A new physiological role for the DNA molecule as a protector against drying stress in desiccation-tolerant microorganisms

Frontiers in Microbiology

Volumn 7, Issue DEC, 2016, Pages

  García Fontana, Cristina ^a   Narváez Reinaldo, Juan J ^a   Castillo, Francisco ^a   González López, Jesús ^a   Luque, Irene ^a   Manzanera, Maximino ^a  

^a UNIVERSITY OF GRANADA   (Spain)

Author keywords

Differential scanning calorimetry; DNA; Lipase activity; RNASeq; Xeroprotection

Indexed keywords

COMPLEMENTARY DNA; DEOXYRIBONUCLEASE I; DESICCANT; DNA; NUCLEASE; RIBONUCLEASE; SYNTHETIC DNA; TRIACYLGLYCEROL LIPASE;

ARTHROBACTER; ARTICLE; BIOFILM; CONTROLLED STUDY; DEFENSE MECHANISM; DESICCATION; DIFFERENTIAL SCANNING CALORIMETRY; DNA SYNTHESIS; DROUGHT; GEL ELECTROPHORESIS; GENE OVEREXPRESSION; GLYCATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MICROBACTERIUM; NONHUMAN; OSMOTIC STRESS; POLYMERASE CHAIN REACTION; PROTEIN STRUCTURE; RNA SEQUENCE; UPREGULATION;

EID: 85009424151     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.02066     Document Type: Article

References (48)

1. Bauer, F., Schweimer, K., Meiselbach, H., Hoffmann, S., Rösch, P., and Sticht, H. (2005). Structural characterization of Lyn-SH3 domain in complex with a herpesviral protein reveals an extended recognition motif that enhances binding affinity. Protein Sci. Publ. Protein Soc. 14, 2487-2498. doi: 10.1110/ps.051563605
2. Boschetti, C., Carr, A., Crisp, A., Eyres, I., Wang-Koh, Y., Lubzens, E., et al. (2012). Biochemical diversification through foreign gene expression in bdelloid rotifers. PLoS Genet. 8:e1003035. doi: 10.1371/journal.pgen.1003035
3. Boschetti, C., Pouchkina-Stantcheva, N., Hoffmann, P., and Tunnacliffe, A. (2011). Foreign genes and novel hydrophilic protein genes participate in the desiccation response of the bdelloid rotifer Adineta ricciae. J. Exp. Biol. 214, 59-68. doi: 10.1242/jeb.050328
4. Cámara-Artigas, A., Martín-García, J. M., Morel, B., Ruiz-Sanz, J., and Luque, I. (2009). Intertwined dimeric structure for the SH3 domain of the c-Src tyrosine kinase induced by polyethylene glycol binding. FEBS Lett. 583, 749-753. doi: 10.1016/j.febslet.2009.01.036
5. Cayley, S., and Record, M. T. (2003). Roles of cytoplasmic osmolytes, water, and crowding in the response of Escherichia coli to osmotic stress: biophysical basis of osmoprotection by glycine betaine. Biochemistry (Mosc.) 42, 12596-12609. doi: 10.1021/bi0347297
6. Cayley, S., and Record, M. T. (2004). Large changes in cytoplasmic biopolymer concentration with osmolality indicate that macromolecular crowding may regulate protein-DNA interactions and growth rate in osmotically stressed Escherichia coli K-12. J. Mol. Recognit. 17, 488-496. doi: 10.1002/jmr.695
7. Chakrabortee, S., Tripathi, R., Watson, M., Schierle, G. S. K., Kurniawan, D. P., Kaminski, C. F., et al. (2012). Intrinsically disordered proteins as molecular shields. Mol. Biosyst. 8, 210-219. doi: 10.1039/c1mb05263b
8. Christie, P. J. (2001). Type IV secretion: intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. Mol. Microbiol. 40, 294-305. doi: 10.1046/j.1365-2958.2001.02302.x
9. Claverys, J.-P., Prudhomme, M., and Martin, B. (2006). Induction of competence regulons as a general response to stress in gram-positive bacteria. Annu. Rev. Microbiol. 60, 451-475. doi: 10.1146/annurev.micro.60.080805.142139
10. Clegg, J. S. (2001). Cryptobiosis-a peculiar state of biological organization. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 128, 613-624. doi: 10.1016/S1096-4959(01)00300-1
11. Clegg, J. S., Seitz, P., Seitz, W., and Hazlewood, C. F. (1982). Cellular responses to extreme water loss: the water-replacement hypothesis. Cryobiology 19, 306-316. doi: 10.1016/0011-2240(82)90159-6
12. Crowe, J. H., Carpenter, J. F., and Crowe, L. M. (1998). The role of vitrification in anhydrobiosis. Annu. Rev. Physiol. 60, 73-103. doi: 10.1146/annurev.physiol.60.1.73
13. da Costa, M. S., Santos, H., and Galinski, E. A. (1998). An overview of the role and diversity of compatible solutes in Bacteria and Archaea. Adv. Biochem. Eng. Biotechnol. 61, 117-153.
14. Hodge, J. E. (1953). Dehydrated foods, chemistry of browning reactions in model systems. J. Agric. Food Chem. 1, 928-943. doi: 10.1021/jf60015a004
15. Hwang, H. I., Hartman, T. G., Rosen, R. T., and Ho, C. T. (1993). Formation of pyrazines from the Maillard reaction of glucose and glutamine-amide-15N. J. Agric. Food Chem. 41, 2112-2115. doi: 10.1021/jf00035a054
16. Julca, I., Alaminos, M., González-López, J., and Manzanera, M. (2012). Xeroprotectants for the stabilization of biomaterials. Biotechnol. Adv. 30, 1641-1654. doi: 10.1016/j.biotechadv.2012.07.002
17. Kado, C. I., and Liu, S. T. (1981). Rapid procedure for detection and isolation of large and small plasmids. J. Bacteriol. 145, 1365-1373.
18. Knowles, D. B., LaCroix, A. S., Deines, N. F., Shkel, I., and Record, M. T. (2011). Separation of preferential interaction and excluded volume effects on DNA duplex and hairpin stability. Proc. Natl. Acad. Sci. U.S.A. 108, 12699-12704. doi: 10.1073/pnas.1103382108
19. Koehler, P. E., Mason, M. E., and Newell, J. A. (1969). Formation of pyrazine compounds in sugar-amino acid model systems. J. Agric. Food Chem. 17, 393-396. doi: 10.1021/jf60162a006
20. Kurz, M. (2008). Compatible solute influence on nucleic acids: many questions but few answers. Saline Syst. 4: 6. doi: 10.1186/1746-1448-4-6
21. Kwak, E.-J., and Lim, S.-I. (2004). The effect of sugar, amino acid, metal ion, and NaCl on model Maillard reaction under pH control. Amino Acids 27, 85-90. doi: 10.1007/s00726-004-0067-7
22. Lippert, K., and Galinski, E. A. (1992). Enzyme stabilization be ectoine-type compatible solutes: protection against heating, freezing and drying. Appl. Microbiol. Biotechnol. 37, 61-65. doi: 10.1007/BF00174204
23. Louis, P., Trüper, H. G., and Galinski, E. A. (1994). Survival of Escherichia coli during drying and storage in the presence of compatible solutes. Appl. Microbiol. Biotechnol. 41, 684-688. doi: 10.1007/BF00167285
24. Manzanera, M., García de Castro, A, Tøndervik, A., Rayner-Brandes, M., Strøm, A. R., and Tunnacliffe, A. (2002). Hydroxyectoine is superior to trehalose for anhydrobiotic engineering of Pseudomonas putida KT2440. Appl. Environ. Microbiol. 68, 4328-4333. doi: 10.1128/AEM.68.9.4328-4333.2002
25. Manzanera, M., García-Fontana, C., Vílchez, J. I., and González-López, J. (2015). Genome sequence of Rhodococcus sp. 4J2A2, a desiccation-tolerant bacterium involved in biodegradation of aromatic hydrocarbons. Genome Announc. 3, e00592-15. doi: 10.1128/genomeA.00592-15
26. Manzanera, M., Santa-Cruz-Calvo, L., Vílchez, J. I., García-Fontana, C., Silva-Castro, G. A., Calvo, C., et al. (2014). Genome sequence of Arthrobacter siccitolerans 4J27, a xeroprotectant-producing desiccation-tolerant microorganism. Genome Announc. 2, e00526-514. doi: 10.1128/genomeA.00526-14
27. Manzanera, M., Vilchez, S., and Tunnacliffe, A. (2004a). High survival and stability rates of Escherichia coli dried in hydroxyectoine. FEMS Microbiol. Lett. 233, 347-352. doi: 10.1016/j.femsle.2004.03.005
28. Manzanera, M., Vilchez, S., and Tunnacliffe, A. (2004b). Plastic encapsulation of stabilized Escherichia coli and Pseudomonas putida. Appl. Environ. Microbiol. 70, 3143-3145. doi: 10.1128/AEM.70.5.3143-3145.2004
29. Martinez, J. C., Viguera, A. R., Serrano, L., Filimonov, V. V., and Mateo, P. L. (1998). The DSC data analysis for small, single-domain proteins. Application to the SH3 domain. React. Funct. Polym. 36, 221-225. doi: 10.1016/S1381-5148(97)00088-6
30. Mattimore, V., and Battista, J. R. (1996). Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J. Bacteriol. 178, 633-637. doi: 10.1128/jb.178.3.633-637.1996
31. Mell, J. C., and Redfield, R. J. (2014). Natural competence and the evolution of DNA uptake specificity. J. Bacteriol. 196, 1471-1483. doi: 10.1128/JB.01293-13
32. Montgomery, D. C. (1999). Experimental design for product and process design and development. J. R. Stat. Soc. Ser. Stat. 48, 159-177. doi: 10.1111/1467-9884.00179
33. Narváez-Reinaldo, J. J., Barba, I., González-López, J., Tunnacliffe, A., and Manzanera, M. (2010). Rapid method for isolation of desiccation-tolerant strains and xeroprotectants. Appl. Environ. Microbiol. 76, 5254-5262. doi: 10.1128/AEM.00855-10
34. Nursten, H. E. (1981). Recent developments in studies of the maillard reaction. Food Chem. 6, 263-277. doi: 10.1016/0308-8146(81)90014-5
35. Pageon, H., Técher, M.-P., and Asselineau, D. (2008). Reconstructed skin modified by glycation of the dermal equivalent as a model for skin aging and its potential use to evaluate anti-glycation molecules. Exp. Gerontol. 43, 584-588. doi: 10.1016/j.exger.2008.04.004
36. Pallen, M. J. (2002). The ESAT-6/WXG100 superfamily-and a new Gram-positive secretion system? Trends Microbiol. 10, 209-212. doi: 10.1016/S0966-842X(02)02345-4
37. Record, M. T., Courtenay, E. S., Cayley, D. S., and Guttman, H. J. (1998). Responses of E. coli to osmotic stress: large changes in amounts of cytoplasmic solutes and water. Trends Biochem. Sci. 23, 143-148. doi: 10.1016/S0968-0004(98)01196-7
38. Reddy, M. K., Weitzel, S. E., Daube, S. S., Jarvis, T. C., and von Hippel, P. H. (1995). Using macromolecular crowding agents to identify weak interactions within DNA replication complexes. Methods Enzymol. 262, 466-476. doi: 10.1016/0076-6879(95)62038-9
39. Requena, J. R., Vidal, P., and Cabezas-Cerrato, J. (1993). Aminoguanidine inhibits protein browning without extensive Amadori carbonyl blocking. Diabetes Res. Clin. Pract. 19, 23-30. doi: 10.1016/0168-8227(93)90141-Q
40. Santacruz-Calvo, L., González-López, J., and Manzanera, M. (2013). Arthrobacter siccitolerans sp. nov., a highly desiccation-tolerant, xeroprotectant-producing strain isolated from dry soil. Int. J. Syst. Evol. Microbiol. 63, 4174-4180. doi: 10.1099/ijs.0.052902-0
41. Sauer, T., and Galinski, T. A. (1998). Bacterial milking: A novel bioprocess for production of compatible solutes. Biotechnol. Bioeng. 59: 128. doi: 10.1002/(SICI)1097-0290(19980705)59:1<128::AID-BIT17>3.0.CO;2-E
42. Szydlowski, L., Boschetti, C., Crisp, A., Barbosa, E. G. G., and Tunnacliffe, A. (2015). Multiple horizontally acquired genes from fungal and prokaryotic donors encode cellulolytic enzymes in the bdelloid rotifer Adineta ricciae. Gene 566, 125-137. doi: 10.1016/j.gene.2015.04.007
43. Tanne, C., Golovina, E. A., Hoekstra, F. A., Meffert, A., and Galinski, E. A. (2014). Glass-forming property of hydroxyectoine is the cause of its superior function as a desiccation protectant. Front. Microbiol. 5:150. doi: 10.3389/fmicb.2014.00150
44. Tunnacliffe, A., and Lapinski, J. (2003). Resurrecting Van Leeuwenhoek's rotifers: a reappraisal of the role of disaccharides in anhydrobiosis. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 358, 1755-1771. doi: 10.1098/rstb.2002.1214
45. Vílchez, J. I., García-Fontana, C., Román-Naranjo, D., González-López, J., and Manzanera, M. (2016). Plant drought tolerance enhancement by trehalose production of desiccation-tolerant microorganisms. Front. Microbiol. 7:1577. doi: 10.3389/fmicb.2016.01577
46. Vorkapic, D., Pressler, K., and Schild, S. (2016). Multifaceted roles of extracellular DNA in bacterial physiology. Curr. Genet. 62, 71-79. doi: 10.1007/s00294-015-0514-x
47. Welsh, D. T. (2000). Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol. Rev. 24, 263-290. doi: 10.1111/j.1574-6976.2000.tb00542.x
48. Zhai, R. G., Zhang, F., Hiesinger, P. R., Cao, Y., Haueter, C. M., and Bellen, H. J. (2008). NAD synthase NMNAT acts as a chaperone to protect against neurodegeneration. Nature 452, 887-891. doi: 10.1038/nature06721