Systemic analysis of the symbiotic function of Buchnera aphidicola, the primary endosymbiont of the pea aphid Acyrthosiphon pisum.

Buchnera aphidicola is the primary obligate intracellular symbiont of most aphid species. B. aphidicola and aphids have been evolving in parallel since their association started, about 150 Myr ago. Both partners have lost their autonomy, and aphid diversification has been confined to smaller ecological niches by this co-evolution. B. aphidicola has undergone major genomic and biochemical changes as a result of adapting to intracellular life. Several genomes of B. aphidicola from different aphid species have been sequenced in the last decade, making it possible to carry out analyses and comparative studies using system-level in silico methods. This review attempts to provide a systemic description of the symbiotic function of aphid endosymbionts, particularly of B. aphidicola from the pea aphid Acyrthosiphon pisum, by analyzing their structural genomic properties, as well as their genetic and metabolic networks.

[1]  Reinhard Diestel,et al.  Graph Theory , 1997 .

[2]  Andrés Moya,et al.  A Small Microbial Genome: The End of a Long Symbiotic Relationship? , 2006, Science.

[3]  A. Moya,et al.  Why are the genomes of endosymbiotic bacteria so stable? , 2003, Trends in genetics : TIG.

[4]  A. Nakabachi,et al.  Aphids acquired symbiotic genes via lateral gene transfer , 2009, BMC Biology.

[5]  A. Douglas Conflict, cheats and the persistence of symbioses. , 2008, The New phytologist.

[6]  A. Douglas,et al.  Partitioning of Symbiotic Bacteria between Generations of an Insect: a Quantitative Study of a Buchnera sp. in the Pea Aphid (Acyrthosiphon pisum) Reared at Different Temperatures , 1997, Applied and environmental microbiology.

[7]  H. Ishikawa,et al.  Intracellular Bacterial Symbionts of Aphids Possess Many Genomic Copies per Bacterium , 1999, Journal of Molecular Evolution.

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

[9]  H. Harada,et al.  A consideration about the origin of aphid intracellular symbiont in connection with gut bacterial flora , 1996 .

[10]  A. Maxmen,et al.  Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress , 2002 .

[11]  H. Ishikawa,et al.  Production of essential amino acids from glutamate by mycetocyte symbionts of the pea aphid, Acyrthosiphon pisum , 1995 .

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

[13]  N. Moran,et al.  Regulation of Transcription in a Reduced Bacterial Genome: Nutrient-Provisioning Genes of the Obligate Symbiont Buchnera aphidicola , 2005, Journal of bacteriology.

[14]  N. Moran,et al.  Sequence evolution in bacterial endosymbionts having extreme base compositions. , 1999, Molecular biology and evolution.

[15]  A. Moya,et al.  The evolution of the heat-shock protein GroEL from Buchnera, the primary endosymbiont of aphids, is governed by positive selection. , 2002, Molecular biology and evolution.

[16]  A. Moya,et al.  Mutational and selective pressures on codon and amino acid usage in Buchnera, endosymbiotic bacteria of aphids. , 2003, Genome research.

[17]  A. E. Douglas Sulphate utilization in an aphid symbiosis , 1988 .

[18]  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.

[19]  N. Moran,et al.  Evolutionary rates for tuf genes in endosymbionts of aphids. , 1998, Molecular biology and evolution.

[20]  J. Galán,et al.  Supramolecular structure of the Salmonella typhimurium type III protein secretion system. , 1998, Science.

[21]  N. Moran,et al.  Evolutionary Origins of Genomic Repertoires in Bacteria , 2005, PLoS biology.

[22]  P. Buchner Endosymbiosis of Animals with Plant Microorganisms , 1965 .

[23]  M. Munson,et al.  Buchnera gen. nov. and Buchnera aphidicola sp. nov., a Taxon Consisting of the Mycetocyte-Associated, Primary Endosymbionts of Aphids , 1991 .

[24]  M. Fares,et al.  The evolution of the flagellar assembly pathway in endosymbiotic bacterial genomes. , 2008, Molecular biology and evolution.

[25]  N. Moran,et al.  Costs and benefits of a superinfection of facultative symbionts in aphids , 2006, Proceedings of the Royal Society B: Biological Sciences.

[26]  D. Mouchiroud,et al.  Gene size reduction in the bacterial aphid endosymbiont, Buchnera. , 1999, Molecular biology and evolution.

[27]  N. Moran Bacterial menageries inside insects. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[28]  H. Ishikawa,et al.  Genomic copy number of intracellular bacterial symbionts of aphids varies in response to developmental stage and morph of their host. , 2000, Insect biochemistry and molecular biology.

[29]  N. Moran,et al.  Tracing the evolution of gene loss in obligate bacterial symbionts. , 2003, Current opinion in microbiology.

[30]  Federica Calevro,et al.  Different Levels of Transcriptional Regulation Due to Trophic Constraints in the Reduced Genome of Buchnera aphidicola APS , 2006, Applied and Environmental Microbiology.

[31]  N. Moran,et al.  Evolutionary Relationships of Three New Species of Enterobacteriaceae Living as Symbionts of Aphids and Other Insects , 2005, Applied and Environmental Microbiology.

[32]  N. Moran,et al.  Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families , 1991, Journal of bacteriology.

[33]  N. Moran,et al.  Intraspecific variation in symbiont genomes: bottlenecks and the aphid-buchnera association. , 2001, Genetics.

[34]  N. Moran,et al.  Consequences of reductive evolution for gene expression in an obligate endosymbiont , 2003, Molecular microbiology.

[35]  A. Moya,et al.  Chromosomal stasis versus plasmid plasticity in aphid endosymbiont Buchnera aphidicola , 2005, Heredity.

[36]  N. Moran Accelerated evolution and Muller's rachet in endosymbiotic bacteria. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[37]  T. Fukatsu,et al.  Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[38]  J. Fayard,et al.  Codon usage bias and tRNA over-expression in Buchnera aphidicola after aromatic amino acid nutritional stress on its host Acyrthosiphon pisum , 2006, Nucleic acids research.

[39]  G. Febvay,et al.  Analysis of energetic amino acid metabolism in Acyrthosiphon pisum: A multidimensional approach to amino acid metabolism in aphids , 1995 .

[40]  J. R. Lobry,et al.  Oriloc: prediction of replication boundaries in unannotated bacterial chromosomes , 2000, Bioinform..

[41]  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.

[42]  Arkady B Khodursky,et al.  Spatial patterns of transcriptional activity in the chromosome of Escherichia coli , 2004, Genome Biology.

[43]  N. Moran,et al.  Facultative bacterial symbionts in aphids confer resistance to parasitic wasps , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[44]  T. Miura,et al.  Developmental Origin and Evolution of Bacteriocytes in the Aphid–Buchnera Symbiosis , 2003, PLoS biology.

[45]  Rahbe,et al.  Fate of dietary sucrose and neosynthesis of amino acids in the pea aphid, acyrthosiphon pisum, reared on different diets , 1999, The Journal of experimental biology.

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

[47]  P. Baumann,et al.  Levels of Buchnera aphidicola Chaperonin GroEL During Growth of the Aphid Schizaphis graminum , 1996, Current Microbiology.

[48]  N. Moran,et al.  The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[49]  G. Febvay,et al.  Metabolic Fate of Energetic Amino Acids in the Aposymbiotic Pea Aphid Acyrthosiphon pisum (Harris) (Homoptera: Aphididae) , 1996 .

[50]  Joshua T Herbeck,et al.  Nonhomogeneous model of sequence evolution indicates independent origins of primary endosymbionts within the enterobacteriales (gamma-Proteobacteria). , 2005, Molecular biology and evolution.

[51]  N. Moran,et al.  Molecular data support a rapid radiation of aphids in the Cretaceous and multiple origins of host alternation , 2000 .

[52]  H. Charles,et al.  Endosymbiont phylogenesis in the dryophthoridae weevils: evidence for bacterial replacement. , 2004, Molecular biology and evolution.

[53]  N. Moran,et al.  Accumulation of Deleterious Mutations in Endosymbionts: Muller’s Ratchet with Two Levels of Selection , 2000, The American Naturalist.

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

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

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

[57]  J. Viñuelas,et al.  Impact of Host Developmental Age on the Transcriptome of the Symbiotic Bacterium Buchnera aphidicola in the Pea Aphid (Acyrthosiphon pisum) , 2009, Applied and Environmental Microbiology.

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

[59]  Federica Calevro,et al.  Conservation of the links between gene transcription and chromosomal organization in the highly reduced genome of Buchnera aphidicola , 2007, BMC Genomics.

[60]  Javier Arsuaga,et al.  Genomic transcriptional response to loss of chromosomal supercoiling in Escherichia coli , 2004, Genome Biology.

[61]  B. Sabater-Muñoz,et al.  Plasmids in the aphid endosymbiont Buchnera aphidicola with the smallest genomes. A puzzling evolutionary story. , 2006, Gene.

[62]  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.

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

[64]  N. Moran,et al.  Functional genomics of Buchnera and the ecology of aphid hosts , 2005, Molecular ecology.

[65]  H. Charles,et al.  A putative insect intracellular endosymbiont stem clade, within the Enterobacteriaceae, infered from phylogenetic analysis based on a heterogeneous model of DNA evolution. , 2001, Comptes rendus de l'Academie des sciences. Serie III, Sciences de la vie.

[66]  A. Douglas Phloem-sap feeding by animals: problems and solutions. , 2006, Journal of experimental botany.

[67]  A. Moya,et al.  Discovery and molecular characterization of a plasmid localized in Buchnera sp. bacterial endosymbiont of the aphid Rhopalosiphum padi , 1995, Journal of Molecular Evolution.

[68]  A. Douglas,et al.  Synthesis of the essential amino acid tryptophan in the pea aphid (Acyrthosiphon pisum) symbiosis , 1992 .

[69]  Hajime Ishikawa,et al.  The 160-Kilobase Genome of the Bacterial Endosymbiont Carsonella , 2006, Science.

[70]  M. Fares,et al.  Selection for translational robustness in Buchnera aphidicola, endosymbiotic bacteria of aphids. , 2009, Molecular biology and evolution.

[71]  A. Moya,et al.  The Striking Case of Tryptophan Provision in the Cedar Aphid Cinara cedri , 2008, Journal of bacteriology.

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

[73]  A. Moya,et al.  Determination of the Core of a Minimal Bacterial Gene Set , 2004, Microbiology and Molecular Biology Reviews.

[74]  Bruno Torrésani,et al.  Decoding the nucleoid organisation of Bacillus subtilis and Escherichia coli through gene expression data , 2005, BMC Genomics.

[75]  N. Moran,et al.  A genomic perspective on nutrient provisioning by bacterial symbionts of insects , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[76]  T. Fukatsu,et al.  Host Plant Specialization Governed by Facultative Symbiont , 2004, Science.

[77]  H. Ishikawa,et al.  Symbionin, an aphid endosymbiont-specific protein—I: Production of insects deficient in symbiont , 1985 .

[78]  T. Fukatsu,et al.  A novel eukaryotic extracellular symbiont in an aphid, Astegopteryx styraci (Homoptera, Aphididae, Hormaphidinae) , 1992 .

[79]  Ran Blekhman,et al.  The "domino theory" of gene death: gradual and mass gene extinction events in three lineages of obligate symbiotic bacterial pathogens. , 2006, Molecular biology and evolution.

[80]  Thomas Dandekar,et al.  Metabolic Interdependence of Obligate Intracellular Bacteria and Their Insect Hosts , 2004, Microbiology and Molecular Biology Reviews.

[81]  Michael J. Smith,et al.  The Yersinia enterocolitica Motility Master Regulatory Operon, flhDC, Is Required for Flagellin Production, Swimming Motility, and Swarming Motility , 1999, Journal of bacteriology.

[82]  T. Fukatsu,et al.  Transmission of symbiotic bacteria Buchnera to parthenogenetic embryos in the aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). , 2003, Arthropod structure & development.

[83]  Paulien Hogeweg,et al.  The role of mutational dynamics in genome shrinkage. , 2007, Molecular biology and evolution.

[84]  J. Fayard,et al.  Assessment of 35mer amino-modified oligonucleotide based microarray with bacterial samples. , 2004, Journal of microbiological methods.