Lightning-triggered electroporation and electrofusion as possible contributors to natural HGT among prokaryotes

TL;DR

This paper explores how lightning-induced electroporation and electrofusion could facilitate natural horizontal gene transfer among prokaryotes, especially in early evolution, by reviewing experimental evidence and environmental conditions.

Contribution

It introduces electroporation and electrofusion as plausible natural mechanisms for HGT, expanding understanding beyond traditional methods like conjugation and transduction.

Findings

Electroporation can cause DNA release and uptake in prokaryotes.

Electrofusion can create hybrids of prokaryotes without cell walls.

Natural conditions during lightning strikes may enable these processes.

Abstract

Phylogenetic studies show that horizontal gene transfer (HGT) is a significant contributor to genetic variability of prokaryotes, and was perhaps even more abundant during early evolution. Hitherto, research of natural HGT has mainly focused on three mechanisms: conjugation, natural competence, and viral transduction. This paper discusses the feasibility of a fourth such mechanism - cell electroporation and/or electrofusion triggered by atmospheric electrostatic discharges (lightnings). A description of electroporation as a phenomenon is followed by a review of experimental evidence that electroporation of prokaryotes in aqueous environments can result in release of non-denatured DNA, as well as uptake of DNA from the surroundings and transformation. Similarly, a description of electrofusion is followed by a review of experiments showing that prokaryotes devoid of cell wall can electrofuse into hybrids expressing the genes of their both precursors. Under sufficiently fine-tuned conditions, electroporation and electrofusion are efficient tools for artificial transformation and hybridization, respectively, but the quantitative analysis developed here shows that conditions for electroporation-based DNA release, DNA uptake and transformation, as well as for electrofusion are also present in many natural aqueous environments exposed to lightnings. Electroporation is thus a plausible contributor to natural HGT among prokaryotes, and could have been particularly important during the early evolution, when the other mechanisms might have been scarcer or nonexistent. In modern prokaryotes, natural absence of the cell wall is rare, but it is reasonable to assume that the wall has formed during evolution, and at least prior to this, electrofusion could also have contributed to HGT. The concluding section outlines several guidelines for assessment of the feasibility of lightning-triggered HGT.