Evolution Powered by Lightning?

In the film derivation of Mary Shelley’s classic, “Frankenstein”, the eccentric doctor floods the body of his chimaeric creation with the energy from a lightning bolt, imparting the monstrous biological assemblage with new life. Pure science fiction?

Well, perhaps not completely.

I’m not referring to the surge of electricity that can sometimes reanimate the heart of a trauma patient. I am also not talking about any discharges of energy that may or may not have catalyzed any of the early chemical reactions on the way to abiogenesis on the primordial earth. I am referring to the potential ability of lightning to accelerate evolution in living soil bacteria, to help living bacteria acquire ‘new life’ in the form of novel physiological abilities.

Horizontal Gene Transfer (HGT)

Recall that in an earlier post (“Evolution’s Usual Suspects: 1. Plagiarizing Wizards“) I described the remarkable ability of many bacteria to integrate into their own chromosome foreign fragments of DNA discarded by other species. This process of horizontal gene transfer (HGT) potentially allows them to acquire physiological traits (e.g. the capacity to break down new compounds for energy) that are encoded on the genes within the recovered fragments. The process could accelerate evolution because once such physiological abilities have evolved once, it provides a shortcut that circumvents the need to repeatedly evolve them in different lineages through lengthy series of mutations.

Graphical representation of horizontal gene transfer. The branched tree-like structure represents the evolutionary lineage (geneological tree) of representatives of earth’s major types of life forms. Sometimes genes can be transferred (horizontal gene transfer) between otherwise distantly related species. This is illustrated by bridges forming between branches of the tree, where genes ‘jump’ from one lineage to another. (Image: Barth F. Smets, Ph.D.)

But how do these bacteria actually take up the DNA fragments from their environment? This is not a trivial problem, and it is at this step that lightning may play a surprising role.

Why is the taking up of DNA a problem? Let’s take a quick refresher of the structure of the bacterial cell envelope, which separates the contents of the bacterium from its environment. If you’re already familiar with the phospholipid bilayer, you can skip to the next section.

The Phospholipid Bilayer — a Refresher

Enter the phospholipid molecule. It looks roughly like a bobby pin, with one head and two parallel tails sticking out of it. The phosphate head is a phosphorous atom with oxygen chemically bonded to it. The lipid tails are mainly long chains of carbon and hydrogen. Together the assembly is known as a phospholipid molecule.

Schematic showing how phospholipid molecules and other components fit into a generalized cell membrane. Image source: Mariana Ruiz (Wikimedia Commons)

Now, recall from chemistry classes on solvents that “like dissolves like”. Water molecules are very polar; i.e. they are relatively more positively charged on one side and relatively more negatively charged on the other. Liquids composed of polar molecules such as water can dissolve other substances that are also relatively polar or charged (such as the aforementioned phosphate head). These water soluble substances are hydrophilic (‘water loving’). But water will not effectively dissolve nonpolar molecules, such as fats, or their subunits, lipids. This includes the lipid tails of the phospholipids.

So, when we try to dissolve phospholipids in water, the hydrophobic (‘water fearing’) lipid tails will clump together, apparently ‘seeking escape’ from the water. This results in a central aggregation of lipid tails all pointing toward each other, with the hydrophilic phosphate heads sticking out all around, arranged as if on the surface of a sphere. These aggregate structures look like little round droplets at extremely high magnification.

What happens if we add lots more phospholipids? Think of what happens when you pull on the ends of a zip-locked bag sealed without any air inside. It spread out flatly, forming a plane composed of two adhering sheets. A sea of phosphate heads form the two outer surfaces of this phospholipid sheet, with the lipid tails hidden between them. A flexible sheet is not a stable structure (think about how your unmade bedsheets’ most stable configuration always appears to be a crumpled mess), so the phospholipid sheet warps and bends until the edges end up meeting. Wherever the edges of this thin phospholipid membrane find each other, they ‘heal’ together, completely hiding the lipids from view of the water, and forming a closed bubble, or vesicle.

We now effectively have a bag composed of a two-layered membrane (a phospholipid bilayer), which is the recipe for holding in the components of a cell — yours, your dog’s your plants’, and yes, those of the bacteria in your gut. There are other rivet-like molecules that cells insert within their phospholipid membranes to strengthen them, and plants, fungi and bacteria perform additional strengthening tricks, such as lining their phospholipid cell membranes with walls composed of cellulose, chitin or peptidoglycan, or adding an extra layer of membrane, but we’ll focus on a simplified cell membrane for now.

“You shall not pass”…Mostly

The phospholipid bilayer is an efficient way of keeping the cell’s components in and much of the environment out. Only certain small molecules may pass through this semi-permeable membrane. In fact, it’s so efficient a barrier that it prevents entry to certain components that the cell needs. So a way must be found to allow entry to desired molecules. Certain charged molecules and large molecules find it especially difficult to pass. DNA is one example.

DNA at Cellular Border Crossings

DNA usually needs not cross the bacterial cell membrane, but in the previous post about HGT, we saw how the integration of foreign DNA fragments could substantially increase the fitness of some bacteria by endowing them with new and useful physiological abilities.

Although many bacteria have evolved special systems of receptors and pores (controlled gateways through the cell membrane) to facilitate uptake of foreign DNA fragments, there are other ways to move DNA across the cell membrane. For example, exposure to certain chemicals, such as calcium chloride, followed by a heat shock, can do this.

Electroporation

In 1982, a team of scientists in Germany [1] found that zapping cells with brief pulses of 80,000 volts of electricity can also elicit DNA uptake. Their objective was to find a way to introduce foreign DNA into cells in order to transform them, meaning to induce them to integrate and express foreign genes in a controlled way. Such practice has enormous potential, allowing the investigation of cancer and the development of novel pest-resistant crops, to name just two applications.

This process of using electric fields to induce DNA uptake by cells is called electroporation. It is called this because the electric shock is thought to briefly tear tiny holes (pores) in the cell’s phospholipid bilayer membrane. These pores are only nanometers in size (a nanometer is one millionth of a millimeter), but they provide channels through which the even smaller DNA fragments may enter the cell.

Provided the electric pulse is not too great, the cell’s repair mechanisms promptly seal the ruptures, but often not before foreign DNA and other substances may have entered, if present. Electroporation has been used to transform cells profusely since its discovery.

Naturally Occurring Electroporation

Transformation of bacteria by uptake of foregin DNA (HGT) is not strictly artificial. It’s been going on for billions of years, and we can see its footprints in the shuffled genetic code of different living organisms: species A may possess genes that originally evolved in species B. Despite tha fact that HGT appears to be a complicated, multi-stage process, it must have occurred at high rates in natural populations of bacteria. Therefore, some additional unaccounted-for process appears to have been acting.

In 2001, a team of French scientists (Demanèche et al., 2001) [2] published the experimental results of a brilliant question: could lightning serve this role of enhancing HGT? Over 100 bolts of lightning are discharged worldwide every second (that’s over 3.1 billion bolts per year), making it a potentially relevant force of natural selection, especially considering the abundant energy released in each discharge.

To test their hypothesis, the researchers enlisted the aid of the most common workhorse of microbiology, a microbe that inhabits our own large intestines, Escherichia coli (properly abbreviated as E. coli). The researchers established sterilized soil microcosms in petri dishes and then introduced bacteria to the soil (E. coli is a very versatile microorganism, and with the proper nutrients, it can grow not only in our intestines, but also in a variety of enviroments, including soil). They also sowed the soil with specific fragments of DNA, which, if taken up and expressed by the bacteria, would make them resistant to certain antibiotics in order to reports its uptake. Then came the innovation: they strung conductive wires through the petri dishes and ran electricity through them, zapping the cultures with a jolt roughly equivalent to a bolt of lightning.

Cloud-to-ground lightning. Image source: أسامة الطيب (Wikimedia Commons)

Surviving Lightning

Any of my readers who have survived being hit by lightning will attest to the charring nature of the experience, and will question why the tiny bacteria in these cultures were not crisped by the simulated lightning. To answer this, keep in mind that when lightning hits the ground, the point at ‘ground zero’ receives the most concentrated burst of energy, and then the electricity spreads out across the ground from there, following the labyrinth of conductive paths traced by tiny channels of water and conductive materials lining the pores in the soil. The further away from ground zero that we look, the less of the original energy remains, and the weaker the jolt. Far enough from the point of the strike, even bacteria will survive the release of energy.

Sandrine Demanèche and her coauthors found that these simulated lightning strikes were mild enough for E. coli to survive, but intense enough to induce the bacteria to take up some of the DNA fragments added to the soil: cultures grown from the soil microcosm yielded antibiotic resistant E. coli [2]. They concluded that this constituted electroporation, because in control cultures without the electrical discharge, no antibiotic resistance was observed in the bacteria. The team also found that the electric fields typically created in soil by the buildup of thunderstorms above was not enough to induce electroporation, but that an actual electrical discharge was required to do the job.

What About Native Soil Bacteria?

It’s fascinating that Demanèche’s team showed that some bacteria can be encouraged to take up foreign DNA by exposure to artificial lightning, but what about natural populations of soil bacteria? E. coli is not a typical soil microbe (even though some of its relatives are). Can electroporation occur in actual soil bacterial communities? Hélène Cérémonie and her coauthors [3] subsequently isolated bacteria from natural soil. Then, using a similar apparatus as Demanèche et al. (2001), they found that several strains of these bacteria (belonging mainly to the genus Pseudomonas) were also capable of lightning-induced transformation.

An example of a species in the bacterial genus Pseudomonas (P. aeruginosa). Image source: Centers for Disease Control and Prevention’s Public Health Image Library (Wikimedia Commons)

Of particular interest, the bacteria in this latter experiment were most receptive to lightning-induced DNA uptake while in their stationary growth phase. Bacterial cultues in the lab usually exhibit a J-shaped growth curve (when we plot population versus time), caused by the cells dividing slowly at first (as they adapt to their new environment, often requiring the synthesis of certain enzymes to make use of the food with which they are provided), then speeding up their reproduction when they are maximally ready to use their resources, and finally slowing down again as their resources run out. When their food runs out, their population reaches a plateau (their growth is stationary), and they begin to die as wastes accumulate in their environment. Many bacteria respond to limited resources by halting most of their cellular functions in order to survive bouts of hardship. It is in this kind of dormant state that soil bacteria are often found in nature; ready to take advantage of bursts of resources between long lean times.

It is interesting that the potentially evolution-accelerating phenomenon of lightning-mediated transformation was observed to be most effective in the state in which bacteria are commonly found in nature. It is in this stationary phase that bacteria should derive the greatest benefit from the acquisition of a new physiological ability.

The Bottom Line: Implications for Evolution

What exactly does lightning-mediated transformation imply for evolution of life on earth? It means that a widespread natural power source is available to fuel a process that can accelerate the rate of evolution over what we would expect if life forms did not trade ‘genetic ideas’ by HGT (recall, horizontal gene transfer).

Because of HGT, the whole world (or at least large portions of it) can be seen as an interconnected laboratory where advantageous mutations may be sampled and combined with other advantageous mutations in unrelated species, giving rise to unexpected and otherwise highly unlikely combinations of adaptations and advancements. Lightning may further speed this up.

Without HGT, each independent lineage of organisms would need to ‘invent’ by evolution all of their capabilities to, say, utilize various food and energy sources, that they acquired since their last shared common ancestor. The swapping of genes that constitutes HGT drastically reduces the need for a high incidence of beneficial mutations. In principle, a new beneficial trait need only evolve once in a single species and be shared by many species via HGT.

The other reason that HGT can accelerate evolution is that not all advantageous mutations need be lost upon the death of the microorganism in which they arise, but can be resurrected if the relevant genes are acquired from the remains of the dead microorganism by a living microbe in its vicinity upon exposure to electricity in the soil (as one mechanism of acquisition). This is akin to the discovery and publication of a trove of lost unpublished manuscripts of a great novelst after the novelist’s death.

Thus far, very little research appears to have been done on lightning-mediated transformation, this naturally occurring form of electroporation. It will be interesting to watch whether further research can give us a better understanding of how much and under what conditions this unusual electrical phenomenon is involved in enhancing HGT, and by extension, the rate of evolution in the natural world.

References

1. Neumann E, Schaefer-Ridder M, Wang Y, Hofschneider PH (1982). Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO Journal. 1(7): 841–845. (FREE DOWNLOAD)

2. Demanèche S, Bertolla F, Buret F, Nalin R, Sailland A, Auriol P, Vogel TM, Simonet P. (2001). Laboratory-Scale Evidence for Lightning-Mediated Gene Transfer in Soil. Applied and Environmental Microbiology. 67(8): 3440-3444. (FREE DOWNLOAD)

3. Cérémonie H, Buret F, Simonet P, Vogel TM. (2004). Isolation of lightning-competent soil bacteria. Applied and Environmental Microbiology. 70(10): 6342-6346. (FREE DOWNLOAD)

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