Polyploidy in archaea and bacteria: About desiccation resistance, giant cell size, long-term survival, enforcement by a eukaryotic host and additional aspects

Journal of Molecular Microbiology and Biotechnology

Volumn 24, Issue 5-6, 2014, Pages 409-419

  Soppa, Jörg ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

Archaea; Bacteria; Polyploidy

Indexed keywords

GENOMIC DNA; PHOSPHATE;

ARCHAEON; AZOTOBACTER VINELANDII; BACTERIA; BACTERIAL CHROMOSOME; BACTERIAL GROWTH; BIODIVERSITY; CELL SIZE; CHROMOSOME SEGREGATION; DEINOCOCCUS RADIODURANS; DESICCATION; EPULOPISCIUM; GENE CONVERSION; GEOLOGICAL TIME; GIANT CELL; HALOBACTERIALES; HALOFERAX VOLCANII; HOMOLOGOUS RECOMBINATION; IONIZING RADIATION; LONG TERM SURVIVAL; METHANOCALDOCOCCUS JANNASCHII; METHANOCOCCUS MARIPALUDIS; METHANOGENIC ARCHAEON; NONHUMAN; POLYPLOIDY; PROKARYOTE; RADIOSENSITIVITY; REVIEW; SINORHIZOBIUM MELILOTI; SOIL MICROFLORA; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; GENETICS; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

AZOTOBACTER VINELANDII; DEINOCOCCUS RADIODURANS; EPULOPISCIUM; EUKARYOTA; HALOFERAX VOLCANII; METHANOCALDOCOCCUS JANNASCHII; METHANOCOCCUS MARIPALUDIS; PROKARYOTA; SINORHIZOBIUM MELILOTI;

ARCHAEA; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; POLYPLOIDY; STRESS, PHYSIOLOGICAL;

EID: 84927780574     PISSN: 14641801     EISSN: 16602412     Source Type: Journal    
DOI: 10.1159/000368855     Document Type: Review

References (87)

1. Anderson AW, Norden H, Cain RF, Parriah G, Duggan D. Studies on the radio-resistant micrococcus. I. The isolation, morphology, cultural characteristics and resistance to gamma radiation. Food Technol 1956; 10: 575-577
2. Angert ER. DNA replication and genomic architecture of very large bacteria. Annu Rev Microbiol 2012; 66: 197-212
3. Angert ER, Clements KD. Initiation of intracellular offspring in Epulopiscium. Mol Microbiol 2004; 51: 827-835
4. Angert ER, Clements KD, Pace NR. The largest bacterium. Nature 1993; 362: 239-241
5. Basu B, Apte SK. Gamma radiation-induced proteome of Deinococcus radiodurans primarily targets DNA repair and oxidative stress alleviation. Mol Cell Proteomics 2012; 11:M111011734
6. Bentchikou E, Servant P, Coste G, Sommer S. A major role of the RecFOR pathway in DNA double-strand break repair through ESDSA in Deinococcus radiodurans. PLoS Genet 2010; 6:e10000774
7. Bishop PE, Premakumar R. Alternative nitrogen fixation systems; in Stacey G, Burris RH, Evans HJ (eds): Biological Nitrogen Fixation. New York, Chapman and Hall, 1992, pp 736-762
8. Bouthier de la Tour C, Boisnard S, Norais C, Toueille M, Bentchikou E, Vannier F, Cox MM, Sommer S, Servant P. The deinococcal DdrB protein is involved in an early step of DNA double strand break repair and in transformation through its single-strand annealing activity. DNA Repair 2011; 10: 1223-1231
9. Bouthier de la Tour CB, Pasot FM, Toueille M, Mirabella B, Guerin P, Blanchard L, Servant P, de Groot A, Sommer S, Armengaud J. Comparative proteomics reveals key proteins recruited to the nucleoid of Deinococcus after radiation-induced DNA damage. Proteomics 2013; 13: 3457-3469
10. Bresler V, Montgomery WL, Fishelson L, Pollak PE. Gigantism in a bacterium, Epulopiscium fishelsoni, correlates with complex patterns in arrangement, quantity, and segregation of DNA. J Bacteriol 1998; 180: 5601-5611
11. Breuert S, Allers T, Spohn G, Soppa J. Regulated polyploidy in halophilic archaea. PLoS One 2006; 1:e92
12. Cavero S, Limbo O, Russel P. Critical functions of Rpa3/Ssb3 in S-phase DNA damage response in fission yeast. PLoS Genet 2010; 6:e1001138
13. Contreras A, Casadesus J. Tn10 mutagenesis in Azotobacter vinelandii. Mol Gen Genet 1987;209: 276-282
14. Dedieu A, Sahinovic E, Guerin P, Blanchard L, et al. Major soluble proteome changes in Deinococcus deserti over the earliest stages following gamma-ray irradiation. Proteome Sci 2013; 11: 3
15. De Veaux LC, Muller JA, Smith J, Petrisko J, Wells DP, DasSarma S. Extremely radiation-resistant mutants of a halophilic archaeon with increased single-stranded DNA-binding protein (RPA) gene expression. Radiat Res 2007; 168: 507-514
16. Farkas A, Maroti G, Durgo H, Gyorgypal Z, Lima RM, Medzihradszky KF, Kereszt A, Mergaert P, Kondorosi E. Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms. Proc Natl Acad Sci USA 2014; 111: 5183-5188
17. Fendrihan S, Berces A, Lammer H, Musso M, Ronto G, Polacsek TK, et al. Investigating the effects of simulated Martian ultraviolet radiation on Halococcus dombrowskii and other extremely halophilic archaebacteria. Astrobiology 2009; 9: 104-112
18. Fendrihan S, Dornmayer-Pfaffenhuemer M, Gerbl FW, Holzinger A, Grosbacher B, Briza P, et al. Spherical particles of halophilic archaea correlate with exposure to low water activity-implications for microbial survival in fluid inclusions of ancient halite. Geobiology 2012; 10: 424-433
19. Fishelson L, Montgomery WL, Myrberg AA. A unique symbiosis in the gut of tropical herbivorous surgeonfish (Acanthuridae, Teleostei) from the Red Sea. Science 1985; 229: 49-51
20. Flint JF, Drzymalski D, Montgomery WL, Southam G, Angert ER. Nocturnal production of endospores in natural populations of epulopiscium-like surgeonfish symbionts. J Bacteriol 2005; 187: 7460-7470
21. Gavini N, Burgess BK. FeMo cofactor synthesis by a nifH mutant with altered MgATP reactivity. J Biol Chem 1992; 267: 21179-21186
22. Gavini N, Hausman BS, Pulakat L, Schreiner RP, Willisamson JA. Identification and mutational analysis of rfbG, the gene encoding CDP-Dglucose- 4,6-dehydratase, isolated from free living soil bacterium Azotobacter vinelandii. Biochem Biophys Res Commun 1997; 240: 153-161
23. Gramain A, Diaz GC, Demergasso C, Lowenstein TK, McGenity TJ. Archaeal diversity along a subterranean salt core from the Salar Grande (Chile). Environ Microbiol 2011; 13: 2105-2121
24. Grant WD, Gemmell RT, McGenity TJ. Halobacteria: the evidence for longevity. Extremophiles 1998; 2: 279-287
25. Griese M, Lange C, Soppa J. Ploidy in cyanobacteria. FEMS Microbiol Lett 2011; 323: 124-131
26. Gruber C, Legat A, Pfaffenhuemer M, Radax C, Weidler G, Busse HJ, Stan-Lotter H. Halobacterium noricense sp. nov., an archaeal isolate from a bore core of an alpine Permian salt deposit, classification of Halobacterium sp. NRC-1 as a strain of H. salinarum and emended description of H. salinarum. Extremophiles 2004; 8: 431-439
27. Hansen MT. Multiplicity of genome equivalents in the radiation-resistant bacterium Micrococcus radiodurans. J Bacteriol 1978; 134: 71-75
28. Hildenbrand C, Stock T, Lange C, Rother M, Soppa J. Genome copy numbers and gene conversion in methanogenic archaea. J Bacteriol 2011; 193: 734-743
29. Hudson JJ, Tailor WD, Schindler DW. Phosphate concentrations in lakes. Nature 2000;406: 54-56
30. Jain IH, Vijayan V, OShea EK. Spatial ordering of chromosomes enhances the fidelity of chromosome partitioning in cyanobacteria Proc Natl Acad Sci USA 2012; 109: 13638-13643
31. Jakkola ST, Zerulla K, Buo Q, Liu Y, Ma H, Yang C, Bamford DH, Chen X, Soppa J, Oksanen H. Halophilic archaea cultivated from surface sterilized middle-late Eocene rock salt are polyploid. PLoS One 2014; 9:e110533
32. Kanesaki Y, Shiwa Y, Tajima N, Suzuki M, Watanabe S, Sato N, Ikeuchi M, Yoshikowa H. Identification of substrain-specific mutations by massively parallel whole-genome resequencing of Synechocystis sp. PCC 6803. DNA Res 2012; 19: 67-79
33. Khakhlova O, Bock R. Elimination of deleterious mutations in plastid genomes by gene conversion. Plant J 2006; 46: 85-94
34. Kondorosi E, Mergaert P, Kereszt A. A paradigm for endosymbiotic life: cell differentiation of Rhizobium bacteria provoked by host plant factors. Annu Rev Microbiol 2013; 67: 611-628
35. Krisko A, Radman M. Protein damage and death by radiation in Escherichia coli and Deinococcus radiodurans. Proc Natl Acad Sci USA 2010; 107: 14373-14377
36. Krisko A, Radman M. Biology of extreme radiation resistance: the way of Deinococcus radiodurans. Cold Spring Harb Perspect Biol 2014; 5:a012765
37. Lange C, Zerulla K, Breuert S, Soppa J. Gene conversion results in the equalization of genome copies in the polyploid haloarchaeon Haloferax volcanii. Mol Microbiol 2011; 80: 666-677
38. Lawson MJ, Jiao J, Fan W, Zhang L. A pattern analysis of gene conversion literature. Comp Funct Genomics 2009; 761512
39. Liu Y, Zhou J, Omelchenko MV, Beliaev AS, Venkateswaran A, Stair J, et al. Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation. Proc Natl Acad Sci USA 2003; 100: 4191-4196
40. Lockhart JS, DeVeaux LC. The essential role of the Deinococcus radiodurans ssb gene in cell survival and radiation tolerance. PLoS One 2013; 8:e71651
41. Luan H, Meng N, Fu J, Chen X, Xu X, Feng Q, Jiang H, Dai J, Yuan X, Lu Y, Roberts AA, Luo X, Chen M, Xu S, Li J, Hamilton CJ, Fang C, Wang J. Genome-wide transcriptome and antioxidant analyses on gamma-irradiated phases of Deinococcus radiodurans R1. PLoS One 2014; 9:e85649
42. Madigan M, Martinko J, Stahl D, Clark D. Biology of Microorganisms. San Francisco, Pearson Education, 2012, pp 1150
43. Malandrin L, Huber H, Bernander R. Nucleoid structure and partition in Methanococcus jannaschii: an archaeon with multiple copies of the chromosome. Genetics 1999; 152: 1315-1323
44. Maldonado R, Garzon A, Dean DR, Casadesus J. Gene dosage analysis in Azotobacter vinelandii. Genetics 1992; 132: 869-878
45. Maldonado R, Jimenez J, Casadesus J. Changes of ploidy during the Azotobacter vinelandii growth cycle. J Bacteriol 1994; 176: 3911-3919
46. Mattimore V, Battista JR. Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J Bacteriol 1996; 178: 633-637
47. Mattimore V, Udupa KS, Berne GA, Battista JR. Genetic characterization of forty ionizing radiation- sensitive strains of Deinococcus radiodurans: linkage information from transformation. J Bacteriol 1995; 177: 5232-5237
48. Mendell JE, Clements KD, Choat JH, Angert ER. Extreme polyploidy in a large bacterium. Proc Natl Acad Sci USA 2008; 105: 6730-6734
49. Mergaert P, Uchiumi T, Alunni B, Evanno G, Cheron A, Catrice O, Mausset AE, Barloy- Hubler F, Galibert F, Kondorosi A, Kondorosi E. Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium - legume symbiosis. Proc Natl Acad Sci USA 2006; 103: 5230-5235
50. Michelsen O, Hansen FG, Albrechtsen B, Jensen PR. The MG1363 and IL1403 laboratory strains of Lactococcus lactis and several dairy strains are diploid. J Bacteriol 2010; 192: 1058-1065
51. Miller DA, Suen G, Clements KD, Angert ER. The genomic basis for the evolution of a novel form of cellular reproduction in the bacterium Epulopiscium. BMC Genomics 2012; 13: 265
52. Montgomery WL, Pollak PE. Epulopiscium fishelsoni NG sp., a protist of uncertain taxonomic affinities from the gut of herbivorous reef fish. J Protozool 1988; 35: 565-569
53. Muller HJ. The relation of recombination to mutational advance. Mutat Res 1964; 106: 2-9
54. Park JS, Vreeland RH, Cho BC, Lowenstein TK, Timofeeff MN, Rosenzweig WD. Haloarchaeal diversity in 23, 121 and 419 MYA salts. Geobiology 2009; 7: 515-523
55. Pecoraro V, Zerulla K, Lange C, Soppa J. Quantification of ploidy in proteobacteria revealed the existence of monoploid, (mero-)oligoploid and polyploid species. PLoS One 2011; 6:e16392
56. Penterman J, Abo RP, De Nisco NJ, Arnold MF, Longhi R, Zanda M, Walker GC. Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis. Proc Natl Acad Sci USA 2014; 111: 3561-3566
57. Petersen TW, Harrison CB, Horner DN, van den Engh G. Flow cytometric characterization of marine microbes. Methods 2012; 57: 350-358
58. Pfeiffer F, Schuster SC, Broicher A, Falb M, Palm P, Rodewald K, Ruepp A, Soppa J, Tittor J, Oesterhelt D. Evolution in the laboratory: the genome of Halobacterium salinarum strain R1 compared to that of strain NRC-1. Genomics 2008a; 91: 335-346
59. Pfeiffer F, Schuster SC, Broicher A, Falb M, Palm P, Rodewald K, Ruepp A, Soppa J, Tittor J, Oesterhelt D. Genome sequences of Halobacterium salinarum: a reply. Genomics 2008b; 91: 553-554
60. Pulakat L, Efuet ET, Gavini N. Segregation pattern of kanamycin resistance marker in Azotobacter vinelandii did not show the constraints expected in a polyploid bacterium. FEMS Microbiol Lett 1998; 160: 247-252
61. Pulakat L, Hausman BS, Lei S, Gavini N. Nif-phenotype of Azotobacter vinelandii UW97 Characterization and mutational analysis. J Biol Chem 1996; 271: 1884-1889
62. Robson RL, Chesshyre JA, Wheeler C, Jones R, Woodley PR, Postgate JR. Genome size and complexity in Azotobacter chroococcum. J Gen Microbiol 1984; 130: 1603-1612
63. Sadoff HL, Berke E, Loperfido B. Physiological studies of encystment in Azotobacter vinelandii. J Bacteriol 1971; 105: 185-189
64. Sadoff HL, Shimel B, Ellis S. Characterization of Azotobacter vinelandii deoxyribonucleic acid and folded chromosomes. J Bacteriol 1979; 138: 871-877
65. Sanders SW, Maxcy RB. Isolation of radiationresistant bacteria without exposure to irradiation. Appl Environ Microbiol 1979; 38: 436-439
66. Santoyo G, Romero D. Gene conversion and concerted evolution in bacterial genomes. FEMS Microbiol Rev 2005; 29: 169-183
67. Schattenhofer M, Wulf J, Kostadinov I, Glockner FO, Zubkov MV, Fuchs BM. Phylogenetic characterisation of picoplanktonic populations with high and low nucleic acid content in the North Atlantic Ocean. Syst Appl Microbiol 2011; 34: 470-475
68. Schneider D, Fuhrmann E, Scholz I, Hess WR, Graumann PL. Fluorescence staining of live cyanobacterial cells suggest non-stringent chromosome segregation and absence of a connection between cytoplasmic and thylakoid membranes. BMC Cell Biol 2007; 8: 39
69. Schubert BA, Lowenstein TK, Timofeeff MN, Parker MA. Halophilic Archaea cultured from ancient halite, Death Valley, California. Environ Microbiol 2010; 12: 440-454
70. Schulz HN, Jorgensen BB. Big bacteria. Annu Rev Microbiol 2001; 55: 105-137
71. Slade D, Lindner AB, Paul G, Radman M. Recombination and replication in DNA repair of heavily irradiated Deinococcus radiodurans. Cell 2009; 136: 1044-1055
72. Stan-Lotter H. Biotic survival over geological times. Astrobiology 2004; 4: 325-326
73. Stan-Lotter H, Pfaffenhuemer M, Legat A, Busse HJ, Radax C, Gruber C. Halococcus dombrowskii sp. nov., an archaeal isolate from a Permian alpine salt deposit. Int J Syst Evol Microbiol 2002; 52: 1807-1814
74. Stock T, Selzer M, Rother M. In vivo requirement of selenophosphate synthesis in archaea. Mol Microbiol 2010; 75: 149-160
75. Suh MH, Pulakat L, Gavini N. Isolation and characterization of nifDK :kanamycin and nitrogen fixation proficient Azotobacter vinelandii strain, and its implication on the status of multiple chromosomes in Azotobacter. Genetica 2000; 110: 101-107
76. Toukdarian A, Saunders G, Selman-Sosa G, Santero E, Woodley P, Kennedy C. Molecular analysis of the Azotobacter vinelandii glnA gene encoding glutamine synthetase. J Bacteriol 1990;172: 6529-6539
77. Trigui H, Masmoudi S, Brochier-Armanet C, Barani A, Gregori G, Denis M, Dukan S, Maalej S. Characterization of hetertrophic prokaryote subgroups in the Sfax coastal solar salterns by combining flow cytometry cell sorting and phylogenetic analysis. Extremophiles 2011; 15: 347-358
78. van de Velde W, Zehirov G, Szatmar A, Debreczeny M, Ishihara H, et al. Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 2010; 327: 1122-1126
79. Vila-Costa M, Gasol JM, Sharma S, Moran MA. Community analysis of high- and low-nucleic acid-containing bacteria in NW Mediterranean coastal waters using 16S rDNA pyrosequencing. Environ Microbiol 2012; 14: 1390-1402
80. Vreeland RH, Piselli AF Jr, McDonnough S, Meyers SS. Distribution and diversity of halophilic bacteria in a subsurface salt formation. Extremophiles 1998; 2: 321-331
81. Ward RJ, Clements KD, Choat JH, Angert ER. Cytology of terminally differentiated Epulopiscium mother cells. DNA Cell Biol 2009; 28: 57-64
82. Xiao W, Wang ZG, Wang YX, Schneegurt MA, Li ZY, Lai YH, et al. Comparative molecular analysis of the prokaryotic diversity of two salt mine soils in southwest China. J Basic Microbiol 2013; 53: 942-952
83. Zahradka K, Slade D, Bailone A, Sommer S, Averbeck D, Petranovic M, Lindner AB, Radman M. Reassembly of shattered chromosomes in Deinococcus radiodurans. Nature 2006; 443: 569-573
84. Zerulla K, Baumann A, Soppa J. Cell cycle and polyploidy in haloarchaea; in Papke RT, Oren A (eds): Genetics and Genomics of Halophiles. Norfolk, Horizon Scientific Press 2014a, pp 145-166
85. Zerulla K, Chimileski S, Nather D, Gophna U, Papke RT, Soppa J. DNA as a phosphate storage polymer and the alternative advantages of polyploidy for growth or survival. PLoS One 2014b;9:e94819
86. Zerulla K, Soppa J. Polyploidy in haloarchaea: advantages for growth and survival. Front Microbiol 2014; 5: 274
87. Zhang C, Wei J, Zheng Z, Ying N, et al. Proteomic analysis of Deinococcus radiodurans recovering from gamma irradiation. Proteomics 2005; 5: 138-143