Preliminary evidences of the presence of extracellular DNA single stranded forms in soil


Autoři: Shamina Imran Pathan aff001;  Paola Arfaioli aff001;  Maria Teresa Ceccherini aff001;  Judith Ascher-Jenull aff002;  Giacomo Pietramellara aff001
Působiště autorů: Department of Agri-food, Environmental, Forestry Science and Technology (DAGRI), University of Florence, Piazzale delle Cascine, Florence, Italy aff001;  Institute of Microbiology, University of Innsbruck, Innsbruck, Austria aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227296

Souhrn

The relevance of extracellular DNA (eDNA) in the soil ecosystem is becoming more and more evident to the scientific community by the progressive discovery of functions accompanying to natural gene transformation. However, despite the increased number of published articles dedicated to eDNA in soil, so far only few are focused on its single stranded form (eDNAss). The present paper is the first to investigate the quantitative relevance of eDNAss in the total soil eDNA pool, discriminating between its linear (eDNAssl) and circular (eDNAssc) forms and the respective weakly (wa) and tightly (ta) adsorbed fractions. The results showed the prevalence of eDNAss and its linear form in both the total soil eDNA pool and its wa and ta fractions. Both of the eDNAss fractions (linear and circular) were characterized by small fragments.

Klíčová slova:

Adsorption – Analysis of variance – DNA – DNA extraction – Elution – Gene pool – Soil ecology – Qubits


Zdroje

1. Ascher J, Ceccherini MT, Pantani LO, Agnelli A, Borgogni F, Guerri G, Nannipieri P, Pietramellara G. Sequential extraction and genetic fingerprinting of a forest soil metagenome. Applied Soil Ecology. 2009; 42:176–181.

2. Carini P, Marsden PJ, Leff JW, Morgan EE, Strickland MS, Fierer N. Relic DNA is abundant in soil and obscures estimates of soil microbial diversity. Nature Microbiology. 2016; 2:16242 doi: 10.1038/nmicrobiol.2016.242 27991881

3. Nagler M, Insam H, Pietramellara G, Ascher-Jenull J. Extracellular DNA in natural environments: features, relevance and applications. Applied Microbiology and Biotechnology. 2018; 102:6343–6356. doi: 10.1007/s00253-018-9120-4 29858957

4. Palchevskiy V, Finkel SE. Escherichia coli competence gene homologs are essential for competitive fitness and the use of DNA as a nutrient. Journal of Bacteriology. 2006; 88 (1):3902–10.

5. Mulcahy H, Charron‐Mazenod L, Lewenza S. Pseudomonas aeruginosa produces an extracellular deoxyribonuclease that is required for utilization of DNA as a nutrient source. Environmental Microbiology. 2010; 12:1621–1629. doi: 10.1111/j.1462-2920.2010.02208.x 20370819

6. Morrissey EM, McHugh TA, Preteska L, Hayer M, Dijkstra P, Hungate BA, Schwartz. Dynamics of extracellular DNA decomposition and bacterial community composition in soil. Soil Biology and Biochemistry. 2015; 86:42–49.

7. Berne C, Kysela DT, Brun YV. A bacterial extracellular DNA inhibits settling of motile progeny cells within a biofilm. Molecular Microbiology. 2010; 77 (4): 815–829. doi: 10.1111/j.1365-2958.2010.07267.x 20598083

8. Gloag ES, Turnbull L, Huang A, Vallotton P, Wang H, Nolan LM, Mililli L, Hunt C, Lu J, Osvath SR, Monahan LG, Cavaliere R, Charles IG, Wand MP, Gee ML, Prabhaka R, Whitchurch CB. Self-organization of bacterial biofilms is facilitated by extracellular DNA. Proceedings of the National Academy of Sciences. 2013; 110:11541–11546. doi: 10.1073/pnas.1218898110 23798445

9. Vorkapic D, Pressler K, Schild S. Multifaceted roles of extracellular DNA in bacterial physiology. Current Genetics. 2016; 62:71–79 doi: 10.1007/s00294-015-0514-x 26328805

10. Swenson TL, Couradeau E, Bowen BP, De Philippis R, Rossi F, Mugnai G, Northenet TR. A novel method to evaluate nutrient retention by biological soil crust exopolymeric matrix. Plant and Soil. 2017; 429:53–64 | https://doi.org/10.1007/s11104-017-3537-x.

11. Young IM, Crawfiord JW. Interactions and Self-Organization in the Soil-Microbe Complex. Science. 2004; 11:304:1634–7.

12. Crawford JW, Deacon L, Grinev D, Harris JA, Ritz K, Singh BK, Young I. Microbial diversity affects self-organization of the soil. Journal of The Royal Society Interface. 2012; 9:302–1310.

13. Allesen-Holm M, Barken KB, Yang L, Klausen M, Webb JS, Kjelleberg S, Molin S, Givskov M, Tolker-Nielsen T. A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Molecular Microbiology. 2006; 59: 1114–1128. doi: 10.1111/j.1365-2958.2005.05008.x 16430688

14. Barken KB, Pamp SJ, Yang L, Gjermansen M, Bertrand JJ, Klausen M, Givskov M, Whitchurch CB, Engel JN, Tolker‐Nielsen T. Roles of type IV pili, flagellum-mediated motility and extracellular DNA in the formation of mature multicellular structures in Pseudomonas aeruginosa biofilms. Environmental Microbiology. 2008; 10:2331–2343. doi: 10.1111/j.1462-2920.2008.01658.x 18485000

15. Paungfoo-Lonhienne C, Lonhienne TGA, Schmidt S. DNA uptake by Arabidopsis induces changes in the expression of CLE peptides which control root morphology Plant Signaling & Behavior. 2010; 5(9):1–3.

16. Hawes MC, Curlango-Rivera G, Xiong Z, Kessler JO. Roles of root border cells in plant defense and regulation of rhizosphere microbial populations by extracellular DNA ‘trapping’. Plant and Soil. 2012; 355:1–16.

17. Hawes MC, McLain J, Ramirez-Andreotta M, Curlango-Rivera G. Extracellular trapping of soil contaminants by root border cells: New insights into plant defense. Agronomy (Basel). 2016; 6:1–9.

18. Mazzoleni S, Cartenì F, Bonanomi G, Senatore M, Termolino P, Giannino F, Incerti G, Rietkerk M, Lanzotti V, Chiusano ML. Inhibitory effects of extracellular self-DNA: a general biological process? New Phytologist. 2015; 206(1):127–32. doi: 10.1111/nph.13306 25628124

19. Beall GW, Somersby DS, Roberts RD, Robson MH, Lewis KL. Analysis of Oligonucleotide DNA Binding and Sedimentation Properties of Montmorillonite Clay Using Ultraviolet Light Spectroscopy. Biomacromolecules. 2009; 10(1):105–112. doi: 10.1021/bm800970v 19061334

20. Matsuura Y, Arakawa S, Okamoto M. Single-strand DNA adsorption characteristics by hollow spherule allophane nano-paticles:pH dependence and computer simulation. Applied Clay Science 2014; 101:591–597.

21. Gardner CM, Gunsch CK. Adsorption capacity of multiple DNA sources to clay minerals and environmental soil matrices less than previously estimated. Chemosphere. 2017; 175:45–51. doi: 10.1016/j.chemosphere.2017.02.030 Epub 2017 Feb 5. 28211334

22. Cleaves HJ, Crapster-Pregont E, Jonsson CM, Jonsson CL, Sverjensky DA, Hazen RA. The adsorption of short single-strand DNA oligomers to mineral surfaces. Chemosphere. 2011; 83: 1560–1567. doi: 10.1016/j.chemosphere.2011.01.023 21316734

23. Sanesi G, Certini G. The umbric epipedon in the N Apennines, Italy—An example from the Vallombrosa Forest. Journal of Plant Nutrition and Soil Science. 2005; 168(3):392–398.

24. Ceccherini MT, Ascher J, Agnelli A, Borgogni F, Pantani OL, Pietramellara G. Experimental discrimination and molecular characterization of the extracellular soil DNA fraction. Antonie van Leeuwenhoek. 2009; 96: 653–657. doi: 10.1007/s10482-009-9354-3 19533410

25. Gagic D, MacLean PH, LI D, Attwod GT, Moon CD. Improving the genetic representation of rare taxa within complex microbial communities using DNA normalization methods. Molecular Ecology Resources. 2015; 15:464–476. doi: 10.1111/1755-0998.12321 25159704

26. Andrews-Pfannkoch C, Fadrosh DW, Thorpe J, Williamson SJ. Hydroxyapatite-Mediated Separation of Double-Strand DNA, Single-Strand DNA, and RNA Genomes from Natural Viral Assemblages. Applied and Environmental Microbiology. 2010; 76 (15):5039–45. doi: 10.1128/AEM.00204-10 20543058

27. Hammer Ø, Harper DAT, Ryan PD. PAST: Paleontological statistic software package for education and data analysis. Palaeontol Electron. 2001; 4:1–9.

28. Saeki K, Ihyo Y, Sakai M, Kunito T. Strong adsorption of DNA molecules on humic acids. Environ Chemistry Letter. 2011; 9:505–509 doi: 10.1007/s10311-011-0310-x

29. Poly F, Chenu C, Simonet P, Rouiller J, Monrozier LJ. Differences between linear chromosomal and supercoiled plasmid DNA in their mechanisms and extent of adsorption on clay minerals. Langmuir. 2000; 16:1233–1238.

30. Franchi M, Ferris JP, Gallori E. Cations as mediators of the adsorption of nucleic acids on clay surfaces in prebiotic environments. Origins of Life and Evolution of Biospheres. 2003; 33:1–16.

31. Pedeira-Segade U, Hao J, Razafitianamaharavo A, Pelletier M, Marry V, Le Crom S, Michot LJ, Daniel I. How do Nucleotides Adsorb On to Clays? Life. 2018; 8:59. doi: 10.3390/life80400592018 30486384

32. Pietramellara G, Franchi M, Gallori E, Nannipieri P. Effect of molecular characteristics of DNA on its adsorption and binding on homoionic montmorillonite and kaolinite. Biology and Fertility of Soils. 2001; 33:402–409 doi: 10.1007/s003740100341

33. Saeki K, Kunito T. Adsorptions of DNA molecules by soils and variable-charged soil. In Mendez Vilas A.Ed. Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology. 2010; 188–195

34. Agnelli A, Ascher J, Corti G, Ceccherini MT, Nannipieri P, Pietramellara G. Distribution of microbial communities in a forest soil profile investigated by microbial biomass, soil respiration and DGGE of total and extracellular DNA. Soil Biology and Biochemistry. 2004; 36 (5):859–868.

35. Khanna M, Stotzky G. Transformation of Bacillus subtilis by DNA bound on montmorillonite and effect of DNase on the transforming ability of bound DNA. Applied Environmental Microbiology. 1992; 58:1930–1939. 1622268

36. Pietramellara G, Ascher J, Ceccherini MT, Guerri G, Nannipieri P. Extracellular DNA in soil and sediment: fate and ecological relevance. Biology and Fertility of Soils. 2009; 45 (3):219–235.

37. Agnelli A, Ascher J, Corti G, Ceccherini MT, Pietramellara G, Nannipieri P. Purification and isotopic signatures (δ13C, δ15N, Δ14C) of soil extracellular DNA. Biology and Fertility of Soils. 2007; 44:353–361.

38. Stotzky G, Persistence and biological activity in soil of insecticidal proteins from Bacillus thuringiensis and of bacterial DNA bound on clays and humic acids. Journal of Environmental Quality. 2000; 29:691–705.

39. D'Souza D, Kool ET. Solvent, pH, and Ionic Effects on the Binding of Single-Strand DNA by Circular Oligodeoxynucleotides. Bioorganic and Medicinal Chemistry Letters. 1994; 21(4):965–970. doi: 10.1016/S0960-894X(01)80664-8 27840561

40. Demaneche S, Jocteur-Monrozier L, Quiquampoix H, Simonet P. Evaluation of Biological and Physical Protection against Nuclease Degradation of Clay-Bound Plasmid DNA. Applied and Environmental Microbiology. 2001; 67(1): 293–299. doi: 10.1128/AEM.67.1.293-299.2001 11133458

41. Wang F, Che R, Xu Z, Wang Y, Cui X. Assessing soil extracellular DNA decomposition dynamics through plasmid amendment coupled with real-time PCR. Journal of Soils and Sediments. 2019; 19, 1:91–96. https://doi.org/10.1007/s11368-018-2176-z.

42. Ceccherini MT, Ascher J, Nannipieri P, Pietramellara G, Vogel T. Vertical advection of extracellular DNA by water capillarity in soil column. Soil Biology and Biochemistry. 2007; 39:158–163.


Článek vyšel v časopise

PLOS One


2020 Číslo 1