Microbial domestication signatures of Lactococcus lactis can be reproduced by experimental evolution

Genome Research

Volumn 22, Issue 1, 2012, Pages 115-124

  Bachmann, Herwig ^a,b,c   Starrenburg, Marjo J C ^a,b   Molenaar, Douwe ^a,b,c   Kleerebezem, Michiel ^a,b,d   Van Hylckama Vlieg, Johan E T ^a,b,e  

^a NIZO FOOD RESEARCH   (Netherlands)

^b KLUYVER CENTRE FOR GENOMICS OF INDUSTRIAL FERMENTATION   (Netherlands)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

^d WAGENINGEN UNIVERSITY   (Netherlands)

^e DANONE RESEARCH   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN MUTL;

AMINO ACID SYNTHESIS; AMINO ACID TRANSPORT; ARTICLE; BACTERIAL GROWTH; BACTERIAL REPRODUCTION; BACTERIAL STRAIN; BACTERIUM COLONY; BACTERIUM ISOLATION; CONTROLLED STUDY; DOMESTICATION; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; LACTOCOCCUS LACTIS; MICROBIAL DOMESTICATION; MILK; MISMATCH REPAIR; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TRANSPOSON;

DAIRY PRODUCTS; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC LOCI; GENOME, BACTERIAL; LACTOCOCCUS LACTIS; POINT MUTATION; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); LACTOCOCCUS LACTIS;

EID: 84855320124     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.121285.111     Document Type: Article

References (56)

1. Bachmann H, de Wilt L, Kleerebezem M, van Hylckama Vlieg JE. 2010. Time-resolved genetic responses of Lactococcus lactis to a dairy environment. Environ Microbiol 12: 1260-1270.
2. Bachmann H, Molenaar D, Kleerebezem M, van Hylckama Vlieg JE. 2011. High local substrate availability stabilizes a cooperative trait. ISME J 5: 929-932.
3. Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, Schneider D, Lenski RE, Kim JF. 2009. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461: 1243-1247.
4. Bartkus JM, Tyler B, Calvo JM. 1991. Transcription attenuation-mediated control of leu operon expression: Influence of the number of Leu control codons. J Bacteriol 173: 1634-1641.
5. Beaumont HJ, Gallie J, Kost C, Ferguson GC, Rainey PB. 2009. Experimental evolution of bet hedging. Nature 462: 90-93.
6. Bolotin A, Wincker P, Mauger S, Jaillon O, Malarme K, Weissenbach J, Ehrlich SD, Sorokin A. 2001. The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res 11: 731-753. (Pubitemid 32447860)
7. Bolotin A, Quinquis B, Renault P, Sorokin A, Ehrlich SD, Kulakauskas S, Lapidus A, Goltsman E, Mazur M, Pusch GD, et al. 2004. Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat Biotechnol 22: 1554-1558. (Pubitemid 40039458)
8. Buckling A, Craig Maclean R, Brockhurst MA, Colegrave N. 2009. The Beagle in a bottle. Nature 457: 824-829.
9. Campbell-Platt G. 1994. Fermented foods - a world perspective. Food Res Int 27: 253-257.
10. Chopin A, Chopin MC, Moillo-Batt A, Langella P. 1984. Two plasmid-determined restriction and modification systems in Streptococcus lactis. Plasmid 11: 260-263. (Pubitemid 14052047)
11. Conrad TM, Joyce AR, Applebee MK, Barrett CL, Xie B, Gao Y, Palsson BO. 2009. Whole-genome resequencing of Escherichia coli K-12 MG1655 undergoing short-term laboratory evolution in lactate minimal media reveals flexible selection of adaptive mutations. Genome Biol 10: R118. doi: 10.1186/gb-2009-10- 10-r118.
12. Dahlberg C, Chao L. 2003. Amelioration of the cost of conjugative plasmid carriage in Eschericha coli K12. Genetics 165: 1641-1649. (Pubitemid 38040259)
13. Delorme C, Godon JJ, Ehrlich SD, Renault P. 1993. Gene inactivation in Lactococcus lactis: Histidine biosynthesis. J Bacteriol 175: 4391-4399. (Pubitemid 23206940)
14. de Visser JA, Lenski RE. 2002. Long-term experimental evolution in Escherichia coli. XI. Rejection of non-transitive interactions as cause of declining rate of adaptation. BMC Evol Biol 2: 19. doi: 10.1186/1471-2148-2-19.
15. de Vos WM, Vos P, de Haard H, Boerrigter I. 1989. Cloning and expression of the Lactococcus lactis subsp. cremoris SK11 gene encoding an extracellular serine proteinase. Gene 85: 169-176. (Pubitemid 20054340)
16. Gitton C, Meyrand M, Wang J, Caron C, Trubuil A, Guillot A, Mistou MY. 2005. Proteomic signature of Lactococcus lactis NCDO763 cultivated in milk. Appl Environ Microbiol 71: 7152-7163. (Pubitemid 43194208)
17. Godon JJ, Chopin MC, Ehrlich SD. 1992. Branched-chain amino acid biosynthesis genes in Lactococcus lactis subsp. lactis. J Bacteriol 174: 6580-6589.
18. Godon JJ, Delorme C, Bardowski J, Chopin MC, Ehrlich SD, Renault P. 1993. Gene inactivation in Lactococcus lactis: Branched-chain amino acid biosynthesis. J Bacteriol 175: 4383-4390. (Pubitemid 23206939)
19. Gore J, Youk H, van Oudenaarden A. 2009. Snowdrift game dynamics and facultative cheating in yeast. Nature 459: 253-256.
20. Guedon E, Sperandio B, Pons N, Ehrlich SD, Renault P. 2005. Overall control of nitrogen metabolism in Lactococcus lactis by CodY, and possible models for CodY regulation in Firmicutes. Microbiology 151: 3895-3909. (Pubitemid 41829970)
21. Hall BM, Ma CX, Liang P, Singh KK. 2009. Fluctuation analysis CalculatOR: a web tool for the determination of mutation rate using Luria-Delbruck fluctuation analysis. Bioinformatics 25: 1564-1565.
22. Hegreness M, Shoresh N, Hartl D, Kishony R. 2006. An equivalence principle for the incorporation of favorable mutations in asexual populations. Science 311: 1615-1617.
23. Herring CD, Raghunathan A, Honisch C, Patel T, Applebee MK, Joyce AR, Albert TJ, Blattner FR, van den Boom D, Cantor CR, et al. 2006. Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nat Genet 38: 1406-1412. (Pubitemid 44837562)
24. Hugenholtz J, Splint R, Konings WN, Veldkamp H. 1987. Selection of protease-positive and protease-negative variants of Streptococcus cremoris. Appl Environ Microbiol 53: 309-314. (Pubitemid 17004613)
25. Juillard V, Le Bars D, Kunji ER, Konings WN, Gripon JC, Richard J. 1995. Oligopeptides are the main source of nitrogen for Lactococcus lactis during growth in milk. Appl Environ Microbiol 61: 3024-3030.
26. Kelly WJ, Davey GP, Ward LJ. 1998. Characterization of lactococci isolated from minimally processed fresh fruit and vegetables. Int J Food Microbiol 45: 85-92. (Pubitemid 29049100)
27. Kelly WJ, Davey GP, Ward LJ. 2000. Novel sucrose transposons from plant strains of Lactococcus lactis. FEMS Microbiol Lett 190: 237-240.
28. Kelly WJ, Ward LJ, Leahy SC. 2010. Chromosomal diversity in Lactococcus lactis and the origin of dairy starter cultures. Genome Biol Evol 2: 729-744.
29. Kunji ER, Hagting A, De Vries CJ, Juillard V, Haandrikman AJ, Poolman B, Konings WN. 1995. Transport of b-casein-derived peptides by the oligopeptide transport system is a crucial step in the proteolytic pathway of Lactococcus lactis. J Biol Chem 270: 1569-1574.
30. Kunji ER, Mierau I, Hagting A, Poolman B, Konings WN. 1996. The proteolytic systems of lactic acid bacteria. Antonie van Leeuwenhoek 70: 187-221. (Pubitemid 26355500)
31. 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.
32. Luria SE, Delbruck M. 1943. Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28: 491-511.
33. Machielsen R, Siezen RJ, van Hijum SA, van Hylckama Vlieg JE. 2011. Molecular description and industrial potential of Tn6098 conjugative transfer conferring a-galactoside metabolism in Lactococcus lactis. Appl Environ Microbiol 77: 555-563.
34. Makarova KS, Koonin EV. 2007. Evolutionary genomics of lactic acid bacteria. J Bacteriol 189: 1199-1208. (Pubitemid 46239741)
35. Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E, Pavlov A, Pavlova N, Karamychev V, Polouchine N, et al. 2006. Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci 103: 15611-15616. (Pubitemid 44625640)
36. McKay LL, Baldwin KA. 1974. Simultaneous loss of proteinase- and lactose-utilizing enzyme activities in Streptococcus lactis and reversal of loss by transduction. Appl Microbiol 28: 342-346.
37. Miller JH. 1996. Spontaneous mutators in bacteria: Insights into pathways of mutagenesis and repair. Annu Rev Microbiol 50: 625-643. (Pubitemid 26337476)
38. Passerini D, Beltramo C, Coddeville M, Quentin Y, Ritzenthaler P, Daveran-Mingot ML, Le Bourgeois P. 2010. Genes but not genomes reveal bacterial domestication of Lactococcus lactis. PLoS ONE 5: e15306. doi: 10.1371/journal.pone.0015306.
39. Peyret N, Seneviratne PA, Allawi HT, SantaLucia J Jr. 1999. Nearest-neighbor thermodynamics and NMR of DNA sequences with internal A·A, C·C, G·G, and T·T mismatches. Biochemistry 38: 3468-3477.
40. Rademaker JL, Herbet H, Starrenburg MJ, Naser SM, Gevers D, Kelly WJ, Hugenholtz J, Swings J, van Hylckama Vlieg JE. 2007. Diversity analysis of dairy and nondairy Lactococcus lactis isolates, using a novel multilocus sequence analysis scheme and (GTG)5-PCR fingerprinting. Appl Environ Microbiol 73: 7128-7137. (Pubitemid 350196659)
41. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: A laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
42. Sanders JW, Leenhouts K, Burghoorn J, Brands JR, Venema G, Kok J. 1998. A chloride-inducible acid resistance mechanism in Lactococcus lactis and its regulation. Mol Microbiol 27: 299-310. (Pubitemid 28035255)
43. Shaver AC, Sniegowski PD. 2003. Spontaneously arising mutL mutators in evolving Escherichia coli populations are the result of changes in repeat length. J Bacteriol 185: 6076-6082. (Pubitemid 37248460)
44. Shaver AC, Dombrowski PG, Sweeney JY, Treis T, Zappala RM, Sniegowski PD. 2002. Fitness evolution and the rise of mutator alleles in experimental Escherichia coli populations. Genetics 162: 557-566. (Pubitemid 35365023)
45. Sieuwerts S, Molenaar D, van Hijum SA, Beerthuyzen M, Stevens MJ, Janssen PW, Ingham CJ, de Bok FA, de Vos WM, van Hylckama Vlieg JE. 2010. Mixed-culture transcriptome analysis reveals the molecular basis of mixed-culture growth in Streptococcus thermophilus and Lactobacillus bulgaricus. Appl Environ Microbiol 76: 7775-7784.
46. Siezen RJ, Renckens B, van Swam I, Peters S, van Kranenburg R, Kleerebezem M, de Vos WM. 2005. Complete sequences of four plasmids of Lactococcus lactis subsp. cremoris SK11 reveal extensive adaptation to the dairy environment. Appl Environ Microbiol 71: 8371-8382. (Pubitemid 41803965)
47. Siezen RJ, Starrenburg MJ, Boekhorst J, Renckens B, Molenaar D, van Hylckama Vlieg JE. 2008. Genome-scale genotype-phenotype matching of two Lactococcus lactis isolates from plants identifies mechanisms of adaptation to the plant niche. Appl Environ Microbiol 74: 424-436.
48. Siezen RJ, Bayjanov J, Renckens B, Wels M, van Hijum SA, Molenaar D, van Hylckama Vlieg JE. 2010. Complete genome sequence of Lactococcus lactis subsp. lactis KF147, a plant-associated lactic acid bacterium. J Bacteriol 192: 2649-2650.
49. Smyth GK, Yang YH, Speed T. 2003. Statistical issues in cDNA microarray data analysis. Methods Mol Biol 224: 111-136.
50. Sniegowski PD, Gerrish PJ, Lenski RE. 1997. Evolution of high mutation rates in experimental populations of E. coli. Nature 387: 703-705.
51. Sorensen KI, Hove-Jensen B. 1996. Ribose catabolism of Escherichia coli: Characterization of the rpiB gene encoding ribose phosphate isomerase B and of the rpiR gene, which is involved in regulation of rpiB expression. J Bacteriol 178: 1003-1011. (Pubitemid 26048015)
52. Taddei F, Radman M, Maynard-Smith J, Toupance B, Gouyon PH, Godelle B. 1997. Role of mutator alleles in adaptive evolution. Nature 387: 700-702.
53. van de Guchte M, Penaud S, Grimaldi C, Barbe V, Bryson K, Nicolas P, Robert C, Oztas S, Mangenot S, Couloux A, et al. 2006. The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution. Proc Natl Acad Sci 103: 9274-9279. (Pubitemid 43902568)
54. van Hylckama Vlieg JE, Rademaker JL, Bachmann H, Molenaar D, Kelly WJ, Siezen RJ. 2006. Natural diversity and adaptive responses of Lactococcus lactis. Curr Opin Biotechnol 17: 183-190.
55. Wegmann U, O'Connell-Motherway M, Zomer A, Buist G, Shearman C, Canchaya C, Ventura M, Goesmann A, Gasson MJ, Kuipers OP, et al. 2007. Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis subsp. cremoris MG1363. J Bacteriol 189: 3256-3270. (Pubitemid 46697416)
56. Wells JM, Wilson PW, Le Page RW. 1993. Improved cloning vectors and transformation procedure for Lactococcus lactis. J Appl Bacteriol 74: 629-636. (Pubitemid 23186563)