Unrecognized Contributions of Dissolved Organic Matter Inducing Photodamages to the Decay of Extracellular DNA in Waters

Abstract

Extracellular DNA (eDNA), which is derived from lysis or secretion of cells, is ubiquitous in various environments and crucial for gene dissemination, bacterial metabolism, biofilm integrity, and aquatic monitoring. However, these processes are largely influenced by damage to eDNA. Photodamage to eDNA, one of the most important types of DNA damage in natural waters, thus far remains unclear. In particular, the roles of the ubiquitous dissolved organic matter (DOM) in this process have yet to be determined. In this study, eDNA photodamage, including both deoxynucleoside damage and strand breaks, proved to be significantly influenced by DOM. DOM competed with eDNA for photons to inhibit the direct photodamage of eDNA. Nevertheless, DOM was photosensitized to produce reactive oxygen species (ROS) (i.e., hydroxyl radicals (·OH) and singlet oxygen (1O2)) to enhance the indirect photodamage of eDNA. The ·OH induced damage to four deoxynucleosides and strand breaks, and the 1O2 substantially enhanced deoxyguanosine damage. The presence of DOM changed the main photodamage products of deoxynucleosides, additional oxidation products induced by ROS formed besides pyrimidine dimers caused by UV. Results indicate that DOM-mediated indirect photodamage contributed significantly to eDNA photodamage in most water bodies. This study revealed the previously unrecognized crucial role of DOM in the decay of eDNA in waters.

Assessment of the UV/Chlorine Process in the Disinfection of Pseudomonas aeruginosa: Efficiency and Mechanism

“…14−16 acids (eDNA) in the UV/H 2 O 2 process and in the natural organic matter photosensitized system. 17,18 However, HO • is nonselective and results in rapid consumption by cellular components before contacting intracellular DNA (iDNA). 18,19 In contrast, RCS (Cl • , Cl 2 •− , and ClO • ) selectively react with compounds containing electron-rich groups, 20 such as amino acids, pyrimidines, and purines.…”

“…HO • has been demonstrated to play an important role in the inactivation of tetracycline-resistant Escherichia coli and in the removal of antibiotic resistance genes (ARGs) ( e.g. , sul 1 and blt ) by UV/chlorine treatment. − Additionally, HO • promotes the elimination of extracellular deoxyribonucleic acids (eDNA) in the UV/H 2 O 2 process and in the natural organic matter photosensitized system. , However, HO • is nonselective and results in rapid consumption by cellular components before contacting intracellular DNA (iDNA). , In contrast, RCS (Cl • , Cl 2 •– , and ClO • ) selectively react with compounds containing electron-rich groups, such as amino acids, pyrimidines, and purines. In addition, the concentrations of RCS, especially ClO • , are higher than that of HO • in the UV/chlorine process .…”

Marine Colloids Promote the Adaptation of Diatoms to Nitrate Contamination by Directional Electron Transfer

“…15,16 Colloids can be photosensitized to produce reactive oxygen species (ROS), such as hydroxyl radicals ( • OH) and singlet oxygen ( 1 O 2 ), under visible-light irradiation. 17 Extracellular polymeric substances (EPSs) produced by microorganisms are ubiquitous and crucial in microbial extracellular electron transfer. 18 Electron transfer mandates the carbon matrix in natural pyrogenic carbon and the microbial reduction of solid-phase humic substances.…”

Why eDNA fractions need consideration in biomonitoring

“…Alternative acronyms/identifiers eDNA Environmental DNA totDNA (total DNA) (Ascher, Ceccherini, Pantani, et al, 2009;Fulgosi et al, 2012;Nagler, Podmirseg, et al, 2018;Nagler et al, 2020), tDNA (Ceccherini et al, 2009;Ramírez et al, 2018) exDNA Extracellular DNA eDNA (Agnelli et al, 2007;Aldeguer-Riquelme et al, 2021;Ascher, Ceccherini, Pantani, et al, 2009;Ceccherini et al, 2009;Gomez-Brandon et al, 2017;Liang et al, 2021;Ramírez et al, 2018;Torti et al, 2015;Vuillemin et al, 2016;Zhang et al, 2020), extDNA (Pansu et al, 2021), relic DNA (Burkert et al, 2019;Carini et al, 2016;Lennon et al, 2018), sDNA (soluble DNA) (Lever et al, 2015), sedaDNA (sediment ancient DNA) (Haile et al, 2009) f-exDNA Free extracellular DNA fDNA (Nagler, Podmirseg, et al, 2018;Nagler et al, 2020), cfDNA (cell-free DNA) (Gravina et al, 2016), cirDNA (Thierry et al, 2016) wb-exDNA Weakly bound extracellular DNA wbDNA (Nagler, Podmirseg, et al, 2018;Nagler et al, 2020), Wa (Pathan et al, 2020), adsDNA (adsorbed DNA) (Ceccherini et al, 2009) tb-exDNA Tightly bound extracellular DNA tbDNA (Nagler, Podmirseg, et al, 2018;Nagler et al, 2020), Ta (Pathan et al, 2020) iDNA intracellular DNA nsDNA (nonsoluble DNA) (Lever et al, 2015), cellular DNA (Taberlet et al, 2012), genomic DNA (Pawlowski et al, 2020) This...…”

“…Elevated organic matter (OM) content seems to play a crucial role in trapping DNAses to soil colloids and minerals and hence, reducing the degradation speed of exDNA (Cai et al, 2006). In aquatic environments, UV‐radiation, dissolved OM‐ and salt concentrations are additional constraints potentially influencing exDNA decay (Ellegaard et al, 2020; Zhang et al, 2020). In addition, also the binding strength to particles (i.e., fDNA, wbDNA or tbDNA) determines the extent of protection, exposition and accessibility of exDNA to degradation by nucleases.…”