Abstract
Symbioses involving prokaryotes living in close relationship with eukaryotic cells have been widely studied from a genomic perspective, especially in the case of insects. In the process toward host accommodation, symbionts experience major genetic and phenotypic changes that can be detected in comparison with free-living relatives. But, as expected, several scenarios allowed the evolution of symbiotic associations, from the first stages of free-living bacteria, through secondary and facultative symbiosis, towards the final point of obligate primary endosymbiosis. Particular relevance has the association formed by the coexistence of several symbionts into a given host. A summary of findings in this field, as well as an evolutionary scenario to explain these changes, is presented in this chapter.
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Andersson SG, Kurland CG (1998) Reductive evolution of resident genomes. Trends Microbiol 6:263–268
Baumann P (2005) Biology bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59:155–189
Baumann L, Baumann P (1994) Growth kinetics of the endosymbiont Buchnera aphidicola in the aphid Schizaphis graminum. Appl Environ Microbiol 60:3440–3443
Baumann L, Thao ML, Hess JM, Johnson MW, Baumann P (2002) The genetic properties of the primary endosymbionts of mealybugs differ from those of other endosymbionts of plant sap-sucking insects. Appl Environ Microbiol 68:3198–3205
Bordenstein SR, Reznikoff WS (2005) Mobile DNA in obligate intracellular bacteria. Nat Rev Microbiol 3:688–699
Bordenstein SR, Wernegreen JJ (2004) Bacteriophage flux in endosymbionts (Wolbachia): infection frequency, lateral transfer, and recombination rates. Mol Biol Evol 21:1981–1991
Brochier C, Gribaldo S, Zivanovic Y, Confalonieri F, Forterre P (2005) Nanoarchaea: representatives of a novel archaeal phylum or a fast-evolving euryarchaeal lineage related to Thermococcales? Genome Biol 6:R42
Buchner P (1965) Endosymbiosis of animals with plant microorganisms. Interscience Publishers, New York
Casjens S (1998) The diverse and dynamic structure of bacterial genomes. Annu Rev Genet 32:339–377
Charles H, Heddi A, Guillaud J, Nardon C, Nardon P (1997) A molecular aspect of symbiotic interactions between the weevil Sitophilus oryzae and its endosymbiotic bacteria: over-expression of a chaperonin. Biochem Biophys Res Commun 239:769–774
Chen D-Q, Montllor CB, Purcell AH (2000) Fitness effects of two facultative endosymbiotic bacteria on the pea aphid, Acyrthosiphon pisum, and the blue alfalfa aphid A. kondoi. Entomol Exp Appl 95:315–323
Clark MA, Moran NA, Baumann P (1999) Sequence evolution in bacterial endosymbionts having extreme base compositions. Mol Biol Evol 16:1586–1598
Cole ST, Eiglmeier K, Parkhill J, James KD, Thomson NR, Wheeler PR, Honore N, Garnier T, Churcher C, Harris D, Mungall K, Basham D, Brown D, Chillingworth T, Connor R, Davies RM, Devlin K, Duthoy S, Feltwell T, Fraser A, Hamlin N, Holroyd S, Hornsby T, Jagels K, Lacroix C, Maclean J, Moule S, Murphy L, Oliver K, Quail MA, Rajandream MA, Rutherford KM, Rutter S, Seeger K, Simon S, Simmonds M, Skelton J, Squares R, Squares S, Stevens K, Taylor K, Whitehead S, Woodward JR, Barrell BG (2001) Massive gene decay in the leprosy bacillus. Nature 409:1007–1011
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
Dale C, Moran NA (2006) Molecular interactions between bacterial symbionts and their hosts. Cell 126:453–465
Dale C, Welburn SC (2001) The endosymbionts of tsetse flies: manipulating host-parasite interactions. Int J Parasitol 31:628–631
Dale C, Young SA, Haydon DT, Welburn SC (2001) The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc Natl Acad Sci USA 98:1883–1888
Dale C, Plague GR, Wang B, Ochman H, Moran NA (2002) Type III secretion systems and the evolution of mutualistic endosymbiosis. Proc Natl Acad Sci USA 99:12397–12402
Dale C, Wang B, Moran N, Ochman H (2003) Loss of DNA recombinational repair enzymes in the initial stages of genome degeneration. Mol Biol Evol 20:1188–1194
Degnan PH, Moran NA (2008) Diverse phage-encoded toxins in a protective insect endosymbiont. Appl Environ Microbiol 74:6782–6791
Degnan PH, Leonardo TE, Cass BN, Hurwitz B, Stern D, Gibbs RA, Richards S, Moran NA (2009a) Dynamics of genome evolution in facultative symbionts of aphids. Environ Microbiol. October 16, Epub ahead of print
Degnan PH, Yu Y, Sisneros N, Wing RA, Moran NA (2009b) Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc Natl Acad Sci USA 106:9063–9068
Dougherty KM, Plague GR (2008) Transposable element loads in a bacterial symbiont of weevils are extremely variable. Appl Environ Microbiol 74:7832–7834
Ferrari J, Darby AC, Daniell HCJG, Douglas AE (2004) Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecol Entomol 29:60–65
Fiala-Médioni A, Michalski JC, Jollès J, Alonso C, Montreuil J (1994) Lysosomic and lysosome activities in gills of bivalves from deep hydrothermal vents. C R Acad Sci Paris 317:239–244
Forterre P, Gribaldo S, Brochier-Armanet C (2009) Happy together: genomic insights into the unique Nanoarchaeum/Ignicoccus association. J Biol 8:7
Foster J, Ganatra M, Kamal I, Ware J, Makarova K, Ivanova N, Bhattacharyya A, Kapatral V, Kumar S, Posfai J, Vincze T, Ingram J, Moran L, Lapidus A, Omelchenko M, Kyrpides N, Ghedin E, Wang S, Goltsman E, Joukov V, Ostrovskaya O, Tsukerman K, Mazur M, Comb D, Koonin E, Slatko B (2005) The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol 3:e121
Gil R, Sabater-Munoz B, Latorre A, Silva FJ, Moya A (2002) Extreme genome reduction in Buchnera spp.: toward the minimal genome needed for symbiotic life. Proc Natl Acad Sci USA 99:4454–4458
Gil R, Silva FJ, Zientz E, Delmotte F, Gonzalez-Candelas F, Latorre A, Rausell C, Kamerbeek J, Gadau J, Hölldobler B, van Ham RCHJ, Gross R, Moya A (2003) The genome sequence of Blochmannia floridanus: comparative analysis of reduced genomes. Proc Natl Acad Sci USA 100:9388–9393
Gil R, Latorre A, Moya A (2004a) Bacterial endosymbionts of insects: insights from comparative genomics. Environ Microbiol 6:1109–1122
Gil R, Silva FJ, Pereto J, Moya A (2004b) Determination of the core of a minimal bacterial gene set. Microbiol Mol Biol Rev 68:518–537
Gil R, Belda E, Gosalbes MJ, Delaye L, Vallier A, Vincent-Monegat C, Heddi A, Silva FJ, Moya A, Latorre A (2008) Massive presence of insertion sequences in the genome of SOPE, the primary endosymbiont of the rice weevil Sitophilus oryzae. Int Microbiol 11:41–48
Goebel W, Gross R (2001) Intracellular survival strategies of mutualistic and parasitic prokaryotes. Trends Microbiol 9:267–273
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
Gomez-Valero L, Rocha EP, Latorre A, Silva FJ (2007) Reconstructing the ancestor of Mycobacterium leprae: the dynamics of gene loss and genome reduction. Genome Res 17:1178–1185
Gosalbes MJ, Lamelas A, Moya A, Latorre A (2008) The striking case of tryptophan provision in the cedar aphid Cinara cedri. J Bacteriol 190:6026–6029
Guay J-F, Boudreault S, Michaud D, Cloutier C (2009) Impact of environmental stress on aphid clonal resistance to parasitoids: role of Hamiltonella defensa bacterial symbiosis in association with a new facultative symbiont of the pea aphid. J Insect Physiol 55:919–926
Hackstein JHP, van Alen TA, Rosenberg J (2006) Methane production by terrestrial arthropods. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Springer, Heidelberg, pp 155–182
Heddi A, Charles H, Khatchadourian C, Bonnot G, Nardon P (1998) Molecular characterization of the principal symbiotic bacteria of the weevil Sitophilus oryzae: a peculiar G + C content of an endocytobiotic DNA. J Mol Evol 47:52–61
Heddi A, Grenier AM, Khatchadourian C, Charles H, Nardon P (1999) Four intracellular genomes direct weevil biology: nuclear, mitochondrial, principal endosymbiont, and Wolbachia. Proc Natl Acad Sci USA 96:6814–6819
Jin Q, Yuan Z, Xu J, Wang Y, Shen Y, Lu W, Wang J, Liu H, Yang J, Yang F, Zhang X, Zhang J, Yang G, Wu H, Qu D, Dong J, Sun L, Xue Y, Zhao A, Gao Y, Zhu J, Kan B, Ding K, Chen S, Cheng H, Yao Z, He B, Chen R, Ma D, Qiang B, Wen Y, Hou Y, Yu J (2002) Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157. Nucleic Acids Res 30:4432–4441
Klasson L, Walker T, Sebaihia M, Sanders MJ, Quail MA, Lord A, Sanders S, Earl J, O'Neill SL, Thomson N, Sinkins SP, Parkhill J (2008) Genome evolution of Wolbachia strain wPip from the Culex pipiens group. Mol Biol Evol 25:1877–1887
Klasson L, Westberg J, Sapountzis P, Naslund K, Lutnaes Y, Darby AC, Veneti Z, Chen L, Braig HR, Garrett R, Bourtzis K, Andersson SG (2009) The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proc Natl Acad Sci USA 106:5725–5730
Koga R, Tsuchida T, Fukatsu T (2003) Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc Biol Sci 270:2543–2550
Kono M, Koga R, Shimada M, Fukatsu T (2008) Infection dynamics of coexisting beta- and gammaproteobacteria in the nested endosymbiotic system of mealybugs. Appl Environ Microbiol 74:4175–4184
Latorre A, Gil R, Silva FJ, Moya A (2005) Chromosomal stasis versus plasmid plasticity in aphid endosymbiont Buchnera aphidicola. Heredity 95:339–347
Lefevre C, Charles H, Vallier A, Delobel B, Farrell B, Heddi A (2004) Endosymbiont phylogenesis in the Dryophthoridae weevils: evidence for bacterial Replacement. Mol Biol Evol 21:965–973
Lopez-Sanchez MJ, Neef A, Patino-Navarrete R, Navarro L, Jimenez R, Latorre A, Moya A (2008) Blattabacteria, the endosymbionts of cockroaches, have small genome sizes and high genome copy numbers. Environ Microbiol 10:3417–3422
López-Sánchez MJ, Neef A, Peretó J, Patiño-Navarrete R, Pignatelli M, Latorre A, Moya A (2009) Evolutionary convergence and nitrogen metabolism in Blattabacterium strain Bge, primary endosymbiont of the cockroach Blattella germanica. PLoS Genet 5:e1000721
Luisi PL, Oberholzer T, Lazcano A (2002) The notion of a DNA minimal cell: a general discourse and some gidelines for an experimental approach. Helv Chim Acta 85:1759–1777
Makarova KS, Koonin EV (2005) Evolutionary and functional genomics of the Archaea. Curr Opin Microbiol 8:586–594
Margulis L (1993) Symbiosis in cell evolution. Microbial communities in the archaean and proterozoic eons. W. H. Freeman and Co., New York
McCutcheon JP, Moran NA (2007) Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc Natl Acad Sci USA 104:19392–19397
McCutcheon JP, McDonald BR, Moran NA (2009) Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial symbiont. PLoS Genet 5:e1000565
McGraw EA, O'Neill SL (2004) Wolbachia pipientis: intracellular infection and pathogenesis in Drosophila. Curr Opin Microbiol 7:67–70
Montllor CB, Maxmen A, Purcell AH (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27:189–195
Moran NA, Mira A (2001) The process of genome shrinkage in the obligate symbiont Buchnera aphidicola. Genome Biol 2:RESEARCH0054
Moran NA, Plague GR (2004) Genomic changes following host restriction in bacteria. Curr Opin Genet Dev 14:627–633
Moran NA, Telang A (1998) The evolution of bacteriocyte-associated endosymbionts in insects. Bioscience 48:295–304
Moya A, Latorre A, Sabater-Munoz B, Silva FJ (2002) Comparative molecular evolution of primary (Buchnera) and secondary symbionts of aphids based on two protein-coding genes. J Mol Evol 55:127–137
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
Moya A, Gil R, Latorre A (2009) The evolutionary history of symbiotic associations among bacteria and their animal hosts: a model. Clin Microbiol Infect 15:11–13
Munson MA, Baumann P, Moran NA (1992) Phylogenetic relationships of the endosymbionts of mealybugs (Homoptera: Pseudococcidae) based on 16S rDNA sequences. Mol Phylogenet Evol 1:26–30
Nakabachi A, Yamashita A, Toh H, Ishikawa H, Dunbar HE, Moran NA, Hattori M (2006) The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314:267
Ochman H, Moran NA (2001) Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 292:1096–1099
Oliver KM, Moran NA, Hunter MS (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci USA 102:12795–12800
Oliver KM, Degnan PH, Hunter MS, Moran NA (2009) Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325:992–994
Perez-Brocal V, Gil R, Ramos S, Lamelas A, Postigo M, Michelena JM, Silva FJ, Moya A, Latorre A (2006) A small microbial genome: the end of a long symbiotic relationship? Science 314:312–313
Plague GR, Dunbar HE, Tran PL, Moran NA (2008) Extensive proliferation of transposable elements in heritable bacterial symbionts. J Bacteriol 190:777–779
Podar M, Anderson I, Makarova KS, Elkins JG, Ivanova N, Wall MA, Lykidis A, Mavromatis K, Sun H, Hudson ME, Chen W, Deciu C, Hutchison D, Eads JR, Anderson A, Fernandes F, Szeto E, Lapidus A, Kyrpides NC, Saier MH Jr, Richardson PM, Rachel R, Huber H, Eisen JA, Koonin EV, Keller M, Stetter KO (2008) A genomic analysis of the archaeal system Ignicoccus hospitalis–Nanoarchaeum equitans. Genome Biol 9:R158
Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21:541–554
Rispe C, Delmotte F, van Ham RCHJ, Moya A (2004) Mutational and selective pressures on codon and amino acid usage in Buchnera, endosymbiotic bacteria of aphids. Genome Res 14:44–53
Russell JA, Moran NA (2006) Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc Biol Sci 273:603–610
Russell JA, Latorre A, Sabater-Munoz B, Moya A, Moran NA (2003) Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol Ecol 12:1061–1075
Sabater-Munoz B, van Ham RC, Moya A, Silva FJ, Latorre A (2004) Evolution of the leucine gene cluster in Buchnera aphidicola: insights from chromosomal versions of the cluster. J Bacteriol 186:2646–2654
Sabree ZL, Kambhampati S, Moran NA (2009) Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont. Proc Natl Acad Sci USA 106:19521–19526
Scarborough CL, Ferrari J, Godfray HC (2005) Aphid protected from pathogen by endosymbiont. Science 310:1781
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
Silva FJ, Latorre A, Moya A (2001) Genome size reduction through multiple events of gene disintegration in Buchnera APS. Trends Genet 17:615–618
Silva FJ, Latorre A, Moya A (2003) Why are the genomes of endosymbiotic bacteria so stable? Trends Genet 19:176–180
Simon JC, Carre S, Boutin M, Prunier-Leterme N, Sabater-Mun B, Latorre A, Bournoville R (2003) Host-based divergence in populations of the pea aphid: insights from nuclear markers and the prevalence of facultative symbionts. Proc Biol Sci 270:1703–1712
Tamames J, Gil R, Latorre A, Pereto J, Silva FJ, Moya A (2007) The frontier between cell and organelle: genome analysis of Candidatus Carsonella ruddii. BMC Evol Biol 7:181
Tamas I, Klasson L, Canback B, Naslund AK, Eriksson AS, Wernegreen JJ, Sandstrom JP, Moran NA, Andersson SG (2002) 50 million years of genomic stasis in endosymbiotic bacteria. Science 296:2376–2379
Thao ML, Gullan PJ, Baumann P (2002) Secondary (gamma-Proteobacteria) endosymbionts infect the primary (beta-Proteobacteria) endosymbionts of mealybugs multiple times and coevolve with their hosts. Appl Environ Microbiol 68:3190–3197
Toh H, Weiss BL, Perkin SA, Yamashita A, Oshima K, Hattori M, Aksoy S (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
Tokuda G, Lo N, Takase A, Yamada A, Hayashi Y, Watanabe H (2008) Purification and partial genome characterization of the bacterial endosymbiont Blattabacterium cuenoti from the fat bodies of cockroaches. BMC Res Notes 1:118
Touchon M, Rocha EP (2007) Causes of insertion sequences abundance in prokaryotic genomes. Mol Biol Evol 24:969–981
Tsuchida T, Koga R, Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science 303:1989
van Ham RC, Kamerbeek J, Palacios C, Rausell C, Abascal F, Bastolla U, Fernandez JM, Jimenez L, Postigo M, Silva FJ, Tamames J, Viguera E, Latorre A, Valencia A, Moran F, Moya A (2003) Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci USA 100:581–586
van Hoek AH, van Alen TA, Sprakel VS, Leunissen JA, Brigge T, Vogels GD, Hackstein JH (2000) Multiple acquisition of methanogenic archaeal symbionts by anaerobic ciliates. Mol Biol Evol 17:251–258
von Dohlen CD, Moran NA (2000) Molecular data support a rapid radiation of aphids (Aphididae) in the Cretaceous and multiple origins of host alternation. Biol J Linn Soc 71:689–717
von Dohlen CD, Kohler S, Alsop ST, McManus WR (2001) Mealybug beta-proteobacterial endosymbionts contain gamma-proteobacterial symbionts. Nature 412:433–436
Waters E, Hohn MJ, Ahel I, Graham DE, Adams MD, Barnstead M, Beeson KY, Bibbs L, Bolanos R, Keller M, Kretz K, Lin X, Mathur E, Ni J, Podar M, Richardson T, Sutton GG, Simon M, Soll D, Stetter KO, Short JM, Noordewier M (2003) The genome of Nanoarchaeum equitans: insights into early archaeal evolution and derived parasitism. Proc Natl Acad Sci USA 100:12984–12988
Wei J, Goldberg MB, Burland V, Venkatesan MM, Deng W, Fournier G, Mayhew GF, Plunkett G 3rd, Rose DJ, Darling A, Mau B, Perna NT, Payne SM, Runyen-Janecky LJ, Zhou S, Schwartz DC, Blattner FR (2003) Complete genome sequence and comparative genomics of Shigella flexneri serotype 2a strain 2457T. Infect Immun 71:2775–2786
Welburn SC, Maudlin I (1999) Tsetse-trypanosome interactions: rites of passage. Parasitol Today 15:399–403
Wernegreen JJ (2005) For better or worse: genomic consequences of intracellular mutualism and parasitism. Curr Opin Genet Dev 15:572–583
Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87:4576–4579
Woyke T, Teeling H, Ivanova NN, Huntemann M, Richter M, Gloeckner FO, Boffelli D, Anderson IJ, Barry KW, Shapiro HJ, Szeto E, Kyrpides NC, Mussmann M, Amann R, Bergin C, Ruehland C, Rubin EM, Dubilier N (2006) Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443:950–955
Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R, Brownlie JC, McGraw EA, Martin W, Esser C, Ahmadinejad N, Wiegand C, Madupu R, Beanan MJ, Brinkac LM, Daugherty SC, Durkin AS, Kolonay JF, Nelson WC, Mohamoud Y, Lee P, Berry K, Young MB, Utterback T, Weidman J, Nierman WC, Paulsen IT, Nelson KE, Tettelin H, O'Neill SL, Eisen JA (2004) Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2:E69
Wu D, Daugherty SC, Van Aken SE, Pai GH, Watkins KL, Khouri H, Tallon LJ, Zaborsky JM, Dunbar HE, Tran PL, Moran NA, Eisen JA (2006) Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol 4:e188
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Financial support was provided by grants BFU2006/06003/BMC (Ministerio de Eduación y Ciencia, Spain) and BFU2009-12895-C02-01/BMC (Ministerio de Ciencia e Innovación, Spain) to A.L., and FP7-KBBE-2007- 212894 (European VII Framework Program) to A.M.
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Gil, R., Latorre, A., Moya, A. (2010). Evolution of Prokaryote-Animal Symbiosis from a Genomics Perspective. In: Hackstein, J. (eds) (Endo)symbiotic Methanogenic Archaea. Microbiology Monographs, vol 19. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-13615-3_11
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