D-Alanyl-D-alanine ligase as a broad-host-range counterselection marker in vancomycin-resistant lactic acid bacteria

Journal of Bacteriology

Volumn 200, Issue 13, 2018, Pages

  Zhang, Shenwei ^a   Oh, Jee Hwan ^a   Alexander, Laura M ^a   özçam, Mustafa ^a   van Pijkeren, Jan Peter ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Counterselection; Ddl ligase; Genome editing; Lactic acid bacteria; Lactobacillus; Lactobacillus reuteri; Peptidoglycan; Probiotics; Vancomycin resistance

Indexed keywords

CHLORAMPHENICOL; DEXTRO ALANINE DEXTRO ALANINE LIGASE; ERYTHROMYCIN; VANCOMYCIN; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; D-ALANYLALANINE SYNTHETASE; PEPTIDE SYNTHASE;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CELL; CELL GROWTH; CONTROLLED STUDY; COUNTERSELECTION MARKER; ENZYME ACTIVITY; EXPRESSION VECTOR; GENE EDITING; GENETIC MARKER; HETEROLOGOUS EXPRESSION; HOMOLOGOUS RECOMBINATION; LACTIC ACID BACTERIUM; LACTOBACILLUS; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS BREVIS; LACTOBACILLUS CASEI; LACTOBACILLUS DELBRUECKII; LACTOBACILLUS FERMENTUM; LACTOBACILLUS PLANTARUM; LACTOBACILLUS REUTERI; LACTOBACILLUS RHAMNOSUS; LACTOBACILLUS SAKEI; LACTOBACILLUS SALIVARIUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLASMID; PRIORITY JOURNAL; SUICIDE GENE; SUICIDE SUBSTRATE; VANCOMYCIN RESISTANCE; CLASSIFICATION; DRUG EFFECT; ENZYMOLOGY; GENETICS; LACTOBACILLALES; METABOLISM;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; LACTOBACILLALES; PEPTIDE SYNTHASES; PHYLOGENY; VANCOMYCIN; VANCOMYCIN RESISTANCE;

EID: 85048275789     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00607-17     Document Type: Article

References (52)

1. Tamang JP, Watanabe K, Holzapfel WH. 2016. Review: diversity of microorganisms in global fermented foods and beverages. Front Microbiol 7:377. https://doi.org/10.3389/fmicb.2016.00377
2. Klaenhammer TR, Altermann E, Pfeiler E, Buck BL, Goh YJ, O'Flaherty S, Barrangou R, Duong T. 2008. Functional genomics of probiotic Lactobacilli. J Clin Gastroenterol 42(Suppl 3 Pt 2):S160-S162. https://doi.org/ 10.1097/MCG.0b013e31817da140
3. Ljungh A, Wadström T. 2006. Lactic acid bacteria as probiotics. Curr Issues Intest Microbiol 7:73-89
4. Bron PA, Kleerebezem M. 2011. Engineering lactic acid bacteria for increased industrial functionality. Bioengineered Bugs 2:80-87. https:// doi.org/10.4161/bbug.2.2.13910
5. Gaspar P, Neves AR, Ramos A, Gasson MJ, Shearman CA, Santos H. 2004. Engineering Lactococcus lactis for production of mannitol: high yields from food-grade strains deficient in lactate dehydrogenase and the mannitol transport system. Appl Environ Microbiol 70:1466-1474. https://doi.org/10.1128/AEM.70.3.1466-1474.2004
6. Ladero V, Ramos A, Wiersma A, Goffin P, Schanck A, Kleerebezem M, Hugenholtz J, Smid EJ, Hols P. 2007. High-level production of the low-calorie sugar sorbitol by Lactobacillus plantarum through metabolic engineering. Appl Environ Microbiol 73:1864-1872. https://doi.org/10 .1128/AEM.02304-06
7. Oh JH, van Pijkeren J-P. 2014. CRISPR-Cas9-assisted recombineering in Lactobacillus reuteri. Nucleic Acids Res 42:e131. https://doi.org/10.1093/ nar/gku623
8. van Pijkeren J-P, Britton RA. 2012. High efficiency recombineering in lactic acid bacteria. Nucleic Acids Res 40:e76. https://doi.org/10.1093/ nar/gks147
9. Karlskås IL, Maudal K, Axelsson L, Rud I, Eijsink VGH, Mathiesen G. 2014. Heterologous protein secretion in Lactobacilli with modified pSIP vectors. PLoS One 9:e91125. https://doi.org/10.1371/journal.pone.0091125
10. Renye JA, Somkuti GA. 2010. Nisin-induced expression of pediocin in dairy lactic acid bacteria. J Appl Microbiol 108:2142-2151
11. de Ruyter PG, Kuipers OP, de Vos WM. 1996. Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin. Appl Environ Microbiol 62:3662-3667
12. Snyder L, Peters J, Henkin T, Champness W. 2013. Molecular genetics of bacteria, 4th ed. ASM Press, Washington, DC
13. Khetrapal V, Mehershahi K, Rafee S, Chen S, Lim CL, Chen SL. 2015. A set of powerful negative selection systems for unmodified Enterobacteriaceae. Nucleic Acids Res 43:e83. https://doi.org/10.1093/nar/gkv248
14. Sun Z, Harris HM, McCann A, Guo C, Argimon S, Zhang W, Yang X, Jeffery IB, Cooney JC, Kagawa TF, Liu W, Song Y, Salvetti E, Wrobel A, Rasinkangas P, Parkhill J, Rea MC, O'Sullivan O, Ritari J, Douillard FP, Paul Ross R, Yang R, Briner AE, Felis GE, de Vos WM, Barrangou R, Klaenhammer TR, Caufield PW, Cui Y, Zhang H, O'Toole PW. 2015. Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera. Nat Commun 6:8322. https://doi.org/10 .1038/ncomms9322
15. Xin Y, Guo T, Mu Y, Kong J. 2017. Development of a counterselectable seamless mutagenesis system in lactic acid bacteria. Microb Cell Fact 16:116. https://doi.org/10.1186/s12934-017-0731-8
16. Goh Y-J, Azcárate-Peril MA, O'Flaherty S, Durmaz E, Valence F, Jardin J, Lortal S, Klaenhammer TR. 2009. Development and application of a upp-based counterselective gene replacement system for the study of the S-layer protein SlpX of Lactobacillus acidophilus NCFM. Appl Environ Microbiol 75:3093-3105. https://doi.org/10.1128/AEM.02502-08
17. Selle K, Goh YJ, O'Flaherty S, Klaenhammer TR. 2014. Development of an integration mutagenesis system in Lactobacillus gasseri. Gut Microbes 5:326-525. https://doi.org/10.4161/gmic.29101
18. Song BF, Ju LZ, Li YJ, Tang LJ. 2014. Chromosomal insertions in the Lactobacillus casei upp gene that are useful for vaccine expression. Appl Environ Microbiol 80:3321-3326. https://doi.org/10.1128/AEM.00175-14
19. Walsh CT. 1993. Vancomycin resistance: decoding the molecular logic. Science 261:308-309. https://doi.org/10.1126/science.8392747
20. Deghorain M, Goffin P, Fontaine L, Mainardi J-L, Daniel R, Errington J, Hallet B, Hols P. 2007. Selectivity for D-lactate incorporation into the peptidoglycan precursors of Lactobacillus plantarum: role of Aad, a VanX-like D-alanyl-D-alanine dipeptidase. J Bacteriol 189:4332-4337. https://doi.org/10.1128/JB.01829-06
21. Walsh CT, Fisher SL, Park IS, Prahalad M, Wu Z. 1996. Bacterial resistance to vancomycin: five genes and one missing hydrogen bond tell the story. Chem Biol 3:21-28. https://doi.org/10.1016/S1074-5521(96)90079-4
22. Healy VL, Lessard IA, Roper DI, Knox JR, Walsh CT. 2000. Vancomycin resistance in enterococci: reprogramming of the D-ala-D-Ala ligases in bacterial peptidoglycan biosynthesis. Chem Biol 7:R109-R119. https:// doi.org/10.1016/S1074-5521(00)00116-2
23. Park IS, Walsh CT. 1997. D-Alanyl-D-lactate and D-alanyl-D-alanine synthesis by D-alanyl-D-alanine ligase from vancomycin-resistant Leuconostoc mesenteroides. Effects of a phenylalanine 261 to tyrosine mutation. J Biol Chem 272:9210-9214
24. Sørvig E, Mathiesen G, Naterstad K, Eijsink VG, Axelsson L. 2005. Highlevel, inducible gene expression in Lactobacillus sakei and Lactobacillus plantarum using versatile expression vectors. Microbiology 151: 2439-2449. https://doi.org/10.1099/mic.0.28084-0
25. Law J, Buist G, Haandrikman A, Kok J, Venema G, Leenhouts K. 1995. A system to generate chromosomal mutations in Lactococcus lactis which allows fast analysis of targeted genes. J Bacteriol 177:7011-7018. https:// doi.org/10.1128/jb.177.24.7011-7018.1995
26. Zelante T, Iannitti RG, Cunha C, De Luca A, Giovannini G, Pieraccini G, Zecchi R, D'Angelo C, Massi-Benedetti C, Fallarino F, Carvalho A, Puccetti P, Romani L. 2013. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 39:372-385. https://doi.org/10.1016/j.immuni.2013.08.003
27. Alander M, Korpela R, Saxelin M, Vilpponen-Salmela T, Mattila-Sandholm T, von Wright A. 1997. Recovery of Lactobacillus rhamnosus GG from human colonic biopsies. Lett Appl Microbiol 24:361-364. https://doi.org/ 10.1046/j.1472-765X.1997.00140.x
28. Kankainen M, Paulin L, Tynkkynen S, von Ossowski I, Reunanen J, Partanen P, Satokari R, Vesterlund S, Hendrickx APA, Lebeer S, De Keersmaecker SCJ, Vanderleyden J, Hämäläinen T, Laukkanen S, Salovuori N, Ritari J, Alatalo E, Korpela R, Mattila-Sandholm T, Lassig A, Hatakka K, Kinnunen KT, Karjalainen H, Saxelin M, Laakso K, Surakka A, Palva A, Salusjärvi T, Auvinen P, de Vos WM. 2009. Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein. Proc Natl Acad Sci U S A 106:17193-17198. https://doi .org/10.1073/pnas.0908876106
29. Lebeer S, Claes IJJ, Vanderleyden J. 2012. Anti-inflammatory potential of probiotics: lipoteichoic acid makes a difference. Trends Microbiol 20: 5-10. https://doi.org/10.1016/j.tim.2011.09.004
30. Tripathi P, Beaussart A, Alsteens D, Dupres V, Claes I, von Ossowski I, de Vos WM, Palva A, Lebeer S, Vanderleyden J, Dufrêne YF. 2013. Adhesion and nanomechanics of pili from the probiotic Lactobacillus rhamnosus GG. ACS Nano 7:3685-3697. https://doi.org/10.1021/nn400705u
31. von Schillde MA, Hormannsperger G, Weiher M, Alpert CA, Hahne H, Bauerl C, van Huynegem K, Steidler L, Hrncir T, Perez-Martinez G, Kuster B, Haller D. 2012. Lactocepin secreted by Lactobacillus exerts antiinflammatory effects by selectively degrading proinflammatory chemokines. Cell Host Microbe 11:387-396. https://doi.org/10.1016/j.chom .2012.02.006
32. Russell WM, Klaenhammer TR. 2001. Efficient system for directed integration into the Lactobacillus acidophilus and Lactobacillus gasseri chromosomes via homologous recombination. Appl Environ Microbiol 67: 4361-4364. https://doi.org/10.1128/AEM.67.9.4361-4364.2001
33. Klare I, Konstabel C, Werner G, Huys G, Vankerckhoven V, Kahlmeter G, Hildebrandt B, Muller-Bertling S, Witte W, Goossens H. 2007. Antimicrobial susceptibilities of Lactobacillus, Pediococcus and Lactococcus human isolates and cultures intended for probiotic or nutritional use. J Antimicrob Chemother 59:900-912. https://doi.org/10.1093/jac/dkm035
34. Georgieva R, Yocheva L, Tserovska L, Zhelezova G, Stefanova N, Atanasova A, Danguleva A, Ivanova G, Karapetkov N, Rumyan N, Karaivanova E. 2015. Antimicrobial activity and antibiotic susceptibility of Lactobacillus and Bifidobacterium spp. intended for use as starter and probiotic cultures. Biotechnol Biotechnol Equip 29:84-91. https://doi.org/10.1080/ 13102818.2014.987450
35. Salminen MK, Rautelin H, Tynkkynen S, Poussa T, Saxelin M, Valtonen V, Jarvinen A. 2006. Lactobacillus bacteremia, species identification, and antimicrobial susceptibility of 85 blood isolates. Clin Infect Dis 42: e35-e44. https://doi.org/10.1086/500214
36. Melkumyan AR, Priputnevich TV, Ankirskaya AS, Murav'eva VV, Lubasovskaya LA. 2015. Effects of antibiotic treatment on the Lactobacillus composition of vaginal microbiota. Bull Exp Biol Med 158:766-768. https:// doi.org/10.1007/s10517-015-2857-1
37. Elliott JA, Facklam RR. 1996. Antimicrobial susceptibilities of Lactococcus lactis and Lactococcus garvieae and a proposed method to discriminate between them. J Clin Microbiol 34:1296-1298
38. Swenson JM, Facklam RR, Thornsberry C. 1990. Antimicrobial susceptibility of vancomycin-resistant Leuconostoc, Pediococcus, and Lactobacillus species. Antimicrob Agents Chemother 34:543-549. https://doi.org/ 10.1128/AAC.34.4.543
39. Taniguchi Y, Choi PJ, Li GW, Chen H, Babu M, Hearn J, Emili A, Xie XS. 2010. Quantifying E. coli proteome and transcriptome with singlemolecule sensitivity in single cells. Science 329:533-538. https://doi.org/ 10.1126/science.1188308
40. Gygi SP, Rochon Y, Franza BR, Aebersold R. 1999. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19:1720-1730. https://doi.org/10.1128/MCB.19.3.1720
41. Duncker SC, Wang L, Hols P, Bienenstock J. 2008. The D-alanine content of lipoteichoic acid is crucial for Lactobacillus plantarum-mediated protection from visceral pain perception in a rat colorectal distension model. Neurogastroenterol Motil 20:843-850. https://doi.org/10.1111/j .1365-2982.2008.01085.x
42. Bull M, Plummer S, Marchesi J, Mahenthiralingam E. 2013. The life history of Lactobacillus acidophilus as a probiotic: a tale of revisionary taxonomy, misidentification and commercial success. FEMS Microbiol Lett 349: 77-87. https://doi.org/10.1111/1574-6968.12293
43. van Pijkeren J-P, Canchaya C, Ryan KA, Li Y, Claesson MJ, Sheil B, Steidler L, O'Mahony L, Fitzgerald GF, van Sinderen D, O'Toole PW. 2006. Comparative and functional analysis of sortase-dependent proteins in the predicted secretome of Lactobacillus salivarius UCC118. Appl Environ Microbiol 72:4143-4153. https://doi.org/10.1128/AEM.03023-05
44. Tauer C, Heinl S, Egger E, Heiss S, Grabherr R. 2014. Tuning constitutive recombinant gene expression in Lactobacillus plantarum. Microb Cell Fact 13:150. https://doi.org/10.1186/s12934-014-0150-z
45. Sambrook J, Russell DW. 2006. Transformation of E. coli by electroporation. CSH Protoc 2006:pdb.prot3933. https://doi.org/10.1101/ pdb.prot3933
46. de Kok S, Stanton LH, Slaby T, Durot M, Holmes VF, Patel KG, Platt D, Shapland EB, Serber Z, Dean J, Newman JD, Chandran SS. 2014. Rapid and reliable DNA assembly via ligase cycling reaction. ACS Synth Biol 3:97-106. https://doi.org/10.1021/sb4001992
47. Rio DC, Ares M, Jr, Hannon GJ, Nilsen TW. 2010. Purification of RNA using TRIzol (TRI reagent). Cold Spring Harb Protoc 2010:pdb.prot5439. https:// doi.org/10.1101/pdb.prot5439
48. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45. https://doi.org/10.1093/nar/ 29.9.e45
49. Kozera B, Rapacz M. 2013. Reference genes in real-time PCR. J Appl Genet 54:391-406. https://doi.org/10.1007/s13353-013-0173-x
50. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59. https://doi.org/10.1016/0378-1119(89)90358-2
51. Gibson DG, Young L, Chuang R-Y, Venter JC, Hutchison CA, Smith HO. 2009. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nature methods 6:343-345. https://doi.org/10.1038/nmeth .1318
52. Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33: 1870-1874. https://doi.org/10.1093/molbev/msw054