Functional specificity of extracellular nucleases of Shewanella oneidensis MR-1

Applied and Environmental Microbiology

Volumn 78, Issue 12, 2012, Pages 4400-4411

  Heun, Magnus ^a   Binnenkade, Lucas ^a   Kreienbaum, Maximilian ^a   Thormann, Kai M ^a  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL SPECIES; BIOFILM FORMATION; CELL AGGREGATES; DIVALENT METAL ION; EXTRACELLULAR; FUNCTIONAL SPECIFICITY; PURIFIED PROTEIN; SHEWANELLA; SHEWANELLA ONEIDENSIS MR-1; STRUCTURAL MATRIX; SUPERCOILED DNA;

BACTERIA; BIOFILMS; DEGRADATION; MANGANESE; MANGANESE COMPOUNDS; NUCLEIC ACIDS; PHOSPHORUS;

NUTRIENTS;

DEOXYRIBONUCLEASE; DIVALENT CATION; DNA; MAGNESIUM; MANGANESE; PHOSPHORUS;

BACTERIUM; BIOFILM; ENZYME ACTIVITY; MITOCHONDRIAL DNA; PHOSPHATASE; PHOSPHORUS; PROTEIN;

ARTICLE; CHEMISTRY; COENZYME; ENZYME SPECIFICITY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; METABOLISM; SECRETION; SHEWANELLA;

CATIONS, DIVALENT; COENZYMES; DEOXYRIBONUCLEASES; DNA; GENE EXPRESSION REGULATION, BACTERIAL; MAGNESIUM; MANGANESE; PHOSPHORUS; SHEWANELLA; SUBSTRATE SPECIFICITY; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); SHEWANELLA; SHEWANELLA ONEIDENSIS; SHEWANELLA ONEIDENSIS MR-1;

EID: 84864094508     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.07895-11     Document Type: Article

References (64)

1. Aiba H, Adhya S, de Crombrugghe B. 1981. Evidence for two functional gal promoters in intact Escherichia coli cells. J. Biol. Chem. 256:11905-11910.
2. Altermark B, Smalas AO, Willassen NP, Helland R. 2006. The structure of Vibrio cholerae extracellular endonuclease I reveals the presence of a buried chloride ion. Acta Crystallogr. D Biol. Crystallogr. 62:1387-1391.
3. Baldwin DS. 1998. Reactive "organic" phosphorus revisited. Water Res. 32:2265-2270.
4. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
5. Berne C, Kysela DT, Brun YV. 2010. A bacterial extracellular DNA inhibits settling of motile progeny cells within a biofilm. Mol. Microbiol. 77:815-829.
6. Bjerrum CJ, Canfield DE. 2002. Ocean productivity before about 1.9 Gyr ago limited by phosphorus adsorption onto iron oxides. Nature 417:159-162.
7. Blokesch M, Schoolnik GK. 2008. The extracellular nuclease Dns and its role in natural transformation of Vibrio cholerae. J. Bacteriol. 190:7232-7240.
8. Bretschger O, et al. 2007. Current production and metal oxide reduction by Shewanella oneidensis MR-1 wild type and mutants. Appl. Environ. Microbiol. 73:7003-7012.
9. Brown RN, Romine MF, Schepmoes AA, Smith RD, Lipton MS. 2010. Mapping the subcellular proteome of Shewanella oneidensis MR-1 using Sarkosyl-based fractionation and LC-MS/MS protein identification. J. Proteome Res. 9:4454-4463.
10. Chang MC, Chang SY, Chen SL, Chuang SM. 1992. Cloning and expression in Escherichia coli of the gene encoding an extracellular deoxyribonuclease (DNase) from Aeromonas hydrophila. Gene 122:175-180.
11. Choi KH, et al. 2005. A Tn7-based broad-range bacterial cloning and expression system. Nat. Methods 2:443-448.
12. Das T, Sharma PK, Busscher HJ, van der Mei HC, Krom BP. 2010. Role of extracellular DNA in initial bacterial adhesion and surface aggregation. Appl. Environ. Microbiol. 76:3405-3408.
13. Das T, Sharma PK, Krom BP, van der Mei HC, Busscher HJ. 2011. Role of eDNA on the adhesion forces between Streptococcus mutans and substratum surfaces: influence of ionic strength and substratum hydrophobicity. Langmuir 27:10113-10118.
14. Dell'Anno A, Corinaldesi C. 2004. Degradation and turnover of extracellularDNAin marine sediments: ecological and methodological considerations. Appl. Environ. Microbiol. 70:4384-4386.
15. Dell'Anno A, Danovaro R. 2005. Extracellular DNA plays a key role in deep-sea ecosystem functioning. Science 309:2179.
16. Dell'Anno A, Fabiano M, Duineveld GCA, Kok A, Danovaro R. 1998. Nucleic acid (DNA, RNA) quantification and RNA/DNA ratio determination in marine sediments: comparison of spectrophotometric, fluorometric, and high-performance liquid chromatography methods and estimation of detrital DNA. Appl. Environ. Microbiol. 64:3238-3245.
17. Dell'Anno A, Fabiano M, Mei ML, Danovaro R. 1999. Pelagic-benthic coupling of nucleic acids in an abyssal location of the northeastern Atlantic Ocean. Appl. Environ. Microbiol. 65:4451-4457.
18. Dominiak DM, Nielsen JL, Nielsen PH. 2011. Extracellular DNA is abundant and important for microcolony strength in mixed microbial biofilms. Environ. Microbiol. 13:710-721.
19. Flemming HC, Wingender J. 2010. The biofilm matrix. Nat. Rev. Microbiol. 8:623-633.
20. Focareta T, Manning PA. 1987. Extracellular proteins of Vibrio cholerae: molecular cloning, nucleotide sequence and characterization of the deoxyribonuclease (DNase) together with its periplasmic localization in Escherichia coli K-12. Gene 53:31-40.
21. Fredrickson JK, et al. 2008. Towards environmental systems biology of Shewanella. Nat. Rev. Microbiol. 6:592-603.
22. Gödeke J, Heun M, Bubendorfer S, Paul K, Thormann KM. 2011. Roles of two Shewanella oneidensis MR-1 extracellular endonucleases. Appl. Environ. Microbiol. 77:5342-5351.
23. Gödeke J, Paul K, Lassak J, Thormann KM. 2011. Phage-induced lysis enhances biofilm formation in Shewanella oneidensis MR-1. ISME J. 5:613-626.
24. Gorby Y, et al. 2008. Redox-reactive membrane vesicles produced by Shewanella. Geobiology 6:232-241.
25. Harmsen M, Lappann M, Knochel S, Molin S. 2010. The role of extracellular DNA during biofilm formation by Listeria monocytogenes. Appl. Environ. Microbiol. 76:2271-2279.
26. Hau HH, Gralnick JA. 2007. Ecology and biotechnology of the genus Shewanella. Annu. Rev. Microbiol. 61:237-258.
27. Heidelberg JF, et al. 2002. Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat. Biotechnol. 20:1118-1123.
28. Hilpert K, Hancock RE. 2007. Use of luminescent bacteria for rapid screening and characterization of short cationic antimicrobial peptides synthesized on cellulose using peptide array technology. Nat. Protoc. 2:1652-1660.
29. Höfle MG, Brettar I. 1996. Genotyping of heterotrophic bacteria from the Central Baltic Sea by use of low-molecular-weight RNA profiles. Appl. Environ. Microbiol. 62:1383-1390.
30. Hudson JJ, Taylor WD, Schindler DW. 2000. Phosphate concentrations in lakes. Nature 406:54-56.
31. Inoue H, Nojima H, Okayama H. 1990. High efficiency transformation of Escherichia coli with plasmids. Gene 96:23-28.
32. Jekel M, Wackernagel W. 1995. The periplasmic endonuclease I of Escherichia coli has amino-acid sequence homology to the extracellular DNases of Vibrio cholerae and Aeromonas hydrophila. Gene 154:55-59.
33. Karl DM, Yanagi K. 1997. Partial characterization of the dissolved organic phosphorus pool in the oligotrophic North Pacific Ocean. Limnol. Oceanogr. 42:1398-1405.
34. Kovach ME, et al. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
35. Lassak J, Henche AL, Binnenkade L, Thormann KM. 2010. ArcS, the cognate sensor kinase in an atypical Arc system of Shewanella oneidensis MR-1. Appl. Environ. Microbiol. 76:3263-3274.
36. Li CL, et al. 2003. DNA binding and cleavage by the periplasmic nuclease Vvn: a novel structure with a known active site. EMBO J. 22:4014-4025.
37. Logan BE. 2009. Exoelectrogenic bacteria that power microbial fuel cells. Nat. Rev. Microbiol. 7:375-381.
38. Mann EE, et al. 2009. Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS One 4:e5822. doi: 10.1371/journal.pone.0005822.
39. Miller VL, Mekalanos JJ. 1988. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170:2575-2583.
40. Mulcahy H, Charron-Mazenod L, Lewenza S. 2008. Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog. 4:e1000213. doi:10.1371/journal.ppat. 1000213.
41. Mulcahy H, Charron-Mazenod L, Lewenza S. 2010. Pseudomonas aeruginosa produces an extracellular deoxyribonuclease that is required for utilization of DNA as a nutrient source. Environ. Microbiol. 12:1621-1629.
42. Mulcahy H, Lewenza S. 2011. Magnesium limitation is an environmental trigger of the Pseudomonas aeruginosa biofilm lifestyle. PLoS One 6:e23307. doi:10.1371/journal.pone.0023307.
43. Myers CR, Nealson KH. 1988. Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 240: 1319-1321.
44. Nealson KH, Scott J. 2003. Ecophysiology of the genus Shewanella, p 1133-1151. In Dworkin M (ed), The prokaryotes: an evolving electronic resource for the microbial community. Springer-NY, LLC, New York, NY.
45. Nijland R, Hall MJ, Burgess JG. 2010. Dispersal of biofilms by secreted, matrix degrading, bacterial DNase. PLoS One 5:e15668. doi:10.1371/ journal.pone.0015668.
46. Palmgren R, Nielsen PH. 1996. Accumulation of DNA in the exopolymeric matrix of activated sludge and bacterial cultures. Water Sci. Technol. 34:233-240.
47. Paulick A, et al. 2009. Two different stator systems drive a single polar flagellum in Shewanella oneidensis MR-1. Mol. Microbiol. 71:836-850.
48. Pinchuk GE, et al. 2008. Utilization of DNA as a sole source of phosphorus, carbon, and energy by Shewanella spp.: ecological and physiological implications for dissimilatory metal reduction. Appl. Environ. Microbiol. 74:1198-1208.
49. Pospiech A, Neumann B. 1995. A versatile quick-prep of genomic DNA from gram-positive bacteria. Trends Genet. 11:217-218.
50. Sambrook K, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
51. Seper A, et al. 2011. Extracellular nucleases and extracellular DNA play important roles in Vibrio cholerae biofilm formation. Mol. Microbiol. 82: 1015-1037.
52. Steichen CT, Cho C, Shao JQ, Apicella MA. 2011. The Neisseria gonorrhoeae biofilm matrix contains DNA, and an endogenous nuclease controls its incorporation. Infect. Immun. 79:1504-1511.
53. Steinberger RE, Holden PA. 2005. Extracellular DNA in single- and multiple-species unsaturated biofilms. Appl. Environ. Microbiol. 71: 5404-5410.
54. Tang X, et al. 2007. Profiling the membrane proteome of Shewanella oneidensis MR-1 with new affinity labeling probes. J. Proteome Res. 6:724-734.
55. Thormann KM, et al. 2006. Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic di-GMP. J. Bacteriol. 188:2681-2691.
56. Thormann KM, Saville RM, Shukla S, Pelletier DA, Spormann AM. 2004. Initial phases of biofilm formation in Shewanella oneidensis MR-1. J. Bacteriol. 186:8096-8104.
57. Thormann KM, Saville RM, Shukla S, Spormann AM. 2005. Induction of rapid detachment in Shewanella oneidensis MR-1 biofilms. J. Bacteriol. 187:1014-1021.
58. Tsai MS, You HL, Tang YF, Liu JW. 2008. Shewanella soft tissue infection: case report and literature review. Int. J. Infect. Dis. 12:e119-e124.
59. Venkateswaran K, et al. 1999. Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov. Int. J. Syst. Bacteriol. 49:705-724.
60. Vilain S, Pretorius JM, Theron J, Brözel VS. 2009. DNA as an adhesin: Bacillus cereus requires extracellularDNAto form biofilms. Appl. Environ. Microbiol. 75:2861-2868.
61. Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS. 2002. Extracellular DNA required for bacterial biofilm formation. Science 295:1487.
62. Wu SI, Lo SK, Shao CP, Tsai HW, Hor LI. 2001. Cloning and characterization of a periplasmic nuclease of Vibrio vulnificus and its role in preventing uptake of foreign DNA. Appl. Environ. Microbiol. 67:82-88.
63. Yang W. 2011. Nucleases: diversity of structure, function and mechanism. Q. Rev. Biophys. 44:1-93.
64. Ziemke F, Brettar I, Höfle MG. 1997. Stability and diversity of the genetic structure of a Shewanella putrefaciens population in the water column of the Central Baltic. Aquat. Microb. Ecol. 13:63-74.