by Elio
Figure 1. Pleurotus dryinus on a tree. Source
I admit to not having paid much attention to the mechanisms that plants and animals use to stand up straight, or, in the case of plants, also to descend into the soil. Yet, on reflection, the skill in detecting the effect of gravity, now called gravitropism, the older term being geotropism, is essential for life. Perhaps my neglect is due to this topic not being much of a microbial concern (although, in fact, what isn't?). However, as we will see, some microbes do know the way up and the way down.
Fungi and People
I will post here pieces that others have written on the subject (more to recognize their expertise than to reveal my laziness). This from an article called "Which way is up? Mushrooms Gravitropism" by my friend Britt Bunyard in a fabulous magazine called Fungi, regarding mushrooms and humans, he says: "Monzer (1996, 1995) more recently proposed a …. simple explanation for how gravitational sensing is accomplished in fungi. And that it's very similar to the system of otolith organs (technically the utricle and saccule) of humans. Within all of us, deep inside our inner ear, there are organs that contain a liquid filled with tiny stone-like particles called otoliths or otoconia (they really are stony, essentially made of limestone and a protein) that rub against tiny hairs that line the inside of the otolith organ. Most of the time, the particles are uniformly settled telling us which way is down. If you are spun around or shaken like a snow globe, the particles move all about giving you a feeling of disorientation, even dizziness.
Figure 2. An Amanita suballiacea mushroom repositioning after being placed horizontally overnight. Source: Britt Bunyard.
Now for more: "And this, Monzer has concluded, is similar to how fungal cells sense gravity. Within hyphal cells, nuclei act as fungal otoliths; their sedimentation within the cells in response to the direction of the gravitational forces tells the fungal cells which way is up. The nuclei are enmeshed in proteinaceous actin filaments that make up the cell's internal "skeleton" (the cytoskeleton). As these nuclei settle, they tug on actin filaments, which in turn tug on the cell walls at their points of attachment. This tension triggers cellular changes in response to gravity, and on the side of the cell feeling gravity's force, microvesicles begin to fill and expand, vacuoles expand, and the entire process causes the expansion of hyphal cells. The net result is that the mushroom stem bends away from the gravitational sensation." See here for a fine piece by Phil Pinzone on gravitropism in the tree-growing mushroom Flammulina velutipes.
Plants
How about plants? The Wikipedia says: "Gravitropism (also known as geotropism) is a turning or growth movement by a plant or fungus in response to gravity. It is a general feature of all higher and many lower plants as well as other organisms. Charles Darwin was one of the first to scientifically document that roots show positive gravitropism and stems show negative gravitropism. That is, roots grow in the direction of gravitational pull (i.e., downward) and stems grow in the opposite direction (i.e., upwards). This behavior can be easily demonstrated with any potted plant. When laid onto its side, the growing parts of the stem begin to display negative gravitropism, growing (biologists say, turning; see tropism) upwards."
How do plants manage these tricks? Consider the behavior of the roots. At the tip of the roots is a subset of cells that contain special organelles called amyloplasts (more about them later) that are involved in perceiving gravity. These amyloplasts are denser than the cytoplasm and thus gravity makes them fall down to the bottom of the cells. These structures, called statoliths, are encircled by a web of actin, which is thought to activate carriers of the plant growth hormones, the auxins. The changed local concentration of auxin leads to differential growth of root tissues, which leads to the turning of the root. Statoliths are also found in the shoots of plants, where they are involved in their turning upward, in the direction opposite that of the gravity stimulus. Thus, roots and shoots, dissimilar though they are, use a common mechanism to sense gravity. See here for a review and here for a nice blog piece on this topic.
Figure 3. Winogradsky column used at the Ecosystems Center, Marine Biological Laboratory at Woods Hole. By Joseph Vallino. Source
Now about the amyloplasts. The Wikipedia says: "Amyloplasts are non-pigmented organelles found in some plant cells. They are responsible for the synthesis and storage of starch granules. Amyloplasts also convert this starch back into sugar when the plant needs energy. Large numbers of amyloplasts can be found in fruit and in underground storage tissues of some plants, such as in potato tubers. Amyloplasts and chloroplasts are closely related, and amyloplasts can turn into chloroplasts; this is for instance observed when potato tubers are exposed to light and turn green." Notice that the amyloplasts likely originated by the endosymbiosis of a bacterium, thus we are back in the microbial world.
Bacteria
Certain bacteria and archaea also know which way is up, but, best I can tell, none use gravitropism for this purpose (the huge Achromatium bacteria probably being the notable exception; there are always exceptions in biology). This is not surprising, given that the small dimensions of most microbial cells do not allow for significant differences in the force of gravity between the two ends of a rod-shaped bacterium. Rather, many microbes sense chemical cues in the environment such as gradients in the concentration of oxygen, sulfides, and any of a large variety of other substrates. Phototaxis, (positive and negative – photophobia) also happen, and so do reactions to temperature gradients, toxic chemicals, and untold other factors. These responses often result in the layering of a given species in a water column or in soils. Clear examples in the lab are Winogradsky columns (discussed here).
Figure 4. Thioploca mats on the continental shelf off the coast of Chile swaying more or less upright in the current. Source
Among the most intricate examples of layering are sulfide-oxidizing bacteria that obtain their energy from oxidizing sulfides and use nitrate as the electron acceptor. In the shallow waters off the coast of Chile, such bacteria, in the genus Thioploca, make up gigantic mats. To quote from this blog, "sulfides are abundant in the sediment, nitrates in the water column. How to bring the two together? Thioplocas solve the problem by making tubular sheaths that stick out from the ocean's sediment. These sheaths can be as long as 15 cm. Inside them, filaments of the organisms glide up and down, gathering sulfides below and nitrate above. Thioplocas chemotax towards nitrate. They absorb it and transport it downwards, to where the sulfide is abundant, at speeds of about one centimeter per hour. In other words, thioplocas take an elevator to work." The topic of gravitropism in bacteria had an early historical mishap. It took the great Martinus Beijerinck to sort it out.
Figure 5. Bundle of Thioploca araucae extending out of their sheath. The appearance of a braid is seen where the filaments cross over one another, hence the name Thioploca, 'sulfur braid.' Source
Among other examples of how bacteria travel along vertical axes, the most exciting perhaps are the magnetotactic bacteria. Again, the Wikipedia says: "To perform this task, these bacteria have organelles called magnetosomes that contain magnetic crystals. The biological phenomenon of microorganisms tending to move in response to the environment's magnetic characteristics is known as magnetotaxis (although this term is misleading in that every other application of the term taxis involves a stimulus-response mechanism). In contrast to the magnetoreception of animals, the bacteria contain fixed magnets that force the bacteria into alignment – even dead cells align, just like a compass needle The alignment is believed to aid these organisms in reaching regions of optimal oxygen concentration."
In Conclusion
So here you have it, when it comes to gravitropism, animals, plants, and mushrooms all tell which way is up or down using tiny weights: small pebbles, organelles, and nuclei, respectively. Bacteria, when facing up-and-down related challenges, use external signals other than gravity, mainly by sensing chemical gradients, magnetism, and light. Chaque'un a son goût, but in Biology each taste works perfectly well to respond to a particular environmental trial. Vive la Vie!
