Lightning-triggered electroporation as a mechanism for horizontal gene transfer

Abstract

Horizontal gene transfer (HGT) plays a prominent role in evolution and genetic variability of life. Five biotic mechanisms of HGTamong prokaryotes have so far been extensively characterized: conjugation, competence, transduction, gene transfer agent particles, and transitory fusion with recombination; but it seems questionable whether they can account for all ongoing HGT, and it is even less clear how HGT could have proceeded before any of these mechanisms - themselves products of evolution - had developed. An alternative and perhaps more general path to HGT is offered by non-biochemical, yet natural mechanisms of destabilization of the membranes enveloping the genetic material: freeze-thaw cycles, abrasive action of gravel and sand, and electroporation triggered by lightning strokes. This chapter focuses on the latter mechanism of gene transfer - DNA uptake and heritable expression based on reversible electroporation (electrotransformation), which is by far the most efficient technique of artificial HGT, reported to date for bacteria from at least 13 of their 29 currently recognized taxonomic phyla, archaea from at least two of their five phyla, microalgae from at least three of their six phyla, and yeasts from both their phyla. As a complement, irreversible electroporation is a mechanism of DNA release (electroextraction), although less efficient in the laboratory than chemical extraction. It is shown that conditions for electroporation-based DNA release, uptake, and transformation are present in many natural habitats exposed to lightning strokes, with quantitative estimates that the number of microorganisms subjected to conditions for lightning-triggered HGT, particularly in freshwater habitats, may well exceed 1017 per year.