Sympatric Speciation in a Bacterial Endosymbiont Results in Two Genomes with the Functionality of One

Cell

Volumn 158, Issue 6, 2014, Pages 1270-1280

  Van Leuven, James T ^a   Meister, Russell C ^b   Simon, Chris ^b   McCutcheon, John P ^a,c  

^a UNIVERSITY OF MONTANA   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

^c CANADIAN INSTITUTE FOR ADVANCED RESEARCH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYANOCOBALAMIN; HISTIDINE; METHIONINE; METHIONINE SYNTHASE;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL GENOME; CELLS BY BODY ANATOMY; CHROMOSOME; CICADA; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOLOGY; ENDOSYMBIONT; FLUORESCENCE MICROSCOPY; GENE DUPLICATION; GENE LOSS; GENOME ANALYSIS; GENOMICS; GENUS; HODGKINIA CICADICOLA; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PSEUDOGENE; SPECIES DIFFERENTIATION; SPECIES DIVERSITY; SYMPATRY; TETTIGADES; WHOLE GENOME SEQUENCING; ALPHAPROTEOBACTERIA; ANIMAL; CLASSIFICATION; GENETICS; HEMIPTERA; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; SYMBIOSIS;

ALPHAPROTEOBACTERIA; ANIMALS; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; HEMIPTERA; MOLECULAR SEQUENCE DATA; PSEUDOGENES; SYMBIOSIS;

EID: 84908068003     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.07.047     Document Type: Article

References (82)

1. Andersson, S.G., Kurland, C.G., Reductive evolution of resident genomes. Trends Microbiol. 6 (1998), 263–268.
2. Atwood, K.C., Schneider, L.K., Ryan, F.J., Periodic selection in Escherichia coli. Proc. Natl. Acad. Sci. USA 37 (1951), 146–155.
3. Baumann, P., Biology bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59 (2005), 155–189.
4. Baumann, P., Baumann, L., Clark, M.A., Levels of Buchnera aphidicola chaperonin GroEL during growth of the aphid Schizaphis graminum. Curr. Microbiol. 32 (1996), 279–285.
5. Brower, A.V., Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc. Natl. Acad. Sci. USA 91 (1994), 6491–6495.
6. Burger, G., Gray, M.W., Lang, B.F., Mitochondrial genomes: anything goes. Trends Genet. 19 (2003), 709–716.
7. Carver, T., Harris, S.R., Berriman, M., Parkhill, J., McQuillan, J.A., Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics 28 (2012), 464–469.
8. Cohan, F.M., What are bacterial species?. Annu. Rev. Microbiol. 56 (2002), 457–487.
9. Conant, G.C., Wolfe, K.H., Turning a hobby into a job: how duplicated genes find new functions. Nat. Rev. Genet. 9 (2008), 938–950.
10. Darriba, D., Taboada, G.L., Doallo, R., Posada, D., ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27 (2011), 1164–1165.
11. Doolittle, W.F., Sapienza, C., Selfish genes, the phenotype paradigm and genome evolution. Nature 284 (1980), 601–603.
12. Douglas, A.E., Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 43 (1998), 17–37.
13. Ellers, J., Kiers, E.T., Currie, C.R., McDonald, B.R., Visser, B., Visser, B., Ecological interactions drive evolutionary loss of traits. Ecol. Lett. 15 (2012), 1071–1082.
14. Fares, M.A., Ruiz-González, M.X., Moya, A., Elena, S.F., Barrio, E., Endosymbiotic bacteria: groEL buffers against deleterious mutations. Nature, 417, 2002, 398.
15. Finnigan, G.C., Hanson-Smith, V., Stevens, T.H., Thornton, J.W., Evolution of increased complexity in a molecular machine. Nature 481 (2012), 360–364.
16. Friesen, M.L., Saxer, G., Travisano, M., Doebeli, M., Experimental evidence for sympatric ecological diversification due to frequency-dependent competition in Escherichia coli. Evolution 58 (2004), 245–260.
17. Gould, S.J., Lewontin, R.C., The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc. R. Soc. Lond. B Biol. Sci. 205 (1979), 581–598.
18. Gray, M.W., Doolittle, W.F., Has the endosymbiont hypothesis been proven?. Microbiol. Rev. 46 (1982), 1–42.
19. Gray, M.W., Lukes, J., Archibald, J.M., Keeling, P.J., Doolittle, W.F., Cell biology. Irremediable complexity?. Science 330 (2010), 920–921.
20. Gruwell, M.E., Hardy, N.B., Gullan, P.J., Dittmar, K., Evolutionary relationships among primary endosymbionts of the mealybug subfamily phenacoccinae (hemiptera: Coccoidea: Pseudococcidae). Appl. Environ. Microbiol. 76 (2010), 7521–7525.
21. Hughes, A.L., The evolution of functionally novel proteins after gene duplication. Proc. Biol. Sci. 256 (1994), 119–124.
22. Husnik, F., Nikoh, N., Koga, R., Ross, L., Duncan, R.P., Fujie, M., Tanaka, M., Satoh, N., Bachtrog, D., Wilson, A.C.C., et al. Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153 (2013), 1567–1578.
23. Karban, R., Prolonged development in cicadas. Taylor, F., Karban, R., (eds.) The Evolution of Insect Life Cycles, 1986, Springer-Verlag, Heidelberg, Germany, 222–235.
24. Koga, R., Bennett, G.M., Cryan, J.R., Moran, N.A., Evolutionary replacement of obligate symbionts in an ancient and diverse insect lineage. Environ. Microbiol. 15 (2013), 2073–2081.
25. Komaki, K., Ishikawa, H., Intracellular bacterial symbionts of aphids possess many genomic copies per bacterium. J. Mol. Evol. 48 (1999), 717–722.
26. Kuo, C.-H., Ochman, H., Inferring clocks when lacking rocks: the variable rates of molecular evolution in bacteria. Biol. Direct, 4, 2009, 35.
27. Lamelas, A., Gosalbes, M.J., Manzano-Marín, A., Peretó, J., Moya, A., Latorre, A., Serratia symbiotica from the aphid Cinara cedri: a missing link from facultative to obligate insect endosymbiont. PLoS Genet., 7, 2011, e1002357.
28. Lane, N., Martin, W., The energetics of genome complexity. Nature 467 (2010), 929–934.
29. Lang, B.F., Burger, G., O'Kelly, C.J., Cedergren, R., Golding, G.B., Lemieux, C., Sankoff, D., Turmel, M., Gray, M.W., An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387 (1997), 493–497.
30. López-Madrigal, S., Latorre, A., Porcar, M., Moya, A., Gil, R., Mealybugs nested endosymbiosis: going into the ‘matryoshka’ system in Planococcus citri in depth. BMC Microbiol., 13, 2013, 74.
31. Lynch, M., The frailty of adaptive hypotheses for the origins of organismal complexity. Proc. Natl. Acad. Sci. USA 104:Suppl 1 (2007), 8597–8604.
32. Lynch, M., Conery, J.S., The evolutionary fate and consequences of duplicate genes. Science 290 (2000), 1151–1155.
33. Lynch, M., Koskella, B., Schaack, S., Mutation pressure and the evolution of organelle genomic architecture. Science 311 (2006), 1727–1730.
34. Macdonald, S.J., Lin, G.G., Russell, C.W., Thomas, G.H., Douglas, A.E., The central role of the host cell in symbiotic nitrogen metabolism. Proc. Biol. Sci. 279 (2012), 2965–2973.
35. Margulis, L., Symbiosis in cell evolution. 1981, WH Freeman, San Francisco.
36. McCutcheon, J.P., Moran, N.A., Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc. Natl. Acad. Sci. USA 104 (2007), 19392–19397.
37. McCutcheon, J.P., Moran, N.A., Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution. Genome Biol. Evol. 2 (2010), 708–718.
38. McCutcheon, J.P., Moran, N.A., Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10 (2012), 13–26.
39. McCutcheon, J.P., von Dohlen, C.D., An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr. Biol. 21 (2011), 1366–1372.
40. McCutcheon, J.P., McDonald, B.R., Moran, N.A., Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial symbiont. PLoS Genet., 5, 2009, e1000565.
41. McCutcheon, J.P., McDonald, B.R., Moran, N.A., Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc. Natl. Acad. Sci. USA 106 (2009), 15394–15399.
42. Moran, N.A., Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc. Natl. Acad. Sci. USA 93 (1996), 2873–2878.
43. Moran, N.A., Symbiosis as an adaptive process and source of phenotypic complexity. Proc. Natl. Acad. Sci. USA 104:Suppl 1 (2007), 8627–8633.
44. Moran, N.A., Plague, G.R., Sandström, J.P., Wilcox, J.L., A genomic perspective on nutrient provisioning by bacterial symbionts of insects. Proc. Natl. Acad. Sci. USA 100:Suppl 2 (2003), 14543–14548.
45. Moran, N.A., Tran, P., Gerardo, N.M., Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl. Environ. Microbiol. 71 (2005), 8802–8810.
46. Namiki, T., Hachiya, T., Tanaka, H., Sakakibara, Y., MetaVelvet: an extension of Velvet assembler to de novo metagenome assembly from short sequence reads. Nucleic Acids Res., 40, 2012, e155.
47. Ohno, S., Evolution by gene duplication. 1970, Springer-Verlag, Heidelberg, Germany.
48. Otto, S.P., The evolutionary consequences of polyploidy. Cell 131 (2007), 452–462.
49. Papadopoulou, A., Anastasiou, I., Vogler, A.P., Revisiting the insect mitochondrial molecular clock: the mid-Aegean trench calibration. Mol. Biol. Evol. 27 (2010), 1659–1672.
50. Pettersson, M.E., Berg, O.G., Muller's ratchet in symbiont populations. Genetica 130 (2007), 199–211.
51. Plucain, J., Hindré, T., Le Gac, M., Tenaillon, O., Cruveiller, S., Médigue, C., Leiby, N., Harcombe, W.R., Marx, C.J., Lenski, R.E., Schneider, D., Epistasis and allele specificity in the emergence of a stable polymorphism in Escherichia coli. Science 343 (2014), 1366–1369.
52. Ranwez, V., Harispe, S., Delsuc, F., Douzery, E.J.P., MACSE: Multiple Alignment of Coding SEquences accounting for frameshifts and stop codons. PLoS ONE, 6, 2011, e22594.
53. Rice, D.W., Alverson, A.J., Richardson, A.O., Young, G.J., Sanchez-Puerta, M.V., Munzinger, J., Barry, K., Boore, J.L., Zhang, Y., dePamphilis, C.W., et al. Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm Amborella. Science 342 (2013), 1468–1473.
54. Rispe, C., Moran, N.A., Accumulation of Deleterious Mutations in Endosymbionts: Muller's Ratchet with Two Levels of Selection. Am. Nat. 156 (2000), 425–441.
55. Rosenzweig, R.F., Sharp, R.R., Treves, D.S., Adams, J., Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli. Genetics 137 (1994), 903–917.
56. Sachs, J.L., Skophammer, R.G., Regus, J.U., Evolutionary transitions in bacterial symbiosis. Proc. Natl. Acad. Sci. USA 108:Suppl 2 (2011), 10800–10807.
57. Sarkar, S., Hopper, A.K., tRNA nuclear export in saccharomyces cerevisiae: in situ hybridization analysis. Mol. Biol. Cell 9 (1998), 3041–3055.
58. Shigenobu, S., Watanabe, H., Hattori, M., Sakaki, Y., Ishikawa, H., Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407 (2000), 81–86.
59. Sloan, D.B., Moran, N.A., Genome reduction and co-evolution between the primary and secondary bacterial symbionts of psyllids. Mol. Biol. Evol. 29 (2012), 3781–3792.
60. Sloan, D.B., Moran, N.A., The evolution of genomic instability in the obligate endosymbionts of whiteflies. Genome Biol. Evol. 5 (2013), 783–793.
61. Sloan, D.B., Alverson, A.J., Chuckalovcak, J.P., Wu, M., McCauley, D.E., Palmer, J.D., Taylor, D.R., Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol., 10, 2012, e1001241.
62. Sloan, D.B., Nakabachi, A., Richards, S., Qu, J., Murali, S.C., Gibbs, R.A., Moran, N.A., Parallel histories of horizontal gene transfer facilitated extreme reduction of endosymbiont genomes in sap-feeding insects. Mol. Biol. Evol. 31 (2014), 857–871.
63. Smith, D.R., Hamaji, T., Olson, B.J.S.C., Durand, P.M., Ferris, P., Michod, R.E., Featherston, J., Nozaki, H., Keeling, P.J., Organelle genome complexity scales positively with organism size in volvocine green algae. Mol. Biol. Evol. 30 (2013), 793–797.
64. Stoltzfus, A., On the possibility of constructive neutral evolution. J. Mol. Evol. 49 (1999), 169–181.
65. Szathmáry, E., Smith, J.M., The major evolutionary transitions. Nature 374 (1995), 227–232.
66. Thao, M.L., Gullan, P.J., Baumann, P., Secondary (gamma-Proteobacteria) endosymbionts infect the primary (beta-Proteobacteria) endosymbionts of mealybugs multiple times and coevolve with their hosts. Appl. Environ. Microbiol. 68 (2002), 3190–3197.
67. Torres, Belindo A. 1958. Revision Del Genero Tettigades Amy. Y Serv. (Homoptera-Cicadidae). Revista del Museo de La Plata. Seccion Zoologia. VII (53): 51–106, plus 24 plates.
68. Treves, D.S., Manning, S., Adams, J., Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. Mol. Biol. Evol. 15 (1998), 789–797.
69. von Dohlen, C.D., Kohler, S., Alsop, S.T., McManus, W.R., Mealybug beta-proteobacterial endosymbionts contain gamma-proteobacterial symbionts. Nature 412 (2001), 433–436.
70. Whelan, S., Goldman, N., A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18 (2001), 691–699.
71. Wilson, A.C.C., Ashton, P.D., Calevro, F., Charles, H., Colella, S., Febvay, G., Jander, G., Kushlan, P.F., Macdonald, S.J., Schwartz, J.F., et al. Genomic insight into the amino acid relations of the pea aphid, Acyrthosiphon pisum, with its symbiotic bacterium Buchnera aphidicola. Insect Mol. Biol. 19:Suppl 2 (2010), 249–258.
72. Wolfe, K.H., Yesterday's polyploids and the mystery of diploidization. Nat. Rev. Genet. 2 (2001), 333–341.
73. Woyke, T., Tighe, D., Mavromatis, K., Clum, A., Copeland, A., Schackwitz, W., Lapidus, A., Wu, D., McCutcheon, J.P., McDonald, B.R., et al. One bacterial cell, one complete genome. PLoS ONE, 5, 2010, e10314.
74. Wu, D., Daugherty, S.C., Van Aken, S.E., Pai, G.H., Watkins, K.L., Khouri, H., Tallon, L.J., Zaborsky, J.M., Dunbar, H.E., Tran, P.L., et al. Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol., 4, 2006, e188.
75. Yang, Z., PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24 (2007), 1586–1591.
76. Yang, Z., Nielsen, R., Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol. Biol. Evol. 19 (2002), 908–917.
77. Zientz, E., Dandekar, T., Gross, R., Metabolic interdependence of obligate intracellular bacteria and their insect hosts. Microbiol. Mol. Biol. Rev. 68 (2004), 745–770.
78. Bolte, S., Cordelières, F.P., A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224 (2006), 213–232.
79. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., 1000 Genome Project Data Processing Subgroup. The Sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25 (2009), 2078–2079.
80. Pernthaler, J., Glockner, F.O., Schonhuber, W., Amann, R., Fluorescence in situ hybridization (FISH) with rRNA-targeted oligonucleotide probes. Method. Microbiol. 30 (2001), 207–226.
81. Rice, P., Longden, I., Bleasby, A., EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16 (2000), 276–277.
82. Schneider, C.A., Rasband, W.S., Eliceiri, K.W., NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9 (2012), 671–675.