The prospects for Symbiogenetics: emergence of superorganismal genomes and reconstruction of cellular evolution (mini-review)
DOI:
https://doi.org/10.21638/spbu03.2023.105Abstract
The superspecies systems of heredity that arise via coevolution of nonrelated organisms are represented as the subjects of Symbiogenetics, a new research field addressing integration of the heterologous genomes. Evolutionary mechanisms responsible for this integration include: a) interspecies altruism based on the symbionts' refusal from autonomous existence; b) inheritance of symbionts by hosts as of acquired genetic determinants (pangenesis). Under impacts of these factors, endosymbionts may be transformed into the cellular organelles that have lost biological and genetic individuality and sometimes lack their own genomes. The genomically truncated organelles that have retained the abilities for reproduction and metabolism are considered as the models to reconstruct the early stages of cell evolution, including the emergence of its genome.
Keywords:
Symbiogenetics, organellogenesis, hologenomes and symbiogenomes, pangenesis, biological altruism, open genetic systems, biological and genetic individuality, natural selection
Downloads
Download data is not yet available.
References
Andronov, E. E., Igolkina, A. A., Kimeklis, A. K., Vorobyov, N. I., and Provorov, N. A. 2015. Characteristics of natural selection in populations of nodule bacteria (Rhizobium leguminosarum) interacting with different host plants. Russian Journal of Genetics 51:949–956. https://doi.org/10.1134/S1022795415100026
Benzer, S. 1957. The elementary units of heredity; pp. 70–93 in W. D. McElroy and B. Glass (eds), The Chemical Basis of Heredity. Johns Hopkins Press. Baltimore, Maryland.
Bingham, E. T., Groose, R. W., Woodfield, D. R., and Kidwell, K. K. 1994. Complementary gene interactions in alfalfa are greater in autotetraploids than diploids. Crop Science 34:823–829. https://doi.org/10.2135/cropsci1994.0011183X003400040001x
Brueckner, J. and Martin, W. F. 2020. Bacterial genes outnumber archaeal genes in eukaryotic genomes. Genome Biology and Evolution 12:282–292. https://doi.org/10.1093/gbe/evaa047
Claverie, J. M. 2006. Viruses take center stage in cellular evolution. Genome Biology 7:110–115. https://doi.org/10.1186/gb-2006-7-6-110
Darlington, P. J. 1978. Altruism: its characteristics and evolution. Proceedings of the National Academy of Sciences USA 75:385–389. https://doi.org/10.1073/pnas.75.1.385
Darwin, Ch. 1872. The Origin of Species by Means of Natural Selection or the Preservation of Favored Races in the Struggle for Life. 6th ed. 526 pp. John Murray. London.
Denison, R. F. and Kiers, E. T. 2004. Lifestyle alternatives for rhizobia: mutualism, parasitism and foregoing symbiosis. FEMS Microbiology Letters 237:187–193. https://doi.org/10.1016/j.femsle.2004.07.013
Dobzhansky, Th. 1970. Genetics of the evolutionary process. 315 pp. Columbia University Press. New York.
Flor, H. H. 1946. Genetics of pathogenicity in Melampsora lini. Journal of Agricultural Research 73:335–357.
Goryacheva, I. and Andrianov, B. 2021. Reproductive parasitism in insects. The interaction of host and bacteria. Biological Communications 66:17–27. https://doi.org/10.21638/spbu03.2021.103
Harun, A. Y. and Sali, K. 2019. Factors affecting rumen microbial protein synthesis: A review. Veterinary Medicine — Open Journal 4:27–35. https://doi.org/10.17140/VMOJ-4-133
Hurek, T., Handley, L. L., Reinhold-Hurek, B., and Piche, Y. 2002. Azoarcus grass endophytes contribute fixed nitrogen to the plant in an uncilturable state. Molecular Plant-Microbe Interactions 15:233–242. https://doi.org/10.1094/MPMI.2002.15.3.233
Igolkina, A. A., Bazykin, G. A., Chizhevskaya, E. P. Provorov, N. A., and Andronov, E. E. 2019. Matching population diversity of rhizobial nodA and legume NFR5 genes in plant-microbe symbiosis. Ecology and Evolution 9:10377–10386. https://doi.org/10.1002/ece3.5556
Inge-Vechtomov, S. G. 1983. Introduction into Molecular Genetics. 343 pp. Vysshaia shkola Publ. Moscow. (In Russian)
Inge-Vechtomov, S. G. 2015. Genetics in Retrospect. 336 pp. N‑L Publ. St. Petersburg (In Russian)
Jones, J. D. and Dangl, J. L. 2006. The plant immune system. Nature 444(7117):323–329. https://doi.org/10.1038/nature05286
Katz, L. A. 2015. Recent events dominate interdomain lateral gene transfers between prokaryotes and eukaryotes and, with the exception of endosymbiotic gene transfers, few ancient transfer events persist. Philosophical Transactions of the Royal Society B 370:20140324. https://doi.org/10.1098/rstb.2014.0324
Koga, R., Tsuchida, T., and Fukatsu, T. 2003. Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proceedings of the Royal Society B 270:2543–2550. https://doi.org/10.1098/rspb.2003.2537
Kozo-Polyanski, B. M. 1924. New Principle of Biology. Review of the Symbiogenesis Theory. 124 pp. Puchina Publ. Moscow. (In Russian)
Kumar, K., Mella-Herrera, R. A., and Golden, J. W. 2010. Cyanobacterial heterocysts. Cold Spring Harbor Perspectives in Biology 2:a000315. https://doi.org/10.1101/cshperspect.a000315
Kurihara, K., Tamura, M., Shohda, K., Toyota, T., Suzuki, K., and Sugawara, T. 2011. Self-reproduction of supramolecular giant vesicles combined with the amplification of encapsulated DNA. Nature Chemistry 3:775–781. https://doi.org/10.1038/nchem.1127
Lobashev, M. E. 1967. Genetics. 751 pp. Leningrad University Publ. Leningrad. (In Russian)
Loegering, W. Q. 1978. Current concepts of inter-organismal genetics. Annual Review of Phytopathology 16:309–320. https://doi.org/10.1146/annurev.py.16.090178.001521
Margulis, L. 1996. Archaeal-eubacterial mergers in the origin of Eukarya: phylogenetic classification of life. Proceedings of the National Academy of Sciences USA 93:1071–1076. https://doi.org/10.1073/pnas.93.3.1071
Matveeva, T. 2021. New naturally transgenic plants: 2020 update. Biological Communications 66:36–46. https://doi.org/10.21638/spbu03.2021.105
Mereschkowsky, C. 1909. Theory of two plasms as a basis of symbiogeneis, new concept on the origin of organisms. 102 pp. Tipografiia Imperatorskogo universiteta Publ. Kazan. (In Russian)
Mereschkowsky, C. 1910. Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre von der Entstehung der Organismen. Biol. Centralbl. 30:278–288.
Nutman, P. S. 1946. Genetic factors concerned in the symbiosis of clover and nodule bacteria. Nature 157:463–465. https://doi.org/10.1038/157463a0
Oberholzer, T., Wick, R., Luisi, P. L., and Biebricher, C. K. 1995. Enzymatic RNA replication in self-reproducing vesicles: an approach to a minimal cell. Biochemical and Biophysical Research Communications 207:250–257. https://doi.org/10.1006/bbrc.1995.1180
Oda, Y., Larimer, F. W., and Chain, P. S. 2008. Multiple genome sequences reveal adaptations of a phototrophic bacterium to sediment microenvironments. Proceedings of the National Academy of Sciences USA 105:18543–18548. https://doi.org/10.1073/pnas.0809160105
Onishchuk, O. P., Vorobyov, N. I., and Provorov, N. A. 2017. Nodulation competitiveness of nodule bacteria: genetic control and adaptive impacts. Applied Biochemistry and Microbiology 53:117–124. https://doi.org/10.1134/S0003683817020132
Phillips, P. C. 2008. Epistasis — the essential role of gene interactions in the structure and evolution of genetic systems. Nature Reviews Genetics 9:855–867. https://doi.org/10.1038/nrg2452
Provorov, N. A. 2021. Genetic individuality and inter-species altruism: modelling of symbiogenesis using different types of symbiotic bacteria. Biological Communications 66:65–71. https://doi.org/10.21638/spbu03.2021.108
Provorov, N. A., Onishchuk, O. P., Yurgel, S. N., and Simarov, B. V. 2014. Construction of highly-effective symbiotic bacteria: evolutionary models and genetic approaches. Russian Journal of Genetics 50:1125–1136. https://doi.org/10.1134/S1022795414110118
Provorov, N. A., Tikhonovich, I. A., and Vorobyov, N. I. 2016. Symbiogenesis as a model for reconstructing the early stages of genome evolution. Russian Journal of Genetics 52:117–124. https://doi.org/10.1134/S1022795416020101
Provorov, N. A., Tikhonovich, I. A., and Vorobyov, N. I. 2018. Symbiosis and Symbiogenesis. 464 pp. Inform-Navigator Publ. St. Petersburg. (In Russian)
Rey, F. and Harwood, C. S. 2010. FixK, a global regulator of microaerobic growth, controls photosynthesis in Rhodopseudomonas palustris. Molecular Microbiology 75:1007–1020. https://doi.org/10.1111/j.1365-2958.2009.07037.x
Rosenberg, E. and Zilber-Rosenberg, I. 2018. The hologenome concept of evolution after 10 years. Microbiome 6:78. https://doi.org/10.1186/s40168-018-0457-9
Sagan, D. 2021. From Empedocles to Symbiogeneics: Lynn Margulis’s revolutionary influence. on evolutionary biology. BioSystems 204:104386. https://doi.org/10.1016/j.biosystems.2021.104386
Shatskaya, N. V., Bogdanova, V. S., Kosterin, O. E., Vasiliev, G. V., Kimeklis, A. K., Andronov, E. E., and Provorov, N. A. 2019. Plastid and mitochondrial genomes of Vavilovia formosa (Stev.) Fed. and phylogeny of related legume genera. Vavilov Journal of Genetics and Breeding 23(8):972–980. https://doi.org/10.18699/VJ19.574
Smith, D. R. and Keeling, P. J. 2015. Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes. Proceedings of the National Academy of Sciences USA 112:10177–10184. https://doi.org/10.1073/pnas.1422049112
Smith, J. 1989. Generating novelty by symbiosis. Nature 341:284–285. https://doi.org/10.1038/341284a0
Sprent, J. I. 2001. Nodulation in legumes. 105 pp. Cromwell Press Ltd., Kew Royal Botanical Gardens. London.
Tikhonovich, I. A. and Provorov, N. A. 2009. From plant-microbe interactions to Symbiogenetics: a universal paradigm for the inter-species genetic integration. Annals of Applied Biology 154:341–350. https://doi.org/10.1111/j.1744-7348.2008.00306.x
Tikhonovich, I. A. and Provorov, N. A. 2012. Development of symbiogenetics approaches for studying variation and heredity of superspecies systems. Russian Journal of Genetics 48:357–368. https://doi.org/10.1134/S1022795412040126
Tikhonovich, I. A., Andronov, E. E., Borisov, A. Yu., Dolgikh, E. A., Zhernakov, A. I., Provorov, N. A., Rumyantseva, M. L., and Simarov, B. V. 2015. The principle of genome complementarity in the enhancement of plant adaptive capacities. Russian Journal of Genetics 51:831–846. https://doi.org/10.1134/S1022795415090124
von Bertalanffy, L. 1968. General system theory: foundations, development, applications. 258 pp. George Braziller. New York.
Zakharov, I. and Shaikevich, E. 2021. Hereditary symbionts and mitochondria: distribution in insect populations and quasi-linkage of genetic markers. Biological Communications 66:6–16. https://doi.org/10.21638/spbu03.2021.102
Zilber-Rosenberg, I. and Rosenberg, E. 2008. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiology Reviews 32:723–735. https://doi.org/10.1111/j.1574-6976.2008.00123.x
Downloads
Published
2023-05-02
How to Cite
Provorov, N., & Tikhonovich, I. (2023). The prospects for Symbiogenetics: emergence of superorganismal genomes and reconstruction of cellular evolution (mini-review). Biological Communications, 68(1), 49–55. https://doi.org/10.21638/spbu03.2023.105
License
Articles of Biological Communications are open access distributed under the terms of the License Agreement with Saint Petersburg State University, which permits to the authors unrestricted distribution and self-archiving free of charge.
