Inside story

8 November 2013 by Malcolm Campbell, posted in Biology

Everybody has a secret world inside of them. I mean everybody. All of the people in the whole world, I mean everybody — no matter how dull and boring they are on the outside. Inside them they've all got unimaginable, magnificent, wonderful, stupid, amazing worlds... Not just one world. Hundreds of them. Thousands, maybe.” From The Sandman: A Game Of You by Neil Gaiman (1960- )

Despite the fact that they are shedding leaves, the oaks remain regal. Their leaves are acquiring their autumnal deep bronze hue, with hints of amber and ochre. A grove of oaks create a gilded ceiling overhead – the arched sanctuary of a natural cathedral. Together they form a space ideal for reflection – an opportunity for mindfulness.

It’s intriguing how the outward beauty of the oaks intersects with inward reflection. Both are shaped by similar mechanisms. Both are shaped by the workings of tiny bubbles.

All plants and animals, including humans, share a fundamental property – we are all composed of cells. Cells may vary in their details, contingent on the roles they play, they all share in common the fact that they are bags of molecules bound in an envelope called the cell membrane.

The cell membrane, also known as the plasma membrane, can be thought of as making a sack that holds the cellular constituents, the cytoplasm. The plasma membrane functions as a barrier between the cytoplasm and the external environment. As such, it functions as a cell’s interface with external stimuli, as well as a gatekeeper for the flow of chemicals into and out of the cell. In keeping with this, while the plasma membrane is selectively permeable to some chemicals, it also contains sensors and transporters that more actively transmit information and molecules into and out of the cell. In this way, the plasma membrane defines the somewhat independent nature of each cell.

The plasma membrane is largely composed of lipids. Lipids are unique molecules that have two distinct ends. One end if the lipid molecule that has a natural affinity to water-rich environments - the hydrophilic head. The other end is repelled by water, and is said to be the hydrophobic tail. On account of this unique chemistry, when many lipid molecules find themselves together in a water-rich environment they spontaneously form a novel structures to contend with the water. The lipids make little bubbles – vesicles. The vesicles arise due to the fact that the lipids organise themselves into a bilayer membrane. In the bilayer, lipids align with each other so that all of their water-loving heads point into the water, and all of their water-hating tails interact with each other, tail-to-tail. The bilayer is organised thus: head-to-tail-to-tail-to head. Each lipid bilayer forms a sphere, with water on the outside and the inside – making a little bubble. Cells are like large versions of these lipid bilayer-bounded bubbles. 

The plasma membrane is not merely a lipid-bilayer. Other molecules, specifically, different proteins are embedded within the membrane. These proteins, which vary from cell to cell, are what enable the plasma membrane to go about the business of controlling the flux of chemicals and the flow of signals into and out of the cell.

The plasma membrane is a remarkable innovation, but it is not without its problems.

Reflecting on the splendour of the gilded arches of an oak cathedral points to two significant problems with the plasma membrane.

The first problem is one that underlies the gilded beauty of the oak leaves. It is a problem of toxicity.

The second problem is one that underlies our personal reflection. It is a problem of transmitting information.

The bronze hue of oak leaves is attributable to the particular light-absorbing qualities of a special group of molecules known as tannins. Tannins are carbon-rich polymers that plants make as a defence mechanism. Oak leaves are a rich source of tannins. In fact, this class of compounds garnered their name from the old German word for oak, tannan.

There is simultaneously a great advantage and a great disadvantage for a plant that makes tannins. This paradox is revealed the process that bears their name, hide tanning. The process of hide tanning makes use of the tannins extracted from sources rich in these compounds, like oak leaves. In our past, our forebears recognised that the compounds extracted from both oak leaves and bark made animal hides more pliable, and, crucially, more resistant to degradation.

We now know that this is because tannins bind to proteins, particularly collagen, that make up animal hides. When tannins bind collagen proteins, they make them more water repellent, and less amenable to microbial degradation. These features of tannins are what make them such a boon for plants. Plant material that contains tannins is not susceptible to degradation – making it an unpalatable foodstuff for animals and microbes alike. As such, tannins are effective deterrents to animal feeding and microbial disease.

Of course, making a compound that destroys protein function is a double-edged sword. It’s all fine and well when tannins are destroying the functions of proteins of the plant’s mortal enemies. It is another matter altogether when the tannins are destroying the functions of the plant’s own proteins.

And here is the problem.

How does the plant make a compound that is non-discriminatory in its mode of action? When it can just as easily destroy the proteins of the very organism that made them? How do plant cells go about the rest of their normal business when they are simultaneously making a compound that will undermine this business?

Here is where the tiny bubbles come into play. Just as the cell is bound by a plasma membrane, the plant cell is able to partition activities within the cell by hosting other membrane-bound structures inside the cell. Plant cells have many membrane-bound structures, known as organelles, within each cell. The nucleus, where the DNA resides, is one such structure. The vacuole, which functions as a giant store house within the cell, is another. Plants also contain an organelle that is unique to plant cells, the chloroplast.

The chloroplast is a spectacular organelle that is responsible for the business of photosynthesis. It is here where the energy from sunlight is harvested and used to make sugars using carbon dioxide and water as raw materials. The chloroplast is also home to a number of other chemical reactions, many of which are involved in the synthesis of molecules that the plant cell will use for energy, architecture, and, it would appear, defence.

Recently, Geneviève Conéjéro and colleagues in Montpellier, France, found that tannins are likely made within the chloroplast. Now, as is the case with the cell, if the chloroplast was to make tannins, its proteins would similarly be damaged by the tannins. Chloroplasts contend with this by building the tannins inside even smaller bubbles – tiny vesicles. These vesicles, dubbed tannosomes, are little tannin parcels. As soon as the tannins are synthesised, they are packaged up in the tannosome.

Eventually, the tannosome is transported out of the chloroplast, and shunted into the vacuole, where tannins can be stored out of harm’s way, and without creating harm. Tannosomes thereby become tiny stores of chemical weaponry. Contained within the tannosomes, warehoused in the vacuole, the tannins cannot wreak havoc within the cell, but, when the cell is ruptured during animal feeding, or through microbial attack, they are unleashed to fulfil their deterrent dirty work.

Thus, the toxicity problem arising from the gilded beauty of oak leaves is dispatched by merely using tiny bubbles.

Our capacity to perceive and marvel at this, a problem of information transmission, is similarly addressed by tiny bubbles.

We transmit information around our bodies, and store it in our brains, through the activity of specialised cells called neurons. We know that transmission can occur at an incredible rate, with memories being created, recalled, and acted upon in an instant. This requires some remarkable communication between cells.

Some of this communication occurs on the basis of purely chemical signalling – the release a compound from one neuron, and its perception by another neuron. Compounds that function in this capacity are known as neurotransmitters. The challenge with this kind of cell-to-cell signalling is to make it fast…and specific. If the cell were release neurotransmitters by diffusion, all surrounding cells would receive the signal,  and they in turn would release diffused neurotransmitter. The net result would be a something akin to a “blob” of signalling – there would be no directionality to enable the rapid transmission that is necessary. What’s more, if the neurotransmitter is merely diffusing freely within the cell, there is also the problem of the cell being able to discern signal derived from neighbours, versus itself.

Cells contend with this problem by enlisting vesicles in the process of information transmission. Within cells, neurotransmitters are sequestered in high concentrations inside membrane-bound vesicles. In doing so, the cell now has a means by which to contain its own signals.

In order to release the signals in a highly targeted, direction, and specific fashion, the cells directs the neurotransmitter-laden vesicles to specific sites at the plasma membrane. These sites are places where the plasma membranes of two neurons are in close proximity. Such sites are known as synapses.

When a neuron is stimulated by a neurotransmitter, it relays the signal to other neurons by directing its neurotransmitter-laden vesicles to the synapse sites. When the vesicles reach the plasma membrane, their membranes fuse with the plasma membrane, such that their cargo is dumped into synaptic gap between the neurons. The downstream neuron perceives the highly localised neurotransmitter via protein receptors embedded in its plasma membrane in a region known as the post-synaptic density. It then carries the same process forward to other neurons to which it is connected.

There are a number of elements of this process that are themselves worthy of marvel. The targeting of the vesicles to the plasma membrane at the synapse is exquisitely controlled. Each vesicle, known as a neuronal porosome, is itself almost unbelievably miniscule, just 15 nm in size. Despite this, the membrane surrounding the neuronal porosome contain a remarkable array of 40 proteins. Collectively, they assist in the mediation of the process – sequestering neurotransmitter, travelling to the plasma membrane at the appropriate time, and then docking and fusing with it to release the neurotransmitter.

The shared use of tiny bubbles, the real “inside story”, is the truly remarkable feature of the interface between the bronze canopy of the oak grove, and the reflective process it invokes. It speaks to the ancient nature of vesicles, and how their fundamental structure has been utilised time and again for incredibly varied purposes. They are like the matryoshka doll, an embedded replicate that serves a comparable enveloping role. Evolution has used vesicles like a multipurpose tool, employing it in different contexts to accomplish not only analogous roles, but, equally, incredibly divergent roles.

As a species, we frequently attempt to solve new problems by searching for entirely new solutions. If pondering our own existence within the inspiring setting of an autumn oak grove reminds of anything, it’s that old solutions are still monumentally useful. They can be reconfigured, refitted, renovated – fashioned to provide as elegant a fix to new problems as any novelty we might envision.

Images: All photographs by Malcolm M. Campbell.

References:

Brillouet JM, Romieu,C., Schoefs B, Solymosi K, Cheynie V, Fulcrand H, & Conéjéro G (2013) The tannosome is an organelle forming condensed tannins in the chlorophyllous organs of Tracheophyta. Annals of Botany 112: 1003-1014

Cho JW, Lee JS & Jena BP (2010) Conformation states of the neuronal porosome complex. Cell Biology International 34: 1129-1132

Kovari LC, Brunzelle JS, Lewis KT, Cho WJ, Lee JS, Taatjes DJ & Jena BP (2013) X-Ray Solution Structure of the Native Neuronal Porosome-Synaptic Vesicle Complex: Implication in Neurotransmitter Release. Micron. (in press)

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