Non-additive costs and interactions alter the competitive dynamics of co-occurring ecologically distinct plasmids

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1779, 2014, Pages

  Morton, Elise R ^a   Platt, Thomas G ^a   Fuqua, Clay ^a   Bever, James D ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Adaptation; Coevolution; Competition; Epistasis; Facultative pathogen; Plasmid

Indexed keywords

BACTERIUM; COEVOLUTION; COEXISTENCE; COMPETITIVE ABILITY; EPISTASIS; FACULTATIVE BEHAVIOR; NATURAL SELECTION; PLASMID; VIRULENCE;

ADAPTATION; AGROBACTERIUM TUMEFACIENS; ARTICLE; BIOLOGICAL MODEL; COEVOLUTION; COMPETITION; EPISTASIS; EVOLUTION; FACULTATIVE PATHOGEN; GENETICS; GENOTYPE; MICROBIOLOGY; PATHOGENICITY; PLASMID; SUNFLOWER; VIRULENCE;

ADAPTATION; COEVOLUTION; COMPETITION; EPISTASIS; FACULTATIVE PATHOGEN; PLASMID;

ADAPTATION, BIOLOGICAL; AGROBACTERIUM TUMEFACIENS; BIOLOGICAL EVOLUTION; GENETICS; GENOTYPE; HELIANTHUS; MICROBIOLOGY; MODELS, GENETIC; PATHOGENICITY; PLANT TUMOR-INDUCING PLASMIDS; VIRULENCE;

EID: 84902668698     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.2173     Document Type: Article

References (57)

1. Cooper TF, Lenski RE. 2010 Experimental evolution with E. coli in diverse resource environments. I. Fluctuating environments promote divergence of replicate populations. BMC Evol. Biol. 10, 11. (doi:10.1186/1471-2148-10-11)
2. Rozen DE, Habets M, Handel A, de Visser J. 2008 Heterogeneous adaptive trajectories of small populations on complex fitness landscapes. PLoS ONE 3, e1715. (doi:10.1371/journal.pone.0001715)
3. Jasmin JN, Kassen R. 2007 On the experimental evolution of specialization and diversity in heterogeneous environments. Ecol. Lett. 10, 272-281. (doi:10.1111/j.1461-0248.2007.01021.x)
4. Hiller NL et al. 2010 Generation of genic diversity among Streptococcus pneumoniae strains via horizontal gene transfer during a chronic polyclonal pediatric infection. PLoS Pathog. 6, e1001108. (doi:10.1371/journal.ppat.1001108)
5. Heuer H, Smalla K. 2012 Plasmids foster diversification and adaptation of bacterial populations in soil. FEMS Microbiol. Rev. 36, 1083-1104. (doi:10.1111/j.1574-6976.2012.00337.x)
6. Lopez-Guerrero MG et al. 2012 Rhizobial extrachromosomal replicon variability, stability and expression in natural niches. Plasmid 68, 149-158. (doi:10.1016/j.plasmid.2012.07.002)
7. Lamb JW, Hombrecher G, Johnston AWB. 1982 Plasmid-determined nodulation and nitrogenfixation abilities in Rhizobium phaseoli. Mol. Gen. Genet. 186, 449-452. (doi:10.1007/bf00729468)
8. Watson B, Currier TC, Gordon MP, Chilton MD, Nester EW. 1975 Plasmid required for virulence of Agrobacterium tumefaciens. J. Bacteriol. 123, 255-264.
9. Parter M, Kashtan N, Alon U. 2007 Environmental variability and modularity of bacterial metabolic networks. BMC Evol. Biol. 7, 169. (doi:10.1186/ 1471-2148-7-169)
10. Toussaint A, Merlin C. 2002 Mobile elements as a combination of functional modules. Plasmid 47, 26-35. (doi:10.1006/plas.2001.1552)
11. Simonsen L. 1991 The existence conditions for bacterial plasmids: theory and reality. Microb. Ecol. 22, 187-205. (doi:10.1007/BF02540223)
12. Bergstrom CT, Lipsitch M, Levin BR. 2000 Natural selection, infectious transfer and the existence conditions for bacterial plasmids. Genetics 155, 1505-1519.
13. Harrison E, Brockhurst MA. 2012 Plasmid-mediated horizontal gene transfer is a coevolutionary process. Trends Microbiol. 20, 262-267. (doi:10.1016/j.tim.2012.04.003)
14. Eberhard WG. 1990 Evolution in bacterial plasmids and levels of selection. Q. Rev. Biol. 65, 3-22. (doi:10.1086/416582)
15. Rigottier-Gois L, Turner SL, Young JPW, Amarger N. 1998 Distribution of repC plasmid-replication sequences among plasmids and isolates of Rhizobium leguminosarum bv. viciae from field populations. Microbiology UK 144, 771-780. (doi:10.1099/00221287-144-3-771)
16. Platt TG, Bever JD, Fuqua C. 2012 A cooperative virulence plasmid imposes a high fitness cost under conditions that induce pathogenesis. Proc. R. Soc. B 279, 1691-1699. (doi:10.1098/rspb.2011.2002)
17. Lilley AK, Young JP, Bailey MJ. 2000 Bacterial population genetics: do plasmids maintain diversity and adaptation? In Horizontal gene pool: bacterial plasmids and gene spread (ed. CM Thomas), pp. 287-300. Amsterdam, The Netherlands: Hardwood Academic Publishers.
18. Slater SC 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)
19. Elena SF, Lenski RE. 2001 Epistasis between new mutations and genetic background and a test of genetic canalization. Evolution 55, 1746-1752. (doi:10.1111/j.0014-3820.2001.tb00824.x)
20. Sanjuan R, Elena SF. 2006 Epistasis correlates to genomic complexity. Proc. Natl Acad. Sci. USA 103, 14 402-14 405. (doi:10.1073/pnas.0604543103)
21. Novick RP. 1987 Plasmid incompatibility. Microbiol. Rev. 51, 381-395.
22. Cooper TF, Heinemann JA. 2005 Selection for plasmid post-segregational killing depends on multiple infection: evidence for the selection of more virulent parasites through parasite-level competition. Proc. R. Soc. B 272, 403-410. (doi:10.1098/rspb.2004.2921)
23. Chen LS, Chen YC, Wood DW, Nester EW. 2002 A new type IV secretion system promotes conjugal transfer in Agrobacterium tumefaciens. J Bacteriol. 184, 4838-4845. (doi:10.1128/JB.184.17.4838-4845.2002)
24. Paulsson J. 2002 Multileveled selection on plasmid replication. Genetics 161, 1373-1384.
25. Lenski RE, Riley MA. 2002 Chemical warfare from an ecological perspective. Proc. Natl Acad. Sci. USA 99, 556-558. (doi:10.1073/pnas.022641999)
26. Gorecki RK, Koryszewska-Baginska A, Golebiewski M, Zylinska J, Grynberg M, Bardowski JK. 2011 Adaptative potential of the Lactococcus lactis IL594 strain encoded in its 7 plasmids. PLoS ONE 6, e22238. (doi:10.1371/journal.pone.0022238)
27. San Millan A, Heilbron K, MacLean RC. 2013 Positive epistasis between co-infecting plasmids promotes plasmid survival in bacterial populations. ISME J. (doi:10.1038/ismej.2013.182)
28. Dahlberg C, Chao L. 2003 Amelioration of the cost of conjugative plasmid carriage in Eschericha coli K12. Genetics 165, 1641-1649.
29. Dionisio F, Conceicao IC, Marques ACR, Fernandes L, Gordo I. 2005 The evolution of a conjugative plasmid and its ability to increase bacterial fitness. Biol. Lett. 1, 250-252. (doi:10.1098/rsbl.2004.0275)
30. Smith J. 2011 Superinfection drives virulence evolution in experimental populations of bacteria and plasmids. Evolution 65, 831-841. (doi:10. 1111/j.1558-5646.2010.01178.x)
31. Ramisse V, Patra G, Garrigue H, Guesdon JL, Mock M. 1996 Identification and characterization of Bacillus anthracis by multiplex PCR analysis of sequences on plasmids pXO1 and pXO2 and chromosomal DNA. FEMS Microbiol. Lett. 145, 9-16. (doi:10.1111/j. 1574-6968.1996.tb08548.x)
32. Moenneloccoz Y, Weaver RW. 1995 Plasmids and saprophytic growth of Rhizobium leguminosarum bv trifolii W14-2 in soil. FEMS Microbiol. Ecol. 18, 139-144. (doi:10.1111/j.1574-6941.1995.tb00171.x)
33. de Visser J, Cooper TF, Elena SF. 2011 The causes of epistasis. Proc. R. Soc. B 278, 3617-3624. (doi:10. 1098/rspb.2011.1537)
34. Winans SC. 1990 Transcriptional induction of an Agrobacterium regulatory gene at tandem promoters by plant released phenolic compounds, phosphate starvation, and acidic growth media. J. Bacteriol. 172, 2433-2438.
35. Fullner KJ, Lara JC, Nester EW. 1996 Pilus assembly by Agrobacterium T-DNA transfer genes. Science 273, 1107-1109. (doi:10.1126/science.273.5278.1107)
36. Dessaux Y, Petit A, Farrand SK, Murphy PJ. 1998 Opines and opine-like molecules involved in plant-Rhizobiaceae interactions. In The Rhizobiaceae: molecular biology of model plant-associated bacteria (eds HP Spaink, A Kondorosi, PJJ Hooykaas), pp. 173-197. Dordrecht, The Netherlands: Kluwer Academic Publishers.
37. Fuqua WC, Winans SC. 1994 A LuxR-LuxI type regulatory system activates Agrobacterium Ti plasmid conjugal transfer in the presence of a plant tumor metabolite. J. Bacteriol. 176, 2796-2806.
38. Zhang HB, Wang C, Zhang LH. 2004 The quormone degradation system of Agrobacterium tumefaciens is regulated by starvation signal and stress alarmone (p)ppGpp. Mol. Microbiol. 52, 1389-1401. (doi:10. 1111/j.1365-2958.2004.04061.x)
39. Baek C-H, Farrand SK, Park DK, Lee KE, Hwang W, Kim KS. 2005 Genes for utilization of deoxyfructosyl glutamine (DFG), an amadori compound, are widely dispersed in the family Rhizobiaceae. FEMS Microbiol. Ecol. 53, 221-233. (doi:10.1016/j. femsec.2004.12.008)
40. Perez-Mendoza D et al. 2005 Identification of the rctA gene, which is required for repression of conjugative transfer of rhizobial symbiotic megaplasmids. J. Bacteriol. 187, 7341-7350. (doi:10.1128/jb.187.21.7341-7350.2005)
41. Morton ER, Fuqua C. 2012 Genetic manipulation of Agrobacterium. Curr. Protoc. Microbiol. Ch. 3, pp. 1-16, Unit3D.2. (doi:10.1002/9780471729259. mc03d02s25)
42. Tempe J, Petit A, Holsters M, Montagu MV, Schell J. 1977 Thermosensitive step associated with transfer of Ti plasmid during conjugation: possible relation to transformation in crown gall. Proc. Natl Acad. Sci. USA 74, 2848-2849. (doi:10.1073/pnas.74.7.2848)
43. Morton ER, Fuqua C. 2012 Phenotypic analyses of agrobacterium. Curr. Protoc. Microbiol. Ch. 3, pp. 1-15, Unit3D.3. (doi:10.1002/9780471729259. mc03d03s25)
44. Uraji M, Suzuki K, Yoshida K. 2002 A novel plasmid curing method using incompatibility of plant pathogenic Ti plasmids in Agrobacterium tumefaciens. Genes Genet. Syst. 77, 1-9. (doi:10. 1266/ggs.77.1)
45. Lenski RE, Rose MR, Simpson SC, Tadler SC. 1991 Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2, 000 generations. Am. Nat. 138, 1315-1341. (doi:10. 1086/285289)
46. Morton ER, Fuqua C. 2012 Laboratory maintenance of Agrobacterium. Curr. Protoc. Microbiol. Ch. 1, Unit3D.1. 24, 3D.1.1-3D.1.16. (doi:10.1002/9780471729259.mc03d01s24)
47. Winans SC, Kerstetter RA, Nester EW. 1988 Transcriptional regulation of the virA gene and virG gene of Agrobacterium tumefaciens. J. Bacteriol. 170, 4047-4054.
48. Nair GR, Liu ZY, Binns AN. 2003 Reexamining the role of the accessory plasmid pAtC58 in the virulence of Agrobacterium tumefaciens strain C58. Plant Physiol. 133, 989-999. (doi:10.1104/pp.103.030262)
49. Franklin RB, Mills AL. 2009 Importance of spatially structured environmental heterogeneity in controlling microbial community composition at small spatial scales in an agricultural field. Soil Biol. Biochem. 41, 1833-1840. (doi:10.1016/j.soilbio.2009.06.003)
50. Venail PA, Kaltz O, Olivieri I, Pommier T, Mouquet N. 2011 Diversification in temporally heterogeneous environments: effect of the grain in experimental bacterial populations. J. Evol. Biol. 24, 2485-2495. (doi:10.1111/j.1420-9101.2011.02376.x)
51. Modi RI, Adams J. 1991 Coevolution in bacterial plasmid populations. Evolution 45, 656-667. (doi:10.2307/2409918)
52. Poole TL, Callaway TR, Bischoff KM, Loneragan GH, Anderson RC, Nisbet DJ. 2012 Competitive effect of commensal faecal bacteria from growing swine fed chlortetracycline-supplemented feed on bhaemolytic Escherichia coli strains with multiple antimicrobial resistance plasmids. J. Appl. Microbiol. 113, 659-668. (doi:10.1111/j.1365-2672.2012.05365.x)
53. Krimi Z, Petit A, Mougel C, Dessaux Y, Nesme X. 2002 Seasonal fluctuations and long-term persistence of pathogenic populations of Agrobacterium spp. in soils. Appl. Environ. Microbiol. 68, 3358-3365. (doi:10.1128/AEM.68.7.3358-3365. 2002)
54. Ding H, Hynes MF. 2009 Plasmid transfer systems in the rhizobia. Can. J. Microbiol. 55, 917-927. (doi:10.1139/w09-056)
55. Turner PE, Cooper VS, Lenski RE. 1998 Tradeoff between horizontal and vertical modes of transmission in bacterial plasmids. Evolution 52, 315-329. (doi:10.2307/2411070)
56. Haft RJF, Mittler JE, Traxler B. 2009 Competition favours reduced cost of plasmids to host bacteria. ISME J. 3, 761-769. (doi:10.1038/ismej.2009.22)
57. Lang J, Planamente S, Mondy S, Dessaux Y, Moréra S, Faure D. 2013 Concerted transfer of the virulence Ti plasmid and companion At plasmid in the Agrobacterium tumefaciens-induced plant tumour. Mol. Microbiol. 90, 1178-1189. (doi:10.1111/mmi.12423)