Sunday, December 4, 2011

A Russian Doll of Symbiosis

By Chelsey Van Drisse

Symbiosis is a phenomenon in nature defined as the close or direct interaction of two separate species of organisms living together. Some symbiotic relationships are essential to the survival of both organisms. Other symbiotic relationships are facultative, meaning the two organisms can live together but it is not completely necessary for the survival of both parties.  A type of symbiosis known as endosymbiosis is where an organism lives within the body or cells of another organism.
The most prevalent example of endosymbiosis is the origination of mitochondria or chloroplasts in eukaryotic cells. The theory is that mitochondria or chloroplasts evolved from certain bacteria that were engulfed by other bacterial cells. This event is generally supported by the fact that mitochondria in our cells have their own genome, which may be the remnants of their bacterial counterparts. If one were to create a list of symbionts in this world, the list would be never ending. I suggest to anyone in doubt of the high prevalence of symbiosis to look out your window and write down every organism you see. Chances are most, if not all, are products of some symbiotic relationship. In fact, you don’t even have to look out the window, just look at yourself. Thousands of bacterial, archaea or fungal species live within you, digesting your food or preventing the growth of other harmful species.
Some of the most interesting symbionts exist in unexpected habitats, living with the most unexpected of species. A prime example of a complex symbiotic relationship is the species Mixotricha paradoxa from the order Trichomonadida. Its discovery occurred in 1933 by Sutherland and was characterized by long anterior flagella and a complete covering of short cilia (4). This protozoan organism lives within the termite species, Mastotermes darwiniensis. M. paradoxa plays a crucial role in digesting cellulose in the termite gut, which is a major component of the wood termites eat. The cellulose is digested to sugars and acetate that eventually produce methane, hydrogen and carbon dioxide (6). Without this symbiotic relationship, the termite would die because it cannot digest the cellulose on its own (5).
Figure 1. Microscopic image
of M. paradoxa
Although the symbiosis of M. paradoxa with its termite host is fascinating in itself, there is another layer of symbiosis to this system. While M. paradoxa digests the cellulose from wood for the termite, M. paradoxa has its own symbionts living and thriving on the surface and inside itself. Looking at a picture of M. paradoxa, at first glance (Figure 1) it may appear that the protozoan has many cilia that are used for locomotion. This misconception was the accepted mechanism of M. paradoxa until Cleveland and Grimstone described the actual nature and role of these “cilia” in 1964. The authors found these were not actually cilia but the spirochete, Treponema spirochetes, covering the surface as a dense carpet, providing locomotion to the cell. M. paradoxa, use their four anterior flagella for steering while the spirochetes move the cell forward. Together, the two organisms work together to maintain both direction and movement throughout the termite gut. This symbiosis is actually a unique example of movement symbiosis between eukaryotic and prokaryotic microorganisms. 
It is still unknown how this interesting phenomenon occurs between the two different species. It has yet to be discovered how the spirochetes and M. paradoxa communicate and coordinate the direction of movement. It would seem that flagella and spirochetes should automatically synchronize their movement when undulating in close proximity (3).  This theory was supported when living and thriving M. paradoxa had spirochetes that undulated vigorously and were well coordinated, where as dying M. paradoxa the spirochetes cease to undulated in a coordinated manner (1). The difficulty in studying this process comes from the inability to cultivate M. paradoxa or its spirochetes symbionts.
It has been proposed that in addition to providing locomotion to the cell, the spirochetes must serve some other function in this symbiosis. Remember earlier, how it was stated that the sugars that M. paradoxa produced from digesting cellulose eventually produce hydrogen, acetate and carbon dioxide? It is predicted that it is actually the spirochetes acting as methanogens, catalyzing the synthesis of acetate from the hydrogen and carbon dioxide. This acetate formed by both of these microbes is a major carbon and energy source to the termite. The oxidation of this acetate by the termite supports 100% of its respiration requirements (2). Not only are these spirochetes providing locomotion to the M. paradoxa cell, they are also providing acetate as an energy source to the termite.
Figure 2. Cell surface of M. paradoxa.(s) represents spirochetes and (b)
represents rod-shaped bacteria.
Image from Cleveland & Grimstone, 1964
That is a lot of symbiosis to piece together, however, it does not stop there. There is not only one more symbiont in M. paradoxa but two more bacterial species that live in symbiosis with this protozoan. In addition to the spirochetes found on M. paradoxa, abundant epibiotic rod-shaped bacteria live on the surface of the protozoan (Figure 2). The total number of these rod-shaped bacteria per cell is of the order of 100,000. 16S rDNA analysis has shown that these bacteria are related to the Bacteroides genus. It is hypothesized that these rod-shaped bacteria assist in the digestion of cellulose by M. paradoxa but it has not been studied in detail (3). The last known symbiont in this diverse symbiosis is a third bacterial species that lives inside of the cell. These spherical bacteria are hypothesized to work with hydrogenosomes to act as mitochondria for M. paradoxa, which is an organelle that M. paradoxa lacks (1).
Symbiosis is indeed a complicated and complex interaction between multiple species. The evolution of many current organisms today has occurred due to the basis of symbiosis. Many times symbiosis is essential to both organisms, as in the case of M. darwiniensis and its symbiont M. paradoxa. Without M. paradoxa, M. darwiniensis would not live and vice versa. It can be seen in the example of M. paradoxa that symbiosis may be much more in depth than what a first glance may provide. M. paradoxa is exceptional due to the fact that it has three to four microorganisms living in or on it and that some of them play an obvious functional role in the life of their host (1). Although some of the microorganisms such as the rod-shaped bacteria on M. paradoxa have not been proved to play any significant role, it is difficult to believe that these bacteria do not serve some function to their host. The symbiosis of M. darwiniensis, M. paradoxa, the spirochetes and the bacterial counterparts is a unique and fascinating example of how various species live together to survive and function successfully with each other.

1.        Cleveland, L. R., and A. V. Grimstone. 2011. The fine structure of the flagellate Mixotricha paradoxa and its associated micro-organisms. Society 159:668-686.
2.        Leadbetter, J. R. 1999. Acetogenesis from H2 Plus CO2 by Spirochetes from Termite Guts. Science 283:686-689.
3.        Overmann, J. 2006. Molecular basis of symbiosis. Springer Berlin / Heidelberg, Berlin, Germany.
4.        Sutherland, J. L. 1933. Protozoa from Australian termites. Q J Microsc Sci 76:145-163.
5.        Veivers, P. C., R. W. O’Brien, and M. Slaytor. 1983. Selective defaunation of Mastotermes darwiniensis and its effect on cellulose and starch metabolism. Insect Biochemistry 13:95-101.
6.        Wier, A., M. Dolan, D. Grimaldi, R. Guerrero, J. Wagensberg, and L. Margulis. 2002. Spirochete and protist symbionts of a termite ( Mastotermes electrodominicus) in Miocene amber. Image (Rochester, N.Y.) 99:18-21. 


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