIVATION; GENE MUTATION; GENOME ANALYSIS; GENOME REDUCTION; INSECT GENETICS; INSECT GENOME; LIFESTYLE MODIFICATION; METABOLIC PARAMETERS; NONHUMAN; SIMULATION; SODALIS GLOSSINIDIUS; SYSTEMS BIOLOGY; TSETSE FLY; ANIMAL; BACTERIAL GENOME; BIOLOGICAL MODEL; COMPARATIVE STUDY; COMPUTER SIMULATION; DIRECTED MOLECULAR EVOLUTION; ENTEROBACTERIACEAE; ENTEROBACTERIACEAE INFECTION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; METHODOLOGY; MICROBIOLOGY; MOLECULAR EVOLUTION; PHENOTYPE; PHYSIOLOGY; TRANSGENIC ANIMAL;

BACTERIA (MICROORGANISMS); EUKARYOTA; GLOSSINA (GENUS); HEXAPODA; SODALIS GLOSSINIDIUS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; COMPUTER SIMULATION; DIRECTED MOLECULAR EVOLUTION; ENTEROBACTERIACEAE; ENTEROBACTERIACEAE INFECTIONS; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; HOST-PATHOGEN INTERACTIONS; METABOLIC NETWORKS AND PATHWAYS; MODELS, BIOLOGICAL; PHENOTYPE; SYSTEMS BIOLOGY; TSETSE FLIES;

EID: 84856177977     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030652     Document Type: Article

References (77)

1. Moya A, Pereto J, Gil R, Latorre A, (2008) Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat Rev Genet 9: 218-229.
2. Buchner P, (1965) Symbiosis in animals with suck plant juices. In: Buchner P, editors. Endosymbiosis of animals with plant microorganisms New York Interscience pp. 210-432.
3. Baumann P, (2005) Biology bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59: 155-189.
4. Silva FJ, Latorre A, (2008) Genome Reduction During Prokaryotic Evolution. In: Xu Y, Gogarten JP, editors. Computational methods for understanding bacterial and archaeal genomes London Imperial College press pp. 153-184.
5. Moran NA, Plague GR, (2004) Genomic changes following host restriction in bacteria. Curr Opin Genet Dev 14: 627-633.
6. Belda E, Moya A, Silva FJ, (2005) Genome rearrangement distances and gene order phylogeny in gamma-Proteobacteria. Mol Biol Evol 22: 1456-1467.
7. Andersson DI, Hughes D, (1996) Muller's ratchet decreases fitness of a DNA-based microbe. Proc Natl Acad Sci U S A 93: 906-907.
8. Mira A, Ochman H, Moran NA, (2001) Deletional bias and the evolution of bacterial genomes. Trends Genet 17: 589-596.
9. Silva FJ, Latorre A, Moya A, (2001) Genome size reduction through multiple events of gene disintegration in Buchnera APS. Trends Genet 17: 615-618.
10. Gomez-Valero L, Latorre A, Silva FJ, (2004) The evolutionary fate of nonfunctional DNA in the bacterial endosymbiont Buchnera aphidicola. Mol Biol Evol 21: 2172-2181.
11. Gomez-Valero L, Latorre A, Gil R, Gadau J, Feldhaar H, et al. (2008) Patterns and rates of nucleotide substitution, insertion and deletion in the endosymbiont of ants Blochmannia floridanus. Mol Ecol 17 (19): 4382-92.
12. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H, (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407: 81-86.
13. Tamas I, Klasson L, Canback B, Naslund AK, Eriksson AS, et al. (2002) 50 million years of genomic stasis in endosymbiotic bacteria. Science 296: 2376-2379.
14. van Ham RC, Kamerbeek J, Palacios C, Rausell C, Abascal F, et al. (2003) Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci U S A 100: 581-586.
15. Perez-Brocal V, Gil R, Ramos S, Lamelas A, Postigo M, et al. (2006) A small microbial genome: the end of a long symbiotic relationship? Science 314: 312-313.
16. Gil R, Silva FJ, Zientz E, Delmotte F, Gonzalez-Candelas F, et al. (2003) The genome sequence of Blochmannia floridanus: comparative analysis of reduced genomes. Proc Natl Acad Sci U S A 100: 9388-9393.
17. Degnan PH, Lazarus AB, Wernegreen JJ, (2005) Genome sequence of Blochmannia pennsylvanicus indicates parallel evolutionary trends among bacterial mutualists of insects. Genome Res 15: 1023-1033.
18. Nakabachi A, Yamashita A, Toh H, Ishikawa H, Dunbar HE, et al. (2006) The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314: 267.
19. Tamames J, Gil R, Latorre A, Pereto J, Silva FJ, et al. (2007) The frontier between cell and organelle: genome analysis of Candidatus Carsonella ruddii. BMC Evol Biol 7: 181.
20. Andersson JO, Andersson SG, (1999) Genome degradation is an ongoing process in Rickettsia. Mol Biol Evol 16: 1178-1191.
21. Andersson JO, Andersson SG, (2001) Pseudogenes, junk DNA, and the dynamics of Rickettsia genomes. Mol Biol Evol 18: 829-839.
22. Dale C, Maudlin I, (1999) Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans. Int J Syst Bacteriol 49 (Pt 1): 267-275.
23. Akman L, Yamashita A, Watanabe H, Oshima K, Shiba T, et al. (2002) Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat Genet 32: 402-407.
24. Dale C, Beeton M, Harbison C, Jones T, Pontes M, (2006) Isolation, pure culture, and characterization of "Candidatus Arsenophonus arthropodicus", an intracellular secondary endosymbiont from the hippoboscid louse fly Pseudolynchia canariensis. Appl Environ Microbiol 72: 2997-3004.
25. Rio RV, Hu Y, Aksoy S, (2004) Strategies of the home-team: symbioses exploited for vector-borne disease control. Trends Microbiol 12: 325-336.
26. Toh H, Weiss BL, Perkin SA, Yamashita A, Oshima K, et al. (2006) Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res 16: 149-156.
27. Belda E, Moya A, Bentley S, Silva FJ, (2010) Mobile genetic element proliferation and gene inactivation impact over the genome structure and metabolic capabilities of Sodalis glossinidius, the secondary endosymbiont of tsetse flies. BMC Genomics 11: 449.
28. Edwards JS, Palsson BO, (2000) Robustness analysis of the Escherichia coli metabolic network. Biotechnol Prog 16: 927-939.
29. Covert MW, Palsson BO, (2002) Transcriptional regulation in constraints-based metabolic models of Escherichia coli. J Biol Chem 277: 28058-28064.
30. Oberhardt MA, Palsson BO, Papin JA, (2009) Applications of genome-scale metabolic reconstructions. Mol Syst Biol 5: 320.
31. Thomas GH, Zucker J, Macdonald SJ, Sorokin A, Goryanin I, et al. (2009) A fragile metabolic network adapted for cooperation in the symbiotic bacterium Buchnera aphidicola. BMC Syst Biol 3: 24.
32. Pal C, Papp B, Lercher MJ, (2005) Horizontal gene transfer depends on gene content of the host. Bioinformatics 21 (Suppl 2): ii222-ii223.
33. Pal C, Papp B, Lercher MJ, (2005) Adaptive evolution of bacterial metabolic networks by horizontal gene transfer. Nat Genet 37: 1372-1375.
34. Pal C, Papp B, Lercher MJ, Csermely P, Oliver SG, et al. (2006) Chance and necessity in the evolution of minimal metabolic networks. Nature 440: 667-670.
35. Yizhak K, Tuller T, Papp B, Ruppin E, (2011) Metabolic modeling of endosymbiont genome reduction on a temporal scale. Mol Syst Biol 7: 479.
36. Blanc G, Ogata H, Robert C, Audic S, Suhre K, et al. (2007) Reductive genome evolution from the mother of Rickettsia. PLoS Genet 3: e14.
37. Moran NA, McLaughlin HJ, Sorek R, (2009) The dynamics and time scale of ongoing genomic erosion in symbiotic bacteria. Science 323: 379-382.
38. Reed JL, Vo TD, Schilling CH, Palsson BO, (2003) An expanded genome-scale model of Escherichia coli K-12 (iJR904 GSM/GPR). Genome Biol 4: R54.
39. Satishchandran C, Boyle SM, (1986) Purification and properties of agmatine ureohydrolyase, a putrescine biosynthetic enzyme in Escherichia coli. J Bacteriol 165: 843-848.
40. March JC, Eiteman MA, Altman E, (2002) Expression of an anaplerotic enzyme, pyruvate carboxylase, improves recombinant protein production in Escherichia coli. Appl Environ Microbiol 68: 5620-5624.
41. Peng L, Rauzo-Bravo MJ, Shimizu K, (2004) Metabolic flux analysis for a ppc mutant Escherichia coli based on 13C-labelling experiments together with enzyme activity assays and intracellular metabolite measurements. FEMS Microbiol Lett 235: 17-23.
42. Peng L, Shimizu K, (2004) Effect of ppc gene knockout on the metabolism of Escherichia coli in view of gene expressions, enzyme activities and intracellular metabolite concentrations. Appl Microbiol Biotechnol 13.
43. Suthers PF, Zomorrodi A, Maranas CD, (2009) Genome-scale gene/reaction essentiality and synthetic lethality analysis. Mol Syst Biol 5: 301.
44. Gerdes SY, Scholle MD, Campbell JW, Balazsi G, Ravasz E, et al. (2003) Experimental determination and system level analysis of essential genes in Escherichia coli MG1655. J Bacteriol 185: 5673-5684.
45. Burke GR, Moran NA, (2011) Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol Evol 3: 195-208.
46. Edwards JS, Palsson BO, (2000) The Escherichia coli MG1655 in silico metabolic genotype: its definition, characteristics, and capabilities. Proc Natl Acad Sci U S A 97: 5528-5533.
47. Forster J, Famili I, Fu P, Palsson BO, Nielsen J, (2003) Genome-scale reconstruction of the Saccharomyces cerevisiae metabolic network. Genome Res 13: 244-253.
48. Lee DS, Burd H, Liu J, Almaas E, Wiest O, et al. (2009) Comparative genome-scale metabolic reconstruction and flux balance analysis of multiple Staphylococcus aureus genomes identify novel antimicrobial drug targets. J Bacteriol 191: 4015-4024.
49. Puchalka J, Oberhardt MA, Godinho M, Bielecka A, Regenhardt D, et al. (2008) Genome-scale reconstruction and analysis of the Pseudomonas putida KT2440 metabolic network facilitates applications in biotechnology. PLoS Comput Biol 4: e1000210.
50. Oberhardt MA, Puchalka J, Fryer KE, Martins dos Santos V, Papin JA, (2008) Genome-scale metabolic network analysis of the opportunistic pathogen Pseudomonas aeruginosa PAO1. J Bacteriol 190: 2790-2803.
51. Zhang Y, Thiele I, Weekes D, Li Z, Jaroszewski L, et al. (2009) Three-dimensional structural view of the central metabolic network of Thermotoga maritima. Science 325: 1544-1549.
52. Chen X, Li S, Aksoy S, (1999) Concordant evolution of a symbiont with its host insect species: molecular phylogeny of genus Glossina and its bacteriome-associated endosymbiont, Wigglesworthia glossinidia. J Mol Evol 48: 49-58.
53. Welburn SC, Maudlin I, Ellis DS, (1987) In vitro cultivation of rickettsia-like-organisms from Glossina spp. Ann Trop Med Parasitol 81: 331-335.
54. Jeong H, Tombor B, Albert R, Oltvai ZN, Barabasi AL, (2000) The large-scale organization of metabolic networks. Nature 407: 651-654.
55. Albert R, Jeong H, Barabasi AL, (2000) Error and attack tolerance of complex networks. Nature 406: 378-382.
56. Podani J, Oltvai ZN, Jeong H, Tombor B, Barabasi AL, et al. (2001) Comparable system-level organization of Archaea and Eukaryotes. Nat Genet 29: 54-56.
57. Barabasi AL, Oltvai ZN, (2004) Network biology: understanding the cell's functional organization. Nat Rev Genet 5: 101-113.
58. Joyce AR, Reed JL, White A, Edwards R, Osterman A, et al. (2006) Experimental and computational assessment of conditionally essential genes in Escherichia coli. J Bacteriol 188: 8259-8271.
59. Gabaldon T, Pereto J, Montero F, Gil R, Latorre A, et al. (2007) Structural analyses of a hypothetical minimal metabolism. Philos Trans R Soc Lond B Biol Sci 362: 1751-1762.
60. Gil R, Silva FJ, Pereto J, Moya A, (2004) Determination of the core of a minimal bacterial gene set. Microbiol Mol Biol Rev 68: 518-537.
61. Silva FJ, Latorre A, Gomez-Valero L, Moya A, (2007) Genomic changes in bacteria: From free-living to endosymbiotic life. In: Bastolla U, Porto M, Roman E, Vendruscolo M, editors. Structural approaches to sequence evolution Springerlink pp. 149-165.
62. Silva FJ, Latorre A, Moya A, (2003) Why are the genomes of endosymbiotic bacteria so stable? Trends Genet 19: 176-180.
63. Sharples GJ, (2009) For absent friends: life without recombination in mutualistic gamma-proteobacteria. Trends Microbiol 17: 233-242.
64. Mushegian AR, Koonin EV, (1996) A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc Natl Acad Sci U S A 93: 10268-10273.
65. Koonin EV, (2000) How many genes can make a cell: the minimal-gene-set concept. Annu Rev Genomics Hum Genet 1: 99-116.
66. Klasson L, Andersson SG, (2004) Evolution of minimal-gene-sets in host-dependent bacteria. Trends Microbiol 12: 37-43.
67. Hutchison CA, Peterson SN, Gill SR, Cline RT, White O, et al. (1999) Global transposon mutagenesis and a minimal Mycoplasma genome. Science 286: 2165-2169.
68. Kobayashi K, Ehrlich SD, Albertini A, Amati G, Andersen KK, et al. (2003) Essential Bacillus subtilis genes. Proc Natl Acad Sci U S A 100: 4678-4683.
69. Soyer OS, Pfeiffer T, (2010) Evolution under fluctuating environments explains observed robustness in metabolic networks. PLoS Comput Biol 6: e1000907 doi:10.1371/journal.pcbi.1000907.
70. Suyama M, Bork P, (2001) Evolution of prokaryotic gene order: genome rearrangements in closely related species. Trends Genet 17: 10-13.
71. Mira A, Klasson L, Andersson SG, (2002) Microbial genome evolution: sources of variability. Curr Opin Microbiol 5: 506-512.
72. Koonin EV, Wolf YI, (2008) Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res 36: 6688-6719.
73. Moran NA, Mira A, (2001) The process of genome shrinkage in the obligate symbiont Buchnera aphidicola. Genome Biol 2: RESEARCH0054.
74. Boussau B, Karlberg EO, Frank AC, Legault BA, Andersson SG, (2004) Computational inference of scenarios for alpha-proteobacterial genome evolution. Proc Natl Acad Sci U S A 101: 9722-9727.
75. Lewis NE, Hixson KK, Conrad TM, Lerman JA, Charusanti P, et al. (2010) Omic data from evolved E. coli are consistent with computed optimal growth from genome-scale models. Mol Syst Biol 6: 390.
76. Papp B, Notebaart RA, Pal C, (2011) Systems-biology approaches for predicting genomic evolution. Nat Rev Genet 12: 591-602.
77. Becker SA, Feist AM, Mo ML, Hannum G, Palsson BO, et al. (2007) Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox. Nat Protoc 2: 727-738.