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.
Highlights
The presence of extracellular materials, organized as extracellular matrix (ECM), glycocalyx, or mucus layers, has been described in both vertebrates (Huxley-Jones et al, 2007; Möckl, 2020) and invertebrates (Har-el and Tanzer, 1993; Schröder and Bosch, 2016) as well as in plants (Driouich et al, 2013) and microorganisms (Flemming and Wingender, 2010)
The discovery of Mazzoleni et al (2015a) was extended by the same authors to different organisms other than plants, including microbes, fungi, protozoa, and insects (Mazzoleni et al, 2015b). Noticeable, these studies demonstrated that the toxic effect due to exposure to self-DNA in plants is a general phenomenon, that appear to be a typical response in all species in all kingdoms, paving the way to further studies that could address the role and the molecular mechanisms involved in self-extracellular DNA (exDNA) sensing
Further intriguing roles of exDNA produced by an organism or by cells from the same species, have been described in terms of extracellular self-DNA inhibitory effects
Summary
The presence of extracellular materials, organized as extracellular matrix (ECM), glycocalyx, or mucus layers, has been described in both vertebrates (Huxley-Jones et al, 2007; Möckl, 2020) and invertebrates (Har-el and Tanzer, 1993; Schröder and Bosch, 2016) as well as in plants (Driouich et al, 2013) and microorganisms (Flemming and Wingender, 2010). The extracellular structures may fulfill relevant roles in terms of structure and functional organization, contributing to fundamental processes like cell adhesion, migration, proliferation, differentiation, and apoptosis They can act as protective barriers in preventing pathogen invasion, or represent advantageous habitats to facilitate symbiotic interactions, for example favoring adhesion of microbial communities (Yue, 2014; Schröder and Bosch, 2016; Möckl, 2020). The root extracellular traps (RETs), by analogy with the NETs, are identified as high molecular weight compounds surrounding the plant root cap They are mostly composed by carbohydrates, and are produced by the root border cells, playing a crucial role in plant defense (Hawes et al, 2011, 2016; Driouich et al, 2013). The role of exDNA in these matrices is discussed in relationship with the evidence of the inhibitory role of conspecific exDNA on cell growth (Mazzoleni et al, 2015a,b), suggesting possible additional functions for DNA in extracellular matrices
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