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Macro- and microevolution of bacteria in symbiotic systems

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Abstract

Using the examples of diverse interactions among prokaryotes and eukaryotes, the relationships between molecular and population mechanisms of evolution of symbiotic bacteria are addressed. Their circulation in host-environment systems activates microevolutionary factors that direct combinative or reductive genome evolution in facultative, ecologically obligatory, and genetically obligatory symbioses. It is shown on the example of symbiosis of rhizobia with legumes, that due to intensive systemic intra-genome rearrangements and horizontal gene transfer, two types of gene systems evolve in these bacteria: (1) controlling the pathogenesis-like processes of host recognition and penetration and (2) responsible for mutualistic interactions that are related to nitrogen fixation and its transfer to the host. The evolution of gene systems of type 1 is directed by individual (Darwinian, frequency-dependent) selection, which is responsible for gene-for-gene interactions between the partners. In the evolution of the type 2 systems, group (interdeme, kin) selection plays the key role, being responsible for the development of bacterial traits beneficial for the host. It is shown that evolution of mutualism can be described in terms of biological altruism, whose regularities are common for intraspecific and interspecific relationships. Macroevolutionary rearrangements of bacterial genomes result from the structural changes in their populations, wherein various selection modes are combined with stochastic processes (genetic drift, population waves) induced in the symbiotic systems.

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References

  1. Symbiosis: Mechanisms and Model Systems, Seckbach, J., Ed., Dordrecht: Kluwer, 2002.

    Google Scholar 

  2. Karatygin, I.V., Coevolution of Fungi and Plants, Tr. Botanicheskogo Inst. Ross. Acad. Nauk, 1993, no. 9, pp. 1–118.

  3. Douglas, A.E., Symbiotic Interactions, Oxford: Oxford Univ. Press, 1994.

    Google Scholar 

  4. Lederberg, J. and McCray, A.T., “Ome Sweet” Omics—a Genealogical Treasury of Words, Scientist, 2001, vol. 15, p. 8.

    Google Scholar 

  5. De Bary, A., Die Erscheinung der Symbiose, Strassburg: von Karl J. Trubner, 1879.

    Google Scholar 

  6. Lewis, D.H., Symbiosis and Mutualism: Crisp Concepts and Soggy Semantics, The Biology of Mutualism: Ecology and Evolution, Boucher, D.H., Ed., London: Croom Helm, 1985, pp. 29–39.

    Google Scholar 

  7. Quispel, A., Some Theoretical Aspects of Symbiosis, Antonie van Leeuwenhoek, 1951, vol. 17, pp. 69–80.

    Article  PubMed  CAS  Google Scholar 

  8. Tikhonovich, I.A. and Provorov, N.A., Symbiogenetics of Microbe-Plant Interactions, Ekol. Genet., 2003, vol. 1, no. 0, pp. 36–46.

    Google Scholar 

  9. Tikhonovich, I.A., Lugtenberg, B.J.J., and Provorov, N.A., Molecular Microbe-Plant Interactions: New Bridges between Past and Future (Editorial Remarks), Biology of Plant-Microbe Interactions, Tikhonovich, I.A., Lugtenberg, B.J.J., and Provorov, N.A., Eds., St. Petersburg: Biont, 2004, vol. 4, pp. 17–18.

    Google Scholar 

  10. Herre, E.A., Knowlton, N., Mueller, U.G., and Rehner, S.A., The Evolution of Mutualisms: Exploring the Paths between Conflict and Cooperation, Trends Ecol. Evol., 1999, vol. 14, no. 2, pp. 49–53.

    Article  PubMed  Google Scholar 

  11. Provorov, N.A., Molecular Basis of Symbiogenic Evolution: From Free-Living Bacteria to Organelles, Zh. Obshch. Biol., 2005, vol. 66, no. 5, pp. 371–388.

    PubMed  CAS  Google Scholar 

  12. Young, J.P.W. and Haukka, K.E., Diversity and Phylogeny of Rhizobia, New Phytol., 1996, vol. 133, pp. 87–94.

    Article  Google Scholar 

  13. Hibbett, D.S., Gilbert, L.B., and Donoghue, M.J., Evolutionary Instability of Ectomycorrhizal Symbioses in Basidiomycetes, Nature, 2000, vol. 407, pp. 506–508.

    Article  PubMed  CAS  Google Scholar 

  14. Schüßler, A., Molecular Phylogeny, Taxonomy and Evolution of Geosiphon pyriformis and Arbuscular Mycorrhizal Fungi, Plant Soil, 2002, vol. 244, pp. 75–83.

    Article  Google Scholar 

  15. Tikhonovich, I.A. and Provorov, N.A., Genetika simbioticheskoi azotfiksatsii s osnovami selektsii (Genetics of Symbiotic Nitrogen Fixation with Fundamentals of Breeding), St. Petersburg: Nauka, 1998.

    Google Scholar 

  16. Freiberg, C., Fellay, R., Bairoch, A., et al., Molecular Basis of Symbiosis between Rhizobium and Legumes, Nature, 1997, vol. 387, no. 22, pp. 394–401.

    Article  PubMed  CAS  Google Scholar 

  17. Charles, T.C. and Finan, T.M., Analysis of a 1600-kilobase Rhizobium meliloti Megaplasmid Using Defined Deletions Generated in Vivo, Genetics, 1991, vol. 127, no. 1, pp. 5–20.

    PubMed  CAS  Google Scholar 

  18. Kahn, M.L., Schroeder, B.K., House, B.L., et al., Foraging for Meaning-Pstgenome Approaches to Sinorhizobium meliloti, Biology of Plant-Microbe Interactions, Tikhonovich, I.A., Lugtenberg, B.J.J., and Provorov, N.A., Eds., St. Petersburg: Biont, 2004, vol. 4, pp. 416–422.

    Google Scholar 

  19. Farrand, S.K., Kon″yugativnye plazmidy i ikh perenos (Conjugative Plasmids and Their Transfer), Rhizobiaceae: Molekulyarnaya biologiya bakterii, vzaimodeistvuyushchikh s rasteniyami (The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria), Spaink, H.P., Kondorosi, A., and Hooykaas, P. J.J., Eds., St. Petersburg: Biont, 2002, pp. 225–258.

    Google Scholar 

  20. Ogata, H., Audic, S., Renesto-Audiffren, P., et al., Mechanisms of Evolution in Rickettsia conori and R. prowazekii, Science, 2001, vol. 293, pp. 2093–2098.

    Article  PubMed  CAS  Google Scholar 

  21. Ishikawa, H., Genome of Buchera sp. Aps, an Intracellular Symbiotic Bacterium of Pea Aphid, (Acyrtosiphon pisum), Symbiosis: Mechanisms and Model Systems, Seckbach, J., Ed., Dordrecht: Kluwer, 2002, pp. 665–674.

    Google Scholar 

  22. Moran, N.A., Genome Evolution in Symbiotic Bacteria, ASM News, 2002, vol. 68, no. 10, pp. 499–505.

    Google Scholar 

  23. Lang, B.F., Gray, M.W., and Burger, G., Mitochondrial Genome Evolution and the Origin of Eukaryotes, Ann. Rev. Genet., 1999, vol. 33, pp. 351–397.

    Article  PubMed  CAS  Google Scholar 

  24. Leon, P., Arroyo, A., and Mackenzie, S., Nuclear Control of Plastid and Mitochondrial Development in Higher Plants, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1998, vol. 49, pp. 453–480.

    Article  PubMed  CAS  Google Scholar 

  25. Young, J.P.W., Crossman, L.C., Johnston, A.W.B., et al., The Genome of Rhizobium leguminosarum Has Recognizable Core and Accessory Components, Genome Biol., 2006, vol. 7, p. R34.

    Article  PubMed  CAS  Google Scholar 

  26. Dougan, G., Haque, A., and Pickard, D., The Escherichia coli Gene Pool, Curr. Opin. Microbiol., 2001, vol. 4, pp. 90–94.

    Article  PubMed  CAS  Google Scholar 

  27. Downie, J.A. and Young, J.P.W., The ABC of Symbiosis, Nature, 2001, vol. 142, pp. 597–598.

    Article  Google Scholar 

  28. Charles, H. and Ishikawa, H., Physical and Genetic Map of the Genome of Buchnera, the Primary Endosymbiont of the Pea Aphid Acyrtosiphon pisum, J. Mol. Evol., 1999, vol. 48, pp. 142–150.

    Article  PubMed  CAS  Google Scholar 

  29. Kozo-Polyanskii, B.M., Novyi printsip biologii: teorii simbiogeneza (Novel Principle in Biology: Essay of Theory of Symbiogenesis), Moscow: Puchina, 1924.

    Google Scholar 

  30. Lugtenberg, B.J.J., Dekkers, L., and Bloemberg, G., Molecular Determinants of Rhizosphere Colonization by Pseudomonas, Annu. Rev. Phytopathol., 2001, vol. 39, pp. 461–490.

    Article  PubMed  CAS  Google Scholar 

  31. Ovtsyna, A.O. and Tikhonovich, I.A., Structure, Functions and Possible Practical Use of Signaling Molecules Inducing the Development of Pea-Rhizobia Symbiosis, Ekol. Genet., 2004, vol. 2, no. 3, pp. 14–24.

    Google Scholar 

  32. Kaminski, P., Batut, Zh., and Boistard, P., Symbiotic Control of Nitrogen Fixation by Rhizobia, Rhizobiaceae: Molekulyarnaya biologiya bakterii, vzaimodeistvuyushchikh s rasteniyami (The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria), Spaink, H.P., Kondorosi, A., and Hooykaas, P.J.J., Eds., St. Petersburg: Biont, 2002, pp. 465–492.

    Google Scholar 

  33. Spaink, H.P., The Molecular Basis of Infection and Nodulation by Rhizobia: The Ins and Outs of Sympathogenesis, Annu. Rev. Phytopathol., 1995, vol. 33, pp. 345–368.

    Article  PubMed  CAS  Google Scholar 

  34. Santos, R., Herouart, D., Sigaud, S., et al., Oxidative Burst in Alfalfa Sinorhizobium meliloti Symbiotic Interaction, Mol. Plant-Microbe Interact., 2001, vol. 14, no. 3, pp. 86–89.

    Article  PubMed  CAS  Google Scholar 

  35. Gamas, P., de Billy, F., and Truchet, G., Symbiosis-Specific Expression of Two Medicago truncatula Nodulin Genes, MtM1 and MtN13 Encoding Products Homologous to Plant Defense Proteins, Mol. Plant-Microbe Interact., 1998, vol. 11, no. 5, pp. 393–403.

    Article  PubMed  CAS  Google Scholar 

  36. Brewin, N.J., Novel Symbiotic Organelles in the Rhizobium-Legume Interaction, Biology of Plant-Microbe Interactions, Tikhonovich, I.A., Lugtenberg, B.J.J., and Provorov, N.A., Eds., St. Petersburg: Biont, 2004, vol. 4, pp. 476–482.

    Google Scholar 

  37. Ovtsyna, A.O. and Staehelin, C., Bacterial Signals Required for the Rhizobium-Legume Symbiosis, Recent Res. Develop. Microbiol., 2005, vol. 7, pp. 631–648.

    Google Scholar 

  38. Breedveld, M.J. and Miller, K.J., Cyclic β-Glucans of Members of the Family Rhizobiaceae, Microbiol. Rev., 1994, vol. 58, pp. 145–161.

    PubMed  CAS  Google Scholar 

  39. Bridveld, M. and Miller, K.J., Cell Surface β-Glucans, Rhizobiaceae: Molekulyarnaya biologiya bakterii, vzaimodeistvuyushchikh s rasteniyami (The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria), Spaink, H.P., Kondorosi, A., and Hooykaas, P.J.J., Eds., St. Petersburg: Biont, 2002, pp. 101–118.

    Google Scholar 

  40. Deakin, W.J., Bartsev, A.V., Boukli, N.M., et al., Symbiotic Type III Protein System, Biology of Plant-Microbe Interactions, vol. 4, Tikhonovich, I.A., Lugtenberg, B.J.J., and Provorov, N.A., Eds., St. Petersburg: Biont, 2004, vol. 4, pp. 542–544.

    Google Scholar 

  41. Stacey, G., Bradyrhizobium japonicum Nodulation Genetics, FEMS Microbiol. Lett., 1995, vol. 127, pp. 1–9.

    Article  PubMed  CAS  Google Scholar 

  42. Niehaus, K., Albus, U., Baier, R., et al., Symbiotic Suppression of the Medicago sativa Plant Defence System by Rhizobium meliloti Oligosaccharides, Biological Nitrogen Fixation for 21-th Century, Elmerich, C., Kondorosi, A., and Newton, W., Eds., Dordrecht: Kluwer, 1998, pp. 225–226.

    Google Scholar 

  43. Kannenberg, E., Reus, B., Forsberg, S., and Karlson, R., Lipopolysaccharides and K-Antigenes: Structure, Biosynthesis and Functions, Rhizobiaceae: Molekulyarnaya biologiya bakterii, vzaimodeistvuyushchikh s rasteniyami (The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria), Spaink, H.P., Kondorosi, A., and Hooykaas, P.J.J., Eds., St. Petersburg: Biont, 2002, pp. 143–178.

    Google Scholar 

  44. Kapp, D., Niehaus, K., Quandt, J., et al., Cooperative Action of Rhizobium meliloti Nodulation and Infection Mutants during the Process of Forming Mixed Infected Alfalfa Nodules, Plant Cell, 1990, vol. 2, pp. 139–151.

    Article  PubMed  Google Scholar 

  45. Provorov, N.A. and Dolgikh, E.A., Organisms’ Metabolic Integration in Symbiotic Systems, Zh. Obshch. Biol., 2006, vol. 67, no. 6, pp. 403–422.

    PubMed  CAS  Google Scholar 

  46. Lutova, L.A., Provorov, N.A., Tikhodeev, O.N., et al., Genetika razvitiya rastenii (The Genetics of Plant Development), Inge-Vechtomov, S.G., Ed., St. Petersburg: Nauka, 2000.

    Google Scholar 

  47. Tikhonovich, I.A., Borisov, A.Yu., Tsyganov, V.E., et al., Symbiotic Integration of Plant and Microorganisms Genetic Systems, Usp. Sovrem. Biol., 2005, vol. 125, no. 3, pp. 227–238.

    CAS  Google Scholar 

  48. Dobert, R.C., Breil, B.T., and Triplett, E.W., DNA Sequence of the Common Nodulation Genes of Bradyrhizobium elkanii and Their Phylogenetic Relationship to Those of Other Nodulating Bacteria, Mol. Plant-Microbe Interact., 1994, vol. 7, pp. 564–572.

    PubMed  CAS  Google Scholar 

  49. Tikhonovich, I.A., Kozhemyakov, A.P., Ovtsyna, A.O., and Provorov, N.A., Construction of Highly Effective Symbiotic Systems, New Approaches and Techniques in Breeding Sustainable Fodder Crops and Amenity Grasses, Provorov, N.A., Tikhonovich, I.A., and Veronesi, F., Eds., St. Petersburg: Biont, 2002, pp. 131–135.

    Google Scholar 

  50. Guttman, D.S. and Sarkar, S.F., Evolutionary and Functional Genomics of Host Specificity in Pseudomonas syringae, Biology of Plant-Microbe Interactions, Lugtenberg, B.J.J., and Provorov, N.A., Eds., St. Petersburg: Biont, 2004, vol. 4, pp. 132–137.

    Google Scholar 

  51. Vanderplank, J.E., Host-Pathogen Interaction in Plant Disease, New York: Academic, 1982.

    Google Scholar 

  52. Stracke, S., Kistner, C., Yoshida, S., et al., A Plant Receptor-Like Kinase Required for Both Bacterial and Fungal Symbiosis, Nature, 2002, vol. 417, pp. 959–962.

    Article  PubMed  CAS  Google Scholar 

  53. Endre, G., Kereszt, A., Kevei, Z., et al., A Receptor Kinase Regulating Symbiotic Nodule Development, Nature, 2002, vol. 417, pp. 962–966.

    Article  PubMed  CAS  Google Scholar 

  54. Searle, I.R., Men, A.M., Laniya, T.S., et al., Long-Distance Signaling for Nodulation Control in Legumes Requires a CLAVATA1-Like Receptor Kinase, Science, 2002, vol. 299, pp. 109–112.

    Article  PubMed  CAS  Google Scholar 

  55. Radutoiu, S., Madsen, L.H., Madsen, E.B., et al., Plant Recognition of Symbiotic Bacteria Requires Two LysM Receptor-Like Kinases, Nature, 2003, vol. 425, pp. 585–592.

    Article  PubMed  CAS  Google Scholar 

  56. Madsen, E.B., Madsen, L.H., Radutoiu, S., et al., A Receptor Kinase Gene of the LysM Type Is Involved in Legume Perception of Rhizobial Signals, Nature, 2003, vol. 425, pp. 637–640.

    Article  PubMed  CAS  Google Scholar 

  57. Wilson, K.J., Anjaiah, V., Nambiar, P.T., and Ausubel, F.M., Isolation and Characterization of Symbiotic Mutants of Bradyrhizobium sp. (Arachis) Strain NC92: Mutants with Host-Specific Defects in Nodulation and Nitrogen Fixation, J. Bacteriol., 1987, vol. 169, no. 5, pp. 2177–2186.

    PubMed  CAS  Google Scholar 

  58. Chun, J.Y., Sexton, G.L., Roth, L.E., and Stacey, G., Identification and Characterization of a Novel Bradyrhizobium japonicum Gene Involved in Host-Specific Nitrogen Fixation, J. Bacteriol., 1994, vol. 176, no. 21, pp. 6717–6729.

    PubMed  CAS  Google Scholar 

  59. Oh, H.S., Son, O., Chun, J.Y., et al., The Bradyrhizobium japonicum HsfA Gene Exhibits a Unique Developmental Expression Pattern in Cowpea Nodules, Mol. Plant-Microbe Interact., 2001, vol. 14, no. 11, pp. 1286–1292.

    Article  PubMed  CAS  Google Scholar 

  60. Dorosinskii, L.M., The Ecology of Nodule Bacteria, Usp. Mikrobiol., 1975, no. 10, pp. 201–213.

  61. Provorov, N.A., Genetic and Evolutionary Basis of Symbiosis Doctrine, Zh. Obshch. Biol., 2001, vol. 62, no. 6, pp. 472–495.

    PubMed  CAS  Google Scholar 

  62. Provorov, N.A., Borisov, A.Yu., and Tikhonovich, I.A., Comparative Genetics and Evolutionary Morphology of Symbioses Formed by Plants with Nitrogen-Fixing Microbes and Endomycorrhizal Fungi, Zh. Obshch. Biol., 2002, vol. 63, no. 6, pp. 451–472.

    PubMed  CAS  Google Scholar 

  63. Provorov, N.A. and Vorob’ev, N.I., Evolutionary Genetics of Nodule Bacteria: Molecular and Population Aspects, Russ. J. Genet., 2000, vol. 36, no. 12, pp. 1323–1335.

    Article  CAS  Google Scholar 

  64. Pimentel, D., Population Regulation and Genetic Feedback, Science, 1968, vol. 159, pp. 1432–1437.

    Article  PubMed  CAS  Google Scholar 

  65. Frank, S.A., Models of Plant-Pathogen Co-Evolution, Trends Genet., 1992, vol. 8, pp. 213–219.

    PubMed  CAS  Google Scholar 

  66. Ochman, H. and Bergthorsson, U., Rates and Patterns of Chromosome Evolution in Enteric Bacteria, Curr. Opin. Microbiol., 1998, vol. 1, pp. 580–583.

    Article  PubMed  CAS  Google Scholar 

  67. Thompson, J.N. and Burdon, J., Gene-For-Gene Co-Evolution between Plants and Parasites, Nature, 1992, vol. 360, pp. 121–125.

    Article  Google Scholar 

  68. Vorob’ev, N.I. and Provorov, N.A., The Interplay of Darwinian and Frequency Dependent Selection during the Formation of Bacterial Population in ‘Host-Environment’ System, Ekol. Genet., 2005, vol. 3, no. 3, pp. 3–11.

    Google Scholar 

  69. Provorov, N.A. and Vorobyov, N.I., Interplay of Darwinian and Frequency-Dependent Selection in the Host-Associated Microbial Populations, Theor. Population Biol., 2006, vol. 70, no. 3, pp. 262–272.

    Article  Google Scholar 

  70. Maynard Smith, J., Feil, E.J., and Smith, N.H., Population Structure and Evolutionary Dynamics of Pathogenic Bacteria, BioEssays, 2000, vol. 22, pp. 1115–1122.

    Article  Google Scholar 

  71. Schlimme, W., Marchiani, M., Hanselmann, K., and Jenni, B., Gene Transfer between Bacteria within Digestive Vacuoles of Protozoa, FEMS Microb. Ecol., 1997, vol. 23, pp. 239–247.

    Article  CAS  Google Scholar 

  72. Van Elsas, J.D., Trevors, J.T., and Starodub, E.E., Bacterial Conjugation between Pseudomonads in the Rhizosphere of Wheat, FEMS Microb. Ecol., 1998, vol. 53, pp. 299–306.

    Article  Google Scholar 

  73. Laguerre, G., Mavingui, P., Allard, M.R., et al., Typing of Rhizobia by PCR DNA Fingerprinting and PCR-Restriction Lengths Polymorphism Analysis of Chromosomal and Symbiotic Gene Regions: Application to Rhizobium leguminosarum and Its Different Biovars, Appl. Environ. Microbiol., 1996, vol. 62, pp. 2029–2036.

    PubMed  CAS  Google Scholar 

  74. Provorov, N.A., Fokina, I.G., Rumyantseva, M.L., and Simarov, B.V., Sym-Plasmids’ Transfer into Symbiotic Active and Asymbiotic Rizobial Strains: Characteristics of Recombinants and Putative Evolutionary Consequences, Ekol. Genet., 2004, vol. 2, no. 2, pp. 29–34.

    Google Scholar 

  75. Darwin, C., The Origin of Species by Means of Natural Selection, London: John Murray, 1872.

    Google Scholar 

  76. Maynard Smith, J., Generating Novelty by Symbiosis, Nature, 1989, vol. 341, no. 6240, pp. 284–285.

    Article  Google Scholar 

  77. Haldane, J.B.S., The Causes of Evolution, New York: Harper and Raw, 1935.

    Google Scholar 

  78. Hamilton, W.D., The Genetical Evolution of Social Behavior, J. Theor. Biol., 1964, vol. 7, pp. 1–16.

    Article  PubMed  CAS  Google Scholar 

  79. Maynard Smith, J., Group Selection and Kin Selection, Nature, 1964, vol. 201, pp. 1145–1147.

    Article  Google Scholar 

  80. Frank, S.A., Genetics of Mutualism: The Evolution of Altruism between Species, J. Theor. Biol., 1994, vol. 170, pp. 393–400.

    Article  PubMed  CAS  Google Scholar 

  81. Denison, R.F., Legume Sanctions and the Evolution of Symbiotic Cooperation by Rhizobia, Am. Naturalist, 2000, vol. 156, no. 6, pp. 567–576.

    Article  Google Scholar 

  82. Provorov, N.A., Population Genetics of Nodule Bacteria, Zh. Obshch. Biol., 2000, vol. 61, no. 3, pp. 229–257.

    PubMed  CAS  Google Scholar 

  83. Maynard Smith, J., The Evolution of Behaviour, in Evolyutsiya (Evolution), Moscow: Mir, 1981, pp. 195–218.

    Google Scholar 

  84. Jimenez, J. and Casadesus, J., An Altruistic Model of Rhizobium-Legume Association, J. Heredity, 1989, vol. 80, pp. 335–337.

    Google Scholar 

  85. Olivieri, I. and Frank, S.A., The Evolution of Nodulation in Rhizobium: Altruism in the Rhizosphere, J. Heredity, 1994, vol. 85, pp. 46–47.

    Google Scholar 

  86. Yakovlev, G.P., Bobovye zemnogo shara (Legumes of the Earth), Leningrad: Nauka, 1991.

    Google Scholar 

  87. Kozhemyakov, A.P. and Tikhonovich, I.A., Use of Legume Inoculants and Biopreparations of Complex Effect in Agriculture, Dokl. Ross. Akad. S-kh. Nauk, 1998, no. 6, pp. 7–10.

  88. Frank, S.A., Models of Symbiosis, Am. Naturalist, 1997, vol. 150, pp. 80–99.

    Article  Google Scholar 

  89. Shapiro, J.A., Thinking about Bacteria as Multicellular Organisms, Annu. Rev. Microbiol., 1998, vol. 52, pp. 81–104.

    Article  PubMed  CAS  Google Scholar 

  90. Douglas, A.E., Mycetocyte Symbiosis in Insects, Biol. Rev., 1989, vol. 64, pp. 409–434.

    Article  PubMed  CAS  Google Scholar 

  91. Darlington, P.J., Altruism: Its Characteristics and Evolution, Proc. Natl. Acad. Sci. USA, 1978, vol. 75, no. 1, pp. 385–389.

    Article  PubMed  Google Scholar 

  92. Moran, N.A., Accelerated Evolution and Muller’s Ratchet in Endosymbiotic Bacteria, Proc. Natl. Acad. Sci. USA, 1996, vol. 93, pp. 2873–2878.

    Article  PubMed  CAS  Google Scholar 

  93. Levin, B.R. and Bergstrom, C.T., Bacteria Are Different: Observations, Interpretations, Speculations and Opinions about the Mechanisms of Adaptive Evolution in Prokaryotes, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 6981–6985.

    Article  PubMed  CAS  Google Scholar 

  94. Ochman, H., Lawrence, J.G., and Groisman, E.A., Lateral Gene Transfer and the Nature of Bacterial Innovation, Nature, 2000, vol. 405, pp. 299–304.

    Article  PubMed  CAS  Google Scholar 

  95. Korochkin, L.I., Biologiya individual’nogo razvitiya (Biology of Ontogenesis), Moscow: Mosk. Gos. Univ., 2002.

    Google Scholar 

  96. Nazarov, V.I., Evolyutsiya ne po Darvinu (Non-Darwinian Evolution), Moscow: KomKniga, 2005.

    Google Scholar 

  97. Person, C., Samborski, D.J., and Rohringer, R., The Gene-For-Gene Concept, Nature, 1962, vol. 194, pp. 561–562.

    Article  PubMed  CAS  Google Scholar 

  98. Wilson, D.S., Structured Demes and the Evolution of Group-Advantageous Traits, The Amer. Naturalist, 1977, vol. 111, no. 977, pp. 157–185.

    Article  Google Scholar 

  99. Wade, M.J., Kin Selection: Its Components, Science, 1980, vol. 210, pp. 665–667.

    Article  PubMed  Google Scholar 

  100. Michod, R.E. and Abugov, R., Adaptive Topography in Family-Structured Models of Kin Selection, Science, 1980, vol. 210, pp. 667–669.

    Article  PubMed  Google Scholar 

  101. Goodnight, C.J., The Influence of Environmental Variation on Group and Individual Selection in a Cress, Evolution, 1985, vol. 39, no. 3, pp. 545–558.

    Article  Google Scholar 

  102. Wade, M.J., An Experimental Study of Group Selection, Evolution, 1977, vol. 31, pp. 134–153.

    Article  Google Scholar 

  103. Wade, M.J., Soft Selection, Hard Selection, Kin Selection and Group Selection, Am. Naturalist, 1985, vol. 125, pp. 61–73.

    Article  Google Scholar 

  104. Hamilton, W.D., Selfish and Spiteful Behavior in an Evolutionary Model, Nature, 1970, vol. 288, no. 5277, pp. 1218–1220.

    Article  Google Scholar 

  105. Wilson, D.S., Evolution on the Level of Communities, Science, 1976, vol. 192, pp. 1358–1360.

    Article  PubMed  CAS  Google Scholar 

  106. Yang, Z., Adaptive Molecular Evolution, Handbook of Statistical Genetics, Balding, D.J., et al., Eds., New York: Wiley, 2001, pp. 327–350.

    Google Scholar 

  107. Vorontsov, N.N., Razvitie evolyutsionnykh uchenii v biologii (Development of Evolutionary Doctrine in Biology), Moscow: Progress-Traditsiya, 1999.

    Google Scholar 

  108. Popov, I.Yu., Ortogenez protiv darvinizma (Ortogenesis against Darwinism), St. Petersburg: S.-Peterb. Gos. Univ., 2005.

    Google Scholar 

  109. Tikhodeev, O.N., Molecular Mechanisms of Macroevolution, Zh. Obshch. Biol., 2005, vol. 66, no. 1, pp. 13–27.

    PubMed  CAS  Google Scholar 

  110. Ruse, M., Limits of our Knowledge of Evolution, Evolutionary Biology, Clegg, M.T., Hecht, M.K., and Macinryre, R.J., Eds., New York: Kluwer, 2000, vol. 32, pp. 3–33.

    Google Scholar 

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Correspondence to N. A. Provorov.

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Original Russian Text © N.A. Provorov, N.I. Vorobyov, E.E. Andronov, 2008, published in Genetika, 2008, Vol. 44, No. 1, pp. 12–28.

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Provorov, N.A., Vorobyov, N.I. & Andronov, E.E. Macro- and microevolution of bacteria in symbiotic systems. Russ J Genet 44, 6–20 (2008). https://doi.org/10.1134/S102279540801002X

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