Examination of Prokaryotic Multipartite Genome Evolution through Experimental Genome Reduction
Rhizobia are free-living bacteria of agricultural and environmental importance that form root-nodules on leguminous plants and provide these plants with fixed nitrogen. Many of the rhizobia have a multipartite genome, as do several plant and animal pathogens. All isolates of the alfalfa symbiont, Sinorhizobium meliloti, carry three large replicons, the chromosome (∼3.7 Mb), pSymA megaplasmid (∼1.4 Mb), and pSymB chromid (∼1.7 Mb). To gain insight into the role and evolutionary history of these replicons, we have ‘reversed evolution’ by constructing a S. meliloti strain consisting solely of the chromosome and lacking the pSymB chromid and pSymA megaplasmid. As the resulting strain was viable, we could perform a detailed phenotypic analysis and these data provided significant insight into the biology and metabolism of S. meliloti. The data lend direct experimental evidence in understanding the evolution and role of the multipartite genome. Specifically the large secondary replicons increase the organism's niche range, and this advantage offsets the metabolic burden of these replicons on the cell. Additionally, the single-chromosome strain offers a useful platform to facilitate future forward genetic approaches to understanding and manipulating the symbiosis and plant-microbe interactions.
Vyšlo v časopise:
Examination of Prokaryotic Multipartite Genome Evolution through Experimental Genome Reduction. PLoS Genet 10(10): e32767. doi:10.1371/journal.pgen.1004742
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004742
Souhrn
Rhizobia are free-living bacteria of agricultural and environmental importance that form root-nodules on leguminous plants and provide these plants with fixed nitrogen. Many of the rhizobia have a multipartite genome, as do several plant and animal pathogens. All isolates of the alfalfa symbiont, Sinorhizobium meliloti, carry three large replicons, the chromosome (∼3.7 Mb), pSymA megaplasmid (∼1.4 Mb), and pSymB chromid (∼1.7 Mb). To gain insight into the role and evolutionary history of these replicons, we have ‘reversed evolution’ by constructing a S. meliloti strain consisting solely of the chromosome and lacking the pSymB chromid and pSymA megaplasmid. As the resulting strain was viable, we could perform a detailed phenotypic analysis and these data provided significant insight into the biology and metabolism of S. meliloti. The data lend direct experimental evidence in understanding the evolution and role of the multipartite genome. Specifically the large secondary replicons increase the organism's niche range, and this advantage offsets the metabolic burden of these replicons on the cell. Additionally, the single-chromosome strain offers a useful platform to facilitate future forward genetic approaches to understanding and manipulating the symbiosis and plant-microbe interactions.
Zdroje
1. HarrisonPW, LowerRP, KimNK, YoungJP (2010) Introducing the bacterial ‘chromid’: Not a chromosome, not a plasmid. Trends Microbiol 18: 141–148 doi:10.1016/j.tim.2009.12.010
2. LandetaC, DávalosA, CevallosMA, GeigerO, BromS, et al. (2011) Plasmids with a chromosome-like role in rhizobia. J Bacteriol 193: 1317–1326 doi:10.1128/JB.01184-10
3. CouturierE, RochaEP (2006) Replication-associated gene dosage effects shape the genomes of fast-growing bacteria but only for transcription and translation genes. Mol Microbiol 59: 1506–1518 doi:10.1111/j.1365-2958.2006.05046.x
4. Vieira-SilvaS, TouchonM, RochaEP (2010) No evidence for elemental-based streamlining of prokaryotic genomes. Trends Ecol Evol 25: 319–20 author reply 320–1. doi: 10.1016/j.tree.2010.03.001
5. DryseliusR, IzutsuK, HondaT, IidaT (2008) Differential replication dynamics for large and small Vibrio chromosomes affect gene dosage, expression and location. BMC Genomics 9: 559 doi:10.1186/1471-2164-9-559
6. CooperVS, VohrSH, WrocklageSC, HatcherPJ (2010) Why genes evolve faster on secondary chromosomes in bacteria. PLoS Comput Biol 6: e1000732 doi:10.1371/journal.pcbi.1000732
7. ChainPS, DenefVJ, KonstantinidisKT, VergezLM, AgullóL, et al. (2006) Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-mbp genome shaped for versatility. Proc Natl Acad Sci U S A 103: 15280–15287 doi:10.1073/pnas.0606924103
8. SlaterSC, GoldmanBS, GoodnerB, SetubalJC, FerrandSK, et al. (2009) Genome sequences of three Agrobacterium biovars help elucidate the evolution of multichromosome genomes in bacteria. J Bacteriol 191: 2501–2511 doi:10.1128/JB.01779-08
9. MichauxS, PaillissonJ, Carles-NuritMJ, BourgG, Allardet-ServentA, et al. (1993) Presence of two independent chromosomes in the Brucella melitensis 16 M genome. J Bacteriol 175: 701–705.
10. KanekoT, NakamuraY, SatoS, MinamisawaK, UchiumiT, et al. (2002) Complete genomic sequence of nitrogen fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 9: 189–197 doi:10.1093/dnares/9.6.189
11. Jumas-BilakE, Michaux-CharachonS, BourgG, O'CallaghanD, RamuzM (1998) Differences in chromosome number and genome rearrangements in the genus Brucella. Mol Microbiol 27: 99–106 doi:10.1046/j.1365-2958.1998.00661.x
12. MorenoE (1998) Genome evolution within the alpha proteobacteria: why do some bacteria not possess plasmids and others exhibit more than one different chromosome? FEMS Micriobiol Rev 22: 255–275 doi:10.1111/j.1574-6976.1998.tb00370.x
13. HeidelbergJF, EisenJA, NelsonWC, ClaytonRA, GwinnML, et al. (2000) DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406: 477–483 doi:10.1038/35020000
14. GonzálezV, SantamaríaRI, BustosP, Hernández-GonzálezI, Medrano-SotoA, et al. (2006) The partitioned Rhizobium etli genome: Genetic and metabolic redundancy in seven interacting replicons. Proc Natl Acad Sci U S A 103: 3834–3839 doi:10.1073/pnas.0508502103
15. GalardiniM, PiniF, BazzicalupoM, BiondiEG, MengoniA (2013) Replicon-dependent bacterial genome evolution: The case of Sinorhizobium meliloti. Genome Biol Evol 5: 542–558 doi:10.1093/gbe/evt027
16. XuQ, DziejmanM, MekalanosJJ (2003) Determination of the transcriptome of Vibrio cholerae during intraintestinal growth and midexponential phase in vitro. Proc Natl Acad Sci U S A 100: 1286–1291 doi:10.1073/pnas.0337479100
17. BeckerA, BergèsH, KrolE, BruandC, RübergS, et al. (2004) Global changes in gene expression in Sinorhizobium meliloti 1021 under microoxic and symbiotic conditions. Mol Plant Microbe Interact 17: 292–303 doi:10.1094/MPMI.2004.17.3.292
18. EganES, FogelMA, WaldorMK (2005) Divided genomes: Negotiating the cell cycle in prokaryotes with multiple chromosomes. Mol Microbiol 56: 1129–1138 doi:10.1111/j.1365-2958.2005.04622.x
19. GalibertF, FinanTM, LongSR, PühlerA, AbolaP, et al. (2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293: 668–672 doi:10.1126/science.1060966
20. EpsteinB, BrancaA, MudgeJ, BhartiAK, BriskineR, et al. (2012) Population genomics of the facultatively mutualistic bacteria Sinorhizobium meliloti and S. medicae. PLoS Genet 8: e1002868 doi:10.1371/journal.pgen.1002868
21. GuoHJ, WangET, ZhangXX, LiQQ, ZhangYM, et al. (2014) Replicon-dependent differentiation of symbiosis-related genes in Sinorhizobium strains nodulating Glycine max. Appl Environ Microbiol 80: 1245–1255 doi:10.1128/AEM.03037-13
22. FinanTM, WeidnerS, WongK, BuhrmesterJ, ChainP, et al. (2001) The complete sequence of the 1,683-kb pSymB megaplasmid from the N2-fixing endosymbiont Sinorhizobium meliloti. Proc Natl Acad Sci U S A 98: 9889–9894 doi:10.1073/pnas.161294698
23. BarnettMJ, FisherRF, JonesT, KompC, AbolaAP, et al. (2001) Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid. Proc Natl Acad Sci U S A 98: 9883–9888 doi:10.1073/pnas.161294798
24. OresnikIJ, LiuSL, YostCK, HynesMF (2000) Megaplasmid pRme2011a of Sinorhizobium meliloti is not required for viability. J Bacteriol 182: 3582–3586 doi:10.1128/JB.182.12.3582-3586.2000
25. HynesMF, QuandtJ, O'ConnellMP, PühlerA (1989) Direct selection for curing and deletion of Rhizobium plasmids using transposons carrying the Bacillus subtilis sacB gene. Gene 78: 111–120.
26. CharlesTC, FinanTM (1991) Analysis of a 1600-kilobase Rhizobium meliloti megaplasmid using defined deletions generated in vivo. Genetics 127: 5–20.
27. diCenzoG, MilunovicB, ChengJ, FinanTM (2013) The tRNAarg gene and engA are essential genes on the 1.7-mb pSymB megaplasmid of Sinorhizobium meliloti and were translocated together from the chromosome in an ancestral strain. J Bacteriol 195: 202–212 doi:10.1128/JB.01758-12
28. MilunovicB, diCenzoGC, MortonRA, FinanTM (2014) Cell growth inhibition upon deletion of four toxin-antitoxin loci from the megaplasmids of Sinorhizobium meliloti. J Bacteriol 196: 811–824 doi:10.1128/JB.01104-13
29. MacLellanSR, SmallboneLA, SibleyCD, FinanTM (2005) The expression of a novel antisense gene mediates incompatibility within the large repABC family of alpha-proteobacterial plasmids. Mol Microbiol 55: 611–623 doi:10.1111/j.1365-2958.2004.04412.x
30. ChengJ, PoduskaB, MortonRA, FinanTM (2011) An ABC-type cobalt transport system is essential for growth of Sinorhizobium meliloti at trace metal concentrations. J Bacteriol 193: 4405–4416 doi:10.1128/JB.05045-11
31. SalletE, RouxB, Sauviac, JardinaudMF, CarrèreS, et al. (2013) Next-generation annotation of prokaryotic genomes with EuGene-P: application to Sinorhizobium meliloti 2011. DNA Res 20: 339–354 doi:10.1093/dnares/dst014
32. PósfaiG, PlunkettG3rd, FehérT, FrischD, KeilGM, et al. (2006) Emergent properties of reduced-genome Escherichia coli. Science 312: 1044–1046 doi:10.1126/science.1126439
33. AraK, OzakiK, NakamuraK, YamaneK, SekiguchiJ, et al. (2007) Bacillus minimum genome factory: Effective utilization of microbial genome information. Biotechnol Appl Biochem 46: 169–178 doi:10.1042/BA20060111
34. HynesMF, McGregorNF (1990) Two plasmids other than the nodulation plasmid are necessary for formation of nitrogen-fixing nodules by Rhizobium leguminosarum. Mol Microbiol 4: 67–574 doi:10.1111/j.1365-2958.1990.tb00625.x
35. Moënne-LoccozY, BaldaniJI, WeaverRW (1995) Sequential heat-curing of Tn5-Mob-sac labeled plasmids from Rhizobium to obtain derivatives with various combinations of plasmids and no plasmid. Lett Appl Microbiol 20: 175–179 doi:10.1111/j.1472-765X.1995.tb00420.x
36. IwadateY, HondaH, SatoH, HashimotoM, KatoJ (2011) Oxidative stress sensitivity of engineered Escherichia coli cells with a reduced genome. FEMS Microbiol Lett 322: 25–33 doi:10.1111/j.1574-6968.2011.02331.x
37. FinanTM, KunkelB, De VosGF, SignerER (1986) Second symbiotic megaplasmid in Rhizobium meliloti carrying exopolysaccharide and thiamine synthesis genes. J Bacteriol 167: 66–72.
38. YurgelSN, MortimerMW, RiceJT, HumannJL, KahnML (2013) Directed construction and analysis of a Sinorhizobium meliloti pSymA deletion mutant library. Appl Environ Microbiol 79: 2081–2087 doi:10.1128/AEM.02974-12
39. StreitWR, JosephCM, PhillipsDA (1996) Biotin and other water-soluble vitamins are key growth factors for alfalfa root colonization by Rhizobium meliloti 1021. Mol Plant Microbe Interact 9: 330–338.
40. MortonER, MerrittPM, BeverJD, FuquaC (2013) Large deletions in the pAtC58 megaplasmid of Agrobacterium tumefaciens can confer reduced carriage cost and increased expression of virulence genes. Genome Biol Evol 5: 1353–1364 doi:10.1093/gbe/evt095
41. MellataM, AmeissK, MoH, CurtissR3rd (2010) Characterization of the contribution to virulence of three large plasmids of avian pathogenic Escherichia coli chi7122 (O78:K80:H9). Infect Immun 78: 1528–1541 doi:10.1128/IAI.00981-09
42. WongK, GoldingGB (2003) A phylogenetic analysis of the pSymB replicon from the Sinorhizobium meliloti genome reveals a complex evolutionary history. Can J Microbiol 49: 269–280 doi:10.1139/w03-037
43. MauchlineTH, FowlerJE, EastAK, SartorAL, ZaheerR, et al. (2006) Mapping the Sinorhizobium meliloti 1021 solute-binding protein-dependent transportome. Proc Natl Acad Sci U S A 103: 17933–17938 doi:10.1073/pnas.0606673103
44. PoystiNJ, LoewenED, WangZ, OresnikIJ (2007) Sinorhizobium meliloti pSymB carries genes necessary for arabinose transport and catabolism. Microbiology 153: 727–736 doi:10.1099/mic.0.29148-0
45. FinanTM, OresnikI, BottacinA (1988) Mutants of Rhizobium meliloti defective in succinate metabolism. J Bacteriol 170: 3396–3403.
46. GeddesBA, OresnikIJ (2012) Inability to catabolize galactose leads to increased ability to compete for nodule occupancy in Sinorhizobium meliloti. J Bacteriol 194: 5044–5053 doi:10.1128/JB.00982-12
47. WillisLB, WalkerGC (1999) A novel Sinorhizobium meliloti operon encodes an alpha-glucosidase and a periplasmic-binding-protein-dependent transport system for alpha-glucosides. J Bacteriol 181: 4176–4184.
48. JensenJB, PetersNK, BhuvaneswariTV (2002) Redundancy in periplasmic binding protein-dependent transport systems for trehalose, sucrose, and maltose in Sinorhizobium meliloti. J Bacteriol 184: 2978–2986 doi:10.1128/JB.184.11.2978-2986.2002
49. DingH, YipCB, GeddesBA, OresnikIJ, HynesMF (2012) Glycerol utilization by Rhizobium leguminosarum requires an ABC transporter and affects competition for nodulation. Microbiology 158: 1369–1378 doi:10.1099/mic.0.057281-0
50. SteeleTT, FowlerCW, GriffittsJS (2009) Control of gluconate utilization in Sinorhizobium meliloti. J Bacteriol 191: 1355–1358 doi:10.1128/JB.01317-08
51. BiondiEG, TattiE, CompariniD, GiuntiniE, MocaliS, et al. (2009) Metabolic capacity of Sinorhizobium (Ensifer) meliloti strains as determined by phenotype MicroArray analysis. Appl Environ Microbiol 75: 5396–5404 doi:10.1128/AEM.00196-09
52. RichardsonJS, HynesMF, OresnikIJ (2004) A genetic locus necessary for rhamnose uptake and catabolism in Rhizobium leguminosarum bv. trifolii. J Bacteriol 186: 8433–8442 doi:10.1128/JB.186.24.8433-8442.2004
53. LambertA, ØsteråsM, MandonK, PoggiMC, Le RudulierD (2001) Fructose uptake in Sinorhizobium meliloti is mediated by a high-affinity ATP-binding cassette transport system. J Bacteriol 183: 4709–4717 doi:10.1128/JB.183.16.4709-4717.2001
54. GageDJ, LongSR (1998) Alpha-galactoside uptake in Rhizobium meliloti: Isolation and characterization of agpA, a gene encoding a periplasmic binding protein required for melibiose and raffinose utilization. J Bacteriol 180: 5739–5748.
55. GeddesBA, OresnikIJ (2012) Genetic characterization of a complex locus necessary for the transport and catabolism of erythritol, adonitol and L-arabitol in Sinorhizobium meliloti. Microbiology 158: 2180–2191 doi:10.1099/mic.0.057877-0
56. KohlerPR, ZhengJY, SchoffersE, RossbachS (2010) Inositol catabolism, a key pathway in Sinorhizobium meliloti for competitive host nodulation. Appl Environ Microbiol 76: 7972–7980 doi:10.1128/AEM.01972-10
57. Kibitkin K (2011) Transport and metabolism of β-glycosidic sugars in Sinorhizobium meliloti. MSc thesis, McMaster University. Available at: http://hdl.handle.net/11375/9897. Accessed 10 July 2014.
58. GeddesBA, PickeringBS, PoystiNJ, CollinsH, YudistiraH, et al. (2010) A locus necessary for the transport and catabolism of erythritol in Sinorhizobium meliloti. Microbiology 156: 2970–2981 doi:10.1099/mic.0.041905-0
59. AmpomahOY, AvetisyanA, HansenE, SvensonJ, HuserT, et al. (2013) The thuEFGKAB operon of rhizobia and Agrobacterium tumefaciens codes for transport of trehalose, maltitol, and isomers of sucrose and their assimilation through the formation of their 3-keto derivatives. J Bacteriol 195: 3797–3807 doi:10.1128/JB.00478-13
60. MacleanAM, WhiteCE, FowlerJE, FinanTM (2009) Identification of a hydroxyproline transport system in the legume endosymbiont Sinorhizobium meliloti. Mol Plant Microbe Interact 22 (9) 1116–1127 doi:10.1094/MPMI-22-9-1116
61. WhiteCE, GavinaJM, MortonR, Britz-McKibbinP, FinanTM (2012) Control of hydroxyproline catabolism in Sinorhizobium meliloti. Mol Microbiol 85: 1133–1147 doi:10.1111/j.1365-2958.2012.08164.x
62. CharlesTC, AnejaP (1999) Methylmalonyl-CoA mutase encoding gene of sinorhizobium meliloti. Gene 226: 121–127 doi:10.1016/S0378-1119(98)00555-1
63. BoussauB, KarlbergEO, FrankAC, LegaultBA, AnderssonSG (2004) Computational inference of scenarios for alpha-proteobacterial genome evolution. Proc Natl Acad Sci U S A 101: 9722–9727 doi:10.1073/pnas.0400975101
64. PiniF, GalardiniM, BazzicalupoM, MengoniA (2011) Plant-bacteria association and symbiosis: are there common genomic trains in alphaproteobacteria? Genes 2: 1017–1032 doi:10.3390/genes2041017
65. RochaEPC (2006) Inference and analysis of the relative stability of bacterial chromosomes. Mol Biol Evol 23: 513–522 doi:10.1093/molbev/msj052
66. BringhurstRM, CardonZG, GageDJ (2001) Galactosides in the rhizosphere: Utilization by Sinorhizobium meliloti and development of a biosensor. Proc Natl Acad Sci U S A 98: 4540–4545 doi:10.1073/pnas.071375898
67. KneeEM, GongFC, GaoM, TeplitskiM, JonesAR, et al. (2001) Root mucilage from pea and its utilization by rhizosphere bacteria as a sole carbon source. Mol Plant Microbe Interact 14: 775–784 doi:10.1094/MPMI.2001.14.6.775
68. RamachandranVK, EastAK, KarunakaranR, DownieJA, PoolePS (2011) Adaptation of Rhizobium leguminosarum to pea, alfalfa and sugar beet rhizospheres investigated by comparative transcriptomics. Genome Biol 12: R106–2011-12-10-r106 doi:10.1186/gb-2011-12-10-r106
69. Perrine-WalkerFM, HynesMF, RolfeBG (2009) HocartCH (2009) Strain competition and agar affect the interaction of rhizobia with rice. Can J Microbiol 55: 1217–1223 doi:10.1139/w09-077
70. LynchD, O'BrienJ, WelchT, ClarkeP, Ó CuívP, et al. (2001) Genetic organization of the region encoding regulation, biosynthesis, and transport of rhizobactin 1021, a siderophore produced by Sinorhizobium meliloti. J Bacteriol 183: 2576–2585 doi:10.1128/JB.183.8.2576-2585.2001
71. Ó CuívP, ClarkeP, LynchD, O'ConnellM (2004) Identification of rhtX and fptX, novel genes encoding proteins that show homology and function in the utilization of the siderophores rhizobactin 1021 by Sinorhizobium meliloti and pyochelin by Pseudomonas aeruginosa, respectively. J Bacteriol 186: 2996–3005 doi:10.1128/JB.186.10.2996-3005.2004
72. LoperJE, HenkelsMD (1997) Availability of iron to Pseudomonas fluorescens in rhizosphere and bulk soil evaluated with an ice nucleation reporter gene. Appl Environ Microbiol 63: 99–105.
73. ChoudharyM, MackenzieC, NerengK, SodergrenE, WeinstockGM, et al. (1997) Low resolution sequencing of Rhodobacter sphaeroides 2.4.1T: chromosome II is a true chromosome. Microbiology 143: 3085–3099 doi:10.1099/00221287-143-10-3085
74. GuoX, FloresM, MavinguiP, FuentesSI, HernándezG, et al. (2003) Natural genomic design in Sinorhizobium meliloti: novel genomic architectures. Genome Res 13: 1810–1817 doi:10.1101/gr.1260903
75. SongJ, WareA, LiuS-L (2003) Wavelet to predict bacterial ori and ter: a tendency towards a physical balance. BMC Genomics 4: 17 doi:10.1186/1471-2164-4-17
76. CowieA, ChengJ, SibleyCD, FongY, ZaheerR, et al. (2006) An integrated approach to functional genomics: Construction of a novel reporter gene fusion library for Sinorhizobium meliloti. Appl Environ Microbiol 72: 7156–7167 doi:10.1128/AEM.01397-06
77. MeadeHM, LongSR, RuykunGB, BrownSE, AusubelFM (1982) Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis. J Bacteriol 149: 114–122.
78. YuanZC, ZaheerR, FinanTM (2006) Regulation and properties of PstSCAB, a high-affinity, high-velocity phosphate transport system of Sinorhizobium meliloti. J Bacteriol 188: 1089–1102 doi:10.1128/JB.188.3.1089-1102.2006
79. Sambrook J, Fritsch EF, Maniatis T. (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
80. FinanTM, HartweigE, LeMieuxK, BergmanK, WalkerGC, et al. (1984) General transduction in Rhizobium meliloti. J Bacteriol 159: 120–124.
81. MiuraK, KudoMY (1970) An agar-medium for aquatic hyphomycetes. Trans Mycol Soc Jpn 11: 116–118.
82. HirschPR (1979) Plasmid-determined bacteriocin production by Rhizobium leguminosarum. H Gen Microbiol 113: 219–228.
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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
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