Laboratory-Scale Evidence for Lightning-Mediated Gene Transfer in Soil

Abstract

Electrical fields and current can permeabilize bacterial membranes, allowing for the penetration of naked DNA. Given that the environment is subjected to regular thunderstorms and lightning discharges that induce enormous electrical perturbations, the possibility of natural electrotransformation of bacteria was investigated. We demonstrated with soil microcosm experiments that the transformation of added bacteria could be increased locally via lightning-mediated current injection. The incorporation of three genes coding for antibiotic resistance (plasmid pBR328) into the Escherichia coli strain DH10B recipient previously added to soil was observed only after the soil had been subjected to laboratory-scale lightning. Laboratory-scale lightning had an electrical field gradient (700 versus 600 kV m ؊1) and current density (2.5 versus 12.6 kA m ؊2 ) similar to those of full-scale lightning. Controls handled identically except for not being subjected to lightning produced no detectable antibiotic-resistant clones. In addition, simulated storm cloud electrical fields (in the absence of current) did not produce detectable clones (transformation detection limit, 10 ؊9). Natural electrotransformation might be a mechanism involved in bacterial evolution.Ongoing sequencing and comparison of bacterial genomes are gradually modifying our understanding of how bacteria evolved. Although earlier ideas included a point mutationbased evolution occurring slowly and regularly, new theories propose a more erratic evolution in which drastic changes in the genome are due to irregular acquisition of new genetic information by horizontal gene transfers (HGT) (13). However, the frequency of HGT would have had to be so high during bacterial evolution that some evolutionists are questioning the accuracy of the phylogenetic analyses (5). Moreover, these analyses underestimate the actual number of transfers by missing the oldest events. Their efficiency is also limited to the transferred genes, which were successfully fixed in a microbial population by increasing the overall fitness. These sequence-based tools also miss the great majority of transfer events that conferred neutral or deleterious traits and therefore were subsequently deleted. In addition, numerous microcosm-based investigations devoted to studying these events, and specifically natural genetic transformation in environments, such as soil, sediment, and water, conclude that HGT would occur at extremely low frequencies (10,15).Natural transformation of bacteria in soil by extracellular DNA is a multistep process, precluding its occurrence at high frequency (15). When released into the soil at the death of organisms (or more actively for some bacteria), naked DNA has to avoid both enzymatic degradation and irreversible adsorption onto soil particles (4). Moreover, when taken up into the cell, transforming DNA still has to resist the numerous restriction and modification mechanisms and to be integrated into the host genome via homologous or illegitimate recombination (or to repli...

Isolation of Lightning-Competent Soil Bacteria

“…In soil, salt concentrations are described as compatible with the induction of a competent phase (18). In addition, Demanèche et al (8) showed that the electrical parameters occurring during electroporation (in vitro) were similar to those in soil microcosms subjected to lightning-mediated current injection (in situ). Moreover, these authors provided evidence for lightningmediated gene transfer (electrotransformation) of an E. coli strain in sterile soil.…”

“…E. coli strain DH10B was used as the positive control (8), and P. fluorescens C7R12 was used as the Pseudomonas reference strain. The soil experimental system used (soil from Côte Saint-André, France) was the same as that previously described (8). The soil was dried before ␥-sterilization (25-kGy; IONISOS, Dagneux, France).…”

Risks from GMOs due to Horizontal Gene Transfer

“…antibiotic resistance and virulence genes) and then fuse with another bacterium (Dorward et al, 1989;Kadurugamuwa and Beveridge, 1997;Yaron et al, 2000). -Virus-like particles (gene transfer agent) formed from proteins encoded by some bacterial genomes, which can trap random fragments of the genome (about 4400-13 600 base pairs) and transmit them to a second bacterium (Dykhuizen and Baranton, 2001;Lang and Beatty, 2001;Marrs, 1974 (Bos, 1999), by lightning in a manner analogous to genetic modification by electroporation (Demanèche et al, 2001) or desiccation (Gladyshev et al, 2008).…”

Novel Group I Intron in the tRNA Leu (UAA) Gene of a γ-Proteobacterium Isolated from a Deep Subsurface Environment

“…The fact that there is an intronic open reading frame with endonuclease activity in at least one strain (6,7,24) suggests that this intron is capable of mobility. On the other hand, recent evidence (12) suggests that lightning-mediated gene transfer could take place in soil and might be a mechanism involved in bacterial evolution. The introns from this family FIG.…”