Reduction of bacterial genome size and expansion resulting from obligate intracellular lifestyle and adaptation to soil habitat.

• Authors: Tomasz Stępkowski , Andrzej B Legocki
• Languages of publication: EN

Abstracts

EN

Prokaryotic organisms are exposed in the course of evolution to various impacts, resulting often in drastic changes of their genome size. Depending on circumstances, the same lineage may diverge into species having substantially reduced genomes, or such whose genomes have undergone considerable enlargement. Genome reduction is a consequence of obligate intracellular lifestyle rendering numerous genes expendable. Another consequence of intracellular lifestyle is reduction of effective population size and limited possibility of gene acquirement via lateral transfer. This causes a state of relaxed selection resulting in accumulation of mildly deleterious mutations that can not be corrected by recombination with the wild type copy. Thus, gene loss is usually irreversible. Additionally, constant environment of the eukaryotic cell renders that some bacterial genes involved in DNA repair are expandable. The loss of these genes is a probable cause of mutational bias resulting in a high A+T content. While causes of genome reduction are rather indisputable, those resulting in genome expansion seem to be less obvious. Presumably, the genome enlargement is an indirect consequence of adaptation to changing environmental conditions and requires the acquisition and integration of numerous genes. It seems that the need for a great number of capabilities is common among soil bacteria irrespective of their phylogenetic relationship. However, this would not be possible if soil bacteria lacked indigenous abilities to exchange and accumulate genetic information. The latter are considerably facilitated when housekeeping genes are physically separated from adaptive loci which are useful only in certain circumstances.

Keywords

EN

symbiosis; Rickettsia; rhizobium; genome; Buchnera

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2001
• Volume: 48
• Issue: 2
• Pages: 367-381

Dates

published

2001

received

2001-02-14

accepted

2001-05-9

Contributors

author

Tomasz Stępkowski

• Institute of Bioorganic Chemistry Polish Academy of Sciences, Poznań, Poland

author

Andrzej B Legocki

• Institute of Bioorganic Chemistry Polish Academy of Sciences, Poznań, Poland

References

• Alm, R.A., Ling, L.S., Moir, D.T., King, B.L., Brown, E.D., Doig, P.C., Smith, D.R., Noonan, B., Guild, B.C., de Jonge, B.L, Carmel, G., Tummino, P.J., Caruso, A., Uria-Nickelsen, M., Mills, D.M., Ives, C., Gibson, R., Merberg, D., Mills, S.D., Jiang, Q., Taylor, D.E., Vovis, G.F. & Trust, T.J. (1999) Genomic-sequence comparison of two unrelated isolates of the humangastric pathogen Helicobacter pylori. Nature 397, 176-180.
• Andersson, J.O. & Andersson, S.G. (1999) Genome degradation is an ongoing process in Rickettsia. Mol. Biol. Evol. 16, 1178-1191.
• Andersson, J.O. (2000) Evolutionary genomics: is Buchnera a bacterium or an organelle? Curr. Biol. 10, 866-868.
• Andersson, S.G. & Kurland, C.G. (1998) Reductive evolution of resident genomes. Trends Microbiol. 6, 263-268.
• Andersson, S.G., Zomorodipour, A., Andersson, J.O., Sicheritz-Ponten, T., Alsmark, U.C., Podowski, R.M., Naslund, A.K., Eriksson, A.S., Winkler, H.H. & Kurland, C.G. (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396, 133-140.
• Baldani, J.I., Weaver, R.W., Hynes, M.F. & Eardly, B.D. (1992) Utilization of carbon substrates, electrophoretic enzyme patterns, and symbiotic performance of plasmid-cured clover rhizobia. Appl. Environ. Microbiol. 58, 2308- 2314.
• Bandi, C., Anderson, T.J., Genchi, C. & Blaxter, M.L. (1998) Phylogeny of Wolbachia in filarial nematodes. Proc. R. Soc. Lond. B Biol. Sci. 265, 2407-2413.
• Baumann, P., Baumann, L., Lai, C.Y., Rouhbakhsh, D., Moran, N.A. & Clark, M.A. (1995) Genetics, physiology, and evolutionary relationships of the genus Buchnera: Intracellular symbionts of aphids. Annu. Rev. Microbiol. 49, 55-94.
• Berck, S., Perret, X., Quesada-Vincens, D., Prome, J.-C., Broughton, W.J. & Jabbouri, S. (1999) NolL of Rhizobium sp. strain NGR234 is required for O-acetyltransferase activity. J. Bacteriol. 181, 957-964.
• Broughton, W.J. & Perret, X. (1999) Genealogy of legume-rhizobium symbioses. Curr. Opin. Plant Biol. 2, 305-311.
• Brynnel, E.U., Kurland, C.G., Moran, N.A. & Andersson, S.G. (1998) Evolutionary rates for tuf genes in endosymbionts of aphids. Mol. Biol. Evol. 15, 574-582.
• Carlson, R.W., Sanjuan, J., Bhat, U.R., Glushka, J., Spaink, H.P., Wijfjes, A.H., van Brussel, A.A., Stokkermans, T.J., Peters, N.P. & Stacey, G. (1993) The structures and biological activities of the lipo-oligosaccharidenodulation signals produced by type I and II strains of Bradyrhizobium japonicum. J. Biol. Chem. 268, 18372-18381.
• Casjens, S. (1998) The diverse and dynamic structure of bacterial genomes. Annu. Rev. Genet. 32, 339-377.
• Chaintreuil, C., Giraud, E., Prin, Y., Lorquin, J., Ba, A., Gillis, M., de Lajudie, P. & Dreyfus, B. (2000) Photosynthetic bradyrhizobia are natural endophytes of the african wild rice Oryza breviligulata. Appl. Environ. Microbiol. 66, 5437-5447.
• Downie, A.J. (1998) Functions of rhizobial nodulation genes; in The Rhizobiaceae. Molecular Biology of Model Plant-Associated Bacteria (Spaink, H.P., Kondorosi, A., Hooykaas, P.J.J., eds.) pp. 387-402, Kluwer Academic Publishers.
• Fraser, C.M., Casjens, S., Huang, W.M., Sutton, G.G., Clayton, R., Lathigra, R., White, O., Ketchum, K.A., Dodson, R., Hickey, E.K., Gwinn, M., Dougherty, B., Tomb, J.F., Fleischmann, R.D., Richardson, D., Peterson, J., Kerlavage, A.R., Quackenbush, J., Salzberg, S., Hanson, M., van Vugt, R., Palmer, N., Adams, M.D., Gocayne, J., Venter, J.C., et al. (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390, 580-586.
• Fraser, C.M., Gocayne, J.D., White, O., Adams, M.D., Clayton, R.A., Fleischmann, R.D., Bult, C.J., Kerlavage, A.R., Sutton, G., Kelley, J.M., et al. (1995). The minimal gene complement of Mycoplasma genitalium. Science 270, 397-403.
• Freiberg, C., Fellay, R., Bairoch, A., Broughton, W.J., Rosenthal, A. & Perret, X. (1997) Molecular basis of symbiosis between Rhizobium and legumes. Nature 387, 394-401.
• Göttfert, M., Röthlisberger, S., Kündig, C., Beck, C., Marty, R. & Hennecke, H. (2001) Potential symbiosis-specific genes uncovered by sequencing a 410-kb DNA region of the Bradyrhizobium japonicum chromosome. J. Bacteriol. 183, 1405-1412.
• Hacker, J. & Kaper, J.B. (2000) Pathogenicity islands and the evolution of microbes. Annu. Rev. Microbiol. 54, 641-679.
• Handy, J. & Doolittle, R.F. (1999) An attempt to pinpoint the phylogenetic introduction of glutaminyl-tRNA synthetase among bacteria. J. Mol. Evol. 49, 709-715.
• Hanin, M., Jabbouri, S., Quesada-Vincens, D., Freiberg, C., Perret, X., Promé, J.C., Broughton, W.J. & Fellay, R. (1997) Sulphation of Rhizobium sp. NGR234 Nod factors is dependent on noeE, a new host-specificity gene. Mol. Microbiol. 24, 1119-1129.
• Hurst, G.D.D., Walker, L.E. & Majerus, M.E.N. (1996) Bacterial infections of hemocytes associated with the maternally inherited male-killing trait in british populations of the two spot ladybird, Adalia bipunctata. J. Invertebr. Pathol. 68, 286-292.
• Hynes, M.F. & McGregor, N.F. (1990) Two plasmids other than the nodulation plasmid are necessary for formation of nitrogen-fixing nodules by Rhizobium leguminosarum. Mol. Microbiol. 4, 567-574.
• Innes, R.W., Hirose, M.A. & Kuempel, P.L. (1988) Induction of nitrogen-fixing nodules on clover requires only 32 kilobase pairs of DNA from the Rhizobium trifolii symbiosis plasmid. J. Bacteriol. 170, 3793-3802.
• Jabbouri, S.B., Relić, B., Hanin, M., Kamalaprija, P., Burger, U., Promé, D., Promé, J.C. & Broughton, W.J. (1998) nolO and noeI (HsnIII) of Rhizobium sp. NGR234 are involved in 3-O-carbamoylation and 2-O-methylation of Nod factors. J. Biol. Chem. 273, 12047-12055.
• Kado, C.I. (2000) The role of the T-pilus in horizontal gene transfer and tumorigenesis. Curr. Opin. Microbiol. 3, 643-648.
• Kaneko, T., Nakamura, Y., Sato, S., Asamizu, E., Kato, T., Sasamoto, S., Watanabe, A., Idesawa, K., Ishikawa, A., Kawashima, K., Kimura, T., Kishida, Y., Kiyokawa, C., Kohara, M., Matsumoto, M., Matsuno, A., Mochizuki, Y., Nakayama, S., Nakazaki, N., Shimpo, S., Sugimoto, M., Takeuchi, C., Yamada, M. & Tabata, S. (2000) Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res. 7, 331-338.
• Komaki, K. & Ishikawa, H. (1999) Intracellular bacterial symbionts of aphids possess many genomic copies per bacterium. J. Mol. Evol. 48, 717-722.
• Kundig, C., Hennecke, H. & Gottfert, M. (1993) Correlated physical and genetic map of the Bradyrhizobium japonicum 110 genome. J. Bacteriol. 175, 613-622.
• Legocki, A.B., Karłowski, W.M., Podkowiński, J., Sikorski, M.M. & Stępkowski, T. (1997) Advances in molecular characterization of the yellow lupin-Bradyrhizobium sp. (Lupinus) symbiotic model; in NATO ASI Series, vol. G39: Biological Nitrogen Fixation for Ecology and Sustainable Agriculture (Legocki, A.B., Bothe, H. & Puhler, A., eds.) pp. 263-266, Springer-Verlag, Berlin, Heidelberg.
• Lerouge, P., Roche, P., Faucher, C., Maillet, F., Truchet, G., Prome, J.-C. & Denarie, J. (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344, 781-784.
• Lin, W.S., Cunneen, T. & Lee, C.Y. (1994) Sequence analysis and molecular characterization of genes required for the biosynthesis of type 1 capsular polysaccharide in Staphylococcus aureus. J. Bacteriol. 176, 7005-7016.
• Lopez-Lara, I.M., van den Berg, J.D., Thomas- Oates, J.E., Glushka, J., Lugtenberg, B.J. & Spaink, H.P. (1995) Structural identification of the lipo-chitin oligosaccharide nodulation. signals of Rhizobium loti. Mol. Microbiol. 15, 627-638.
• Mergaert, P., Van Montagu, M. & Holsters, M. (1997) Molecular mechanisms of Nod factor diversity. Mol. Microbiol. 25, 811-817.
• Moran, N.A. (1996) Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc. Natl. Acad. Sci. U.S.A. 93, 2873-2878.
• Moran, N.A. & Wernegreen, J.J. (2000) Lifestyle evolution in symbiotic bacteria: Insights from genomics. Trends Ecol. Evol. 15, 321-326.
• Moxon, E.R., Rainey, P.B., Nowak, M.A. & Lenski, R.E. (1994) Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr. Biol. 4, 24-33.
• Newman, E.B., Budman, L.I., Chan, E.C., Greene, R.C., Lin, R.T., Woldringh, C.L. & D'Ari, R. (1998) Lack of S-adenosylmethionine results in a cell division defect in Escherichia coli. J. Bacteriol. 180, 3614-3619.
• Ochman, H., Elwyn, S. & Moran, N.A. (1999) Calibrating bacterial evolution. Proc. Natl. Acad. Sci. U.S.A. 96, 12638-12643.
• Ochman, H., Lawrence, J.G. & Groisman, E.A. (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299-304.
• Oresnik, I.J., Liu, S.L., Yost, C.K. & Hynes, M.F. (2000) Megaplasmid pRme2011a of Sinorhizobium meliloti is not required for viability. J. Bacteriol. 182, 3582-3586.
• Perret, X., Freiberg, C., Rosenthal, A., Broughton, W.J. & Fellay, R. (1999) High-resolution transcriptional analysis of the symbiotic plasmid of Rhizobium sp. NGR234. Mol. Microbiol. 32, 415-425.
• Perret, X., Staehelin, C. & Broughton, W.J. (2000) Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64, 180-201.
• Preisig, O., Anthamatten, D. & Hennecke, H. (1993) Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis. Proc. Natl. Acad. Sci. U.S.A. 90, 3309- 3313.
• Preston, G., Haubold, B. & Rainey, P.B. (1998) Bacterial genomics and adaptation to life on plants: Implications for the evolution of pathogenicity and symbiosis. Curr. Opin. Microbiol. 1, 589-597.
• Price, N.P.J., Relic, B., Talmont, F., Lewin, A., Prome, D., Pueppke, S.G., Maillet, F., Denarie, J., Prome, J.-C. & Broughton, W.J. (1992) Broad-host range Rhizobium species strain NGR234 secretes a family of carbamoylated and fucosylated, nodulation signals that are O-acetylated and sulphated. Mol. Microbiol. 6, 3575-3584.
• Pueppke, S.G. & Broughton, W.J. (1999) Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol. Plant Microbe Interact. 12, 293-318.
• Quesada-Vincens, D., Hanin, M., Broughton, W.J. & Jabbouri, S. (1998) In vitro sulfotransferase activity of NoeE, a nodulation protein of Rhizobium sp. NGR234. Mol. Plant Microbe Interact. 11, 592-600.
• Raoult, D. & Roux, V. (1997) Rickettsioses as paradigms of new or emerging infectious diseases. Clin. Microbiol. Rev. 10, 694-719.
• Romero, D., Brom, S., Martinez-Salazar, J., Girard, M.L., Palacios, R. & Davila, G. (1991) Amplification and deletion of a nod-nif region in the symbiotic plasmid of Rhizobium phaseoli. J. Bacteriol. 173, 2435-2441.
• Rouhbakhsh, D., Lai, C.Y., von Dohlen, C.D., Clark, M.A., Baumann, L., Baumann, P., Moran, N.A. & Voegtlin, D.J. (1996) The tryptophan biosynthetic pathway of aphid endosymbionts (Buchnera): Genetics and evolution of plasmid-associated anthranilate synthase (trpEG) within the aphididae. J. Mol. Evol. 42, 414-421.
• Schlaman, H.R.M., Philips, D.A. & Kondorosi, E. (1998) Genetic organization and transcriptional regulation of rhizobial nodulation genes; in The Rhizobiaceae. Molecular Biology of Model Plant-Associated Bacteria (Spaink, H.P., Kondorosi, A. & Hooykaas, P.J.J., eds.) pp. 361-386, Kluwer Academic Publishers.
• Segovia, L., Pinero, D., Palacios, R. & Martinez-Romero, E. (1991) Genetic structure of a soil population of nonsymbiotic Rhizobium leguminosarum. Appl. Environ. Microbiol. 57, 426-433.
• 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.
• Sikorski, M.M., Stępkowski, T, Świderska, A., Biesiadka, J., Łotocka, B., Kopcińska, J., Golinowski, W. & Legocki, A.B. (1999) Differential expression of symbiosis-related genes in yellow lupine; in Highlights of Nitrogen Fixation Research (Martinez, E. & Hernandez, G., eds.) pp. 125-129, Kluwer Academic/Plenum Publishers, New York.
• Silva, F.J., van Ham, R.C., Sabater, B. & Latorre, A. (1998) Structure and evolution of the leucine plasmids carried by the endosymbiont (Buchnera aphidicola) from aphids of the family Aphididae. FEMS Microbiol. Lett. 168, 43-49.
• Smith, J.M., Smith, N.H., O'Rourke, M. & Spratt, B.G. (1993) How clonal are bacteria? Proc. Natl. Acad. Sci. U.S.A. 90, 4384-4388.
• Stacey, G., Luka, S., Sanjuan, J., Banfalvi, Z., Nieuwkoop, A.J., Chun, J., Forsberg, L.S. & Carlson, R.W. (1994) nodZ, a unique host-specific nodulation gene, is involved in the fucosylation of the lipooligosaccharide nodulation signal of Bradyrhizobium japonicum. J. Bacteriol. 176, 620-633.
• Stephens, R.S., Kalman, S., Lammel, C., Fan, J., Marathe, R., Aravind, L., Mitchell, W., Olinger, L., Tatusov, R.L., Zhao, Q., Koonin, E.V. & Davis, R.W. (1998) Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282, 754-759.
• Stępkowski., T., Świderska, A., Miedzinska, K., Czaplińska, M., Świderski, M., Biesiadka, J. & Legocki, A.B. (2001) Molecular and phylogenetic analysis of nodulation genes in Bradyrhizobium sp. WM9 (Lupinus) suggests early divergence of lupine lineage within the Bradyrhizobium genus. Submitted.
• Sullivan, J.T. & Ronson, C.W. (1998) Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc. Natl. Acad. Sci. U.S.A. 95, 5145-5149.
• Sy, A., Giraud, E., Jourand, P., Garcia, N., Willems, A., de Lajudie, P., Prin, Y., Neyra, M., Gillis, M., Boivin-Masson, C. & Dreyfus, B. (2001) Methylotrophic Methylobacterium nodulate and fix nitrogen in symbiosis with legumes. J. Bacteriol. 183, 214-220.
• Tomb, J.F., White, O., Kerlavage, A.R., Clayton, R.A., Sutton, G.G., Fleischmann, R.D., Ketchum, K.A., Klenk, H.P., Gill, S., Dougherty, B.A., Nelson, K., Quackenbush, J., Zhou, L., Kirkness, E.F., Peterson, S., Loftus, B., Richardson, D., Dodson, R., Khalak, H.G., Glodek, A., McKenney, K., Fitzegerald, L.M., Lee, N., Adams, M.D., Venter, J.C., et al. (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388, 539-547.
• Turner, S.L. & Young, J.P.W. (2000) The glutamine synthetases of rhizobia: Phylogenetics and evolutionary implications. Mol. Biol. Evol. 17, 309-319.
• van Berkum, P. & Eardly, B.D. (1998) Molecular evolutionary systematics of the Rhizobiaceae; in The Rhizobiaceae. Molecular Biology of Model Plant-Associated Bacteria (Spaink, H.P., Kondorosi, A. & Hooykaas, P.J.J., eds.) pp. 1-24, Kluwer Academic Publishers.
• Viprey, V., Del Greco, A., Golinowski, W., Broughton, W.J. & Perret, X. (1998) Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol. Microbiol. 28, 1381-1389.
• Wernegreen, J.J. & Moran, N.A. (1999) Evidence for genetic drift in endosymbionts (Buchnera): Analyses of protein-coding genes. Mol. Biol. Evol. 16, 83-97.