One of my colleagues who does research on the microbes that live in the hindguts of lower termites once remarked that interesting organisms can be found in the most unusual of places. And the lower termite hindgut, by almost anyone’s estimation, is certainly an unusual place. It is also a fascinating place for anyone interested in biology, ecology, evolution, biochemistry, or beautiful natural forms and patterns.
Since my undergraduate days in the early 90s, I have had a deep interest in the tree of life, especially eukaryote phylogeny. After a Ph.D. in Plant Biology at U.C. Davis, I headed off to the University of British Columbia to work in Patrick Keeling's lab to pursue these interests. Anyone who has this peculiar obsession (actually, I think it's peculiar not to have this obsession!) knows that the eukaryote tree comprises mostly protists, and they arguably encompass greater structural, cell biological, biochemical, (and certainly evolutionary!) diversity than all plants, animals, and fungi combined.
In Patrick's lab I developed methods for SEM and TEM imaging of these microbes to investigate their phenotypic character evolution, functional morphology, and symbioses with bacteria in the light of molecular phylogenetic data. In addition to a number of publications (with more to come) and talks in Russia, Germany, Norway, etc. my electron micrographs have been featured on numerous journal covers, textbooks, and invited artistic presentations in Canada and Germany.
On 17 April 2013, a collection of 11 of my scanning electron micrographs of lower termite hindgut protists and their bacterial symbionts will go on permanent exhibit at the Exploratorium museum as they open their new $300 million dollar location on Pier 15 in San Francisco. This is a large (12' x 4') installation in the East Gallery (overlooking the bay):
The waterfront location, the architecture, the exhibits, and sustainable technology (rooftop solar panels, etc) are all amazing, and I encourage anyone with any interest in science/biology, art, experimentation, tinkering, and beautiful views to come out for a visit. For more information on the exhibit, the organisms, additional images and other resources (including a blog!), please visit my website at: KevinJCarpenter.com
As for the organisms...
The hindgut of wood-feeding lower termites--comprising approximately 1000 species (out of a total of several thousand species of termites)--is densely packed with symbiotic protozoa (protists), many of which engulf and enzymatically degrade wood fragments making their way to the termite hindgut. Far from being parasites, numerous studies have shown this to be a mutualsitic symbiosis, by demonstrating that the termites will starve and die if deprived of their protist symbionts. The symbiosis between lower termites and their hindgut protists is one of the longest-studied and best-known examples of microbial symbiosis, dating back nearly a century and a half to the work by Joseph Leidy and others.
The protists are anaerobic flagellates belonging to Parabasalia or Oxymonadida--members of the Excavate eukaryotic supergroup (also including euglenids, trypanosomes, Giardia, and heterolobosean amoebas). There are numerous odd, interesting, beautiful, and instructive things about these protists.
First, they are endemic to termite hindguts and are found nowhere else. Most of the protist species are found only in association with a single species of termite. The termites pass their hindgut biota from adult to newly hatched nymphs and moulting adult termites (which lose their hindgut contents) via specialized feeding behaviors. It is thought that termites evolved social behavior and caste differentiation from their cockroach ancestors partly to pass hindgut protists between individuals.
Second, many of the protist species and lineages have attained large size (up to 300 microns in length), and enormous structural complexity. Some of the protists are estimated to bear up to 50,000 flagella, each associated with specialized proteinaceous structures (kinetosomes, parabasal fibers) inside the cell. Hence, these are likely among the most structurally complex cells known to science. This is in marked contrast to other symbiotic protist lineages such as microsporidia, apicomplexans, and the coral reef symbiont Cyanidioschyzon, all of which have undergone extreme structural reduction. When looking at these termite gut protists in all of their great structural complexity, dwarfing their numerous bacterial surface symbionts, it is is kind of mind-boggling in a sense to realize that this is a unicellular organism!
Third, the cell biology of these organisms is so different from what is taught in undergraduate cell biology (which is really mammalian, or at best, metazoan cell biology), that it may (hopefully) cause one to reflect on how truly diverse and unknown our biosphere really is. As one example of this, in parabasalid protists, mitochondria have become drastically reduced structurally (loss of cristae), functionally (loss of oxidative metabolism/Krebs cycle), and genomically, and their only known function is the conversion of pyruvate to acetate, with the production of hydrogen gas as a waste product. Hence, these relict mitochondria are called hydrogensomes. The oxymonads are among the least understood group of eukaryotes, and for many species it is unknown what they eat (some of the smaller species apparently do not eat wood), how they reproduce, or how they metabolize their food. Some even have a non-canonical genetic code.
The sitution becomes even more complex when we consider the bacteria in lower termite hindgut systems. In light of their importance in the human and other gut microbiomes, it is no surprise that the termite gut is swarming with innumerable bacteria, many of which are likely found only in one species of termite. What is surprising is that an estimated 90% of all bacterial cells in these systems live either on the surface of, or inside of a protist, and are not free-swimming. One study estimates that the large protist Pseudotrichonympha harbors about 100,000 bacterial cells. Microscopy reveals specialized attachment structures that help the bacteria anchor to the protist surface. Our research shows that the large protist Barbulanympha has not only vast numbers of rod-shaped bacteria on its cell surface and interior, but also bacteria surrounding extruded strands of cytoplasm. This is possibly a mechanism to increase the area available for exchange of nutrients.
Recent research on bacteria symbiotic with termite gut protists suggests that they are important in nitrogen metabolism--both in nitrogen fixation and synthesis of vitamins and amino acids. They are thought to transfer these compounds to their host protist (and to the termite) in return for sugars derived from breakdown of wood.
Just as the protists are generally endemic to a single species of termite, in many cases, bacteria found in symbiotic association with the protists are endemic to a single species of protist. Given this close, three-way association between termite, protist, and bacteria, it is perhaps not surprising that evidence of triplex speciation has been found in these organisms: both the bacteria and their protist hosts speciate in tandem in response to termite speciation events. This is one of only a handful of putative cases of triplex speciation.
The symbiosis between termites and protists is actually also present in a species of wood-feeding cockroach--Cryptocercus punctulatus. C. punctulatus is actually more closely related to termites than to other cockroaches (cockroaches are paraphyletic). It is believed that symbiotic protists were present in the hindgut of the ancestor of C. punctulatus and modern termites, which likely lived over 100 million years ago.
Thus, I consider these termite hindgut systems to be among the most unusual, beautiful, and instructive natural laboratories in evolution and ecology known to science. Nature indeed seems to enjoy tinkering, and in that spirit, I think this is well suited to representation in a place like the Exploratorium!
A few references (copied straight out of one of my manuscripts!) for those interested:
Brune, A. & Ohkuma, M. (2011). Role of the termite gut microbiota in symbiotic digestion. In Biology of Termites: A Modern Synthesis, Bignell, D. E., Roisin, Y. and Lo, N. (Eds.), pp. 439-475. London: Springer.
Carpenter, K.J., Chow, L. & Keeling, P.J. (2009). Morphology, phylogeny, and diversity of Trichonympha (Parabasalia: Hypermastigida) of the wood-feeding cockroach Cryptocercus punctulatus. J Eukaryot Microbiol 56(4), 305-313.
Carpenter, K.J., Horak, A., Chow, L. & Keeling, P.J. (2011). Symbiosis, Morphology, and Phylogeny of Hoplonymphidae (Parabasalia) of the Wood-Feeding Roach Cryptocercus punctulatus. Journal of Eukaryotic Microbiology 58(5), 426-436.
Carpenter, K.J., Horak, A. & Keeling, P.J. (2010). Phylogenetic position and morphology of spirotrichosomidae (parabasalia): new evidence from Leptospironympha of Cryptocercus punctulatus. Protist 161(1), 122-132.
Carpenter, K.J. & Keeling, P.J. (2007). Morphology and phylogenetic position of Eucomonympha imla (Parabasalia: Hypermastigida). J Eukaryot Microbiol 54(4), 325-332.
Carpenter, K.J., Waller, R.F. & Keeling, P.J. (2008). Surface morphology of Saccinobaculus (Oxymonadida): implications for character evolution and function in oxymonads. Protist 159(2), 209-221.
Hongoh, Y., Sharma, V.K., Prakash, T., Noda, S., Taylor, T.D., Kudo, T., Sakaki, Y., Toyoda, A., Hattori, M. & Ohkuma, M. (2008a). Complete genome of the uncultured Termite Group 1 bacteria in a single host protist cell. Proc Natl Acad Sci U S A 105(14), 5555-5560.
Hongoh, Y., Sharma, V.K., Prakash, T., Noda, S., Toh, H., Taylor, T.D., Kudo, T., Sakaki, Y., Toyoda, A., Hattori, M. & Ohkuma, M. (2008b). Genome of an endosymbiont coupling N2 fixation to cellulolysis within protist cells in termite gut. Science 322(5904), 1108-1109.
Ohkuma, M. & Brune, A. (2011). Diversity, structure, and evolution of the termite gut microbial community. In Biology of Termites: A Modern Synthesis, Bignell, D. E., Roisin, Y. and Lo, N. (Eds.), pp. 413-438. London: Springer.
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