The Role of DNA in the Extracellular Environment: A Focus on NETs, RETs and Biofilms

Abstract

The capacity to actively release genetic material into the extracellular environment has been reported for bacteria, archaea, fungi, and in general, for microbial communities, but it is also described in the context of multicellular organisms, animals and plants. This material is often present in matrices that locate outside the cells. Extracellular matrices have important roles in defense response and disease in microbes, animal and plants cells, appearing as barrier against pathogen invasion or for their recognition. Specifically, neutrophils extracellular traps (NETs) in animals and root extracellular traps (RETs) in plants, are recognized to be important players in immunity. A growing amount of evidence revealed that the extracellular DNA, in these contexts, plays an active role in the defense action. Moreover, the protective role of extracellular DNA against antimicrobials and mechanical stress also appears to be confirmed in bacterial biofilms. In parallel, recent efforts highlighted different roles of self (homologous) and non-self (heterologous) extracellular DNA, paving the way to discussions on its role as a “Damage-associated molecular pattern” (DAMP). We here provide an evolutionary overview on extracellular DNA in extracellular matrices like RETs, NETs, and microbial biofilms, discussing on its roles and inferring on possible novel functionalities.

Extracellular Fragmented Self-DNA Is Involved in Plant Responses to Biotic Stress

“…Here we show that not only pathogen fragmented DNA but also self-eDNA induces plant responses typical of biotic responses to pathogens and herbivores. The early and late responses induced by treatment of tomato leaves with tomato eDNA imply the “recognition of small-sized nucleotide molecules” as suggested by several authors ( Duran-Flores and Heil, 2018 ; Heil and Vega-Munoz, 2019 ; Monticolo et al, 2020 ) and the involvement of CPKs, RLKs, ERFs, ion homeostasis (calcium, and potassium involvement) and ROS production demonstrated in this work are strongly consistent with this proposition. Moreover, the ROS production induced by eDNA may trigger further DNA degradation and PCD events, which would reinforce the plant response to eDNA.…”

“…An open question remains whether eDNA acts directly on the plant cell and provokes growth-inhibition effects ( Mazzoleni et al, 2015 ) or acts as a DAMP and plays a role as an elicitor. In plant roots, DNA is excreted and released to the root cap environment by lytic processes ( Driouich et al, 2019 ), but DNA could also be degraded by infection and disruption of root cap cells ( Monticolo et al, 2020 ). In the latter case, eDNA might be involved in plant responses to biotic stress and could be released along with other elicitors in the extracellular environment ( Plancot et al, 2013 ).…”

The effect of crop species on DNase-producing bacteria in two soils

“…The plethora of compounds secreted through the root cap mucilage including genetic material (Wen et al 2009;Knox et al 2020;Ropitaux et al 2020;Chambard et al 2021) provide a source of nutrients and energy that may result in differential growth of microbial communities (Berg and Smalla 2009;Haichar et al 2014). Plant DNA enters the soil environment mainly through root exudates, root cap sloughing, pollen dispersal and degradation of plant materials (Levy-Booth et al 2007;Monticolo et al 2020).…”

“…For instance, Stewart and Sinigalliano (1990) reported a decrease in natural transformation frequency in bacteria after incubating marine and artificial sediments with DNase 1. Microbial exDNases contribute to soil functions and have largely been associated with nutrient scavenging activities (Benedik and Strych 1998;Desai and Shankar 2003;Levy-Booth et al 2007;Ibáñez de Aldecoa et al 2017) and virulence of pathogens (Park et al 2019;Monticolo et al 2020). For example, an increase of up to 35-fold in viable bacterial counts was observed 3 days after spiking soils with nucleic acids, thereby implying that microbes use nucleic acids as substrates for growth (Greaves and Wilson 1970).…”

Understanding In Vitro Tissue Culture-Induced Variation Phenomenon in Microspore System

“…Still, the mechanism of exDNA action is not understood. Most shreds of evidence on exDNA role come from studies on plant roots [ 122 , 123 ]. The importance of protein constituents of the mucilage layer and its treatment with proteases was suggested [ 124 ].…”