Symbiosis of Termites and the Microbes in their Gut: Digestion of Lignocellulose
The termite gut contains organisms from all three domains of life, Bacteria, Eukarya, and Archaea. (1) There is a great diversity of microbes in the termite gut, many of which are unidentified because of the tiny size of termites and also because of how hard it is to grow them outside of the termite gut. Additionally many of the bacterial species are exclusively grown in termite guts. (2)
Lower Termites versus Higher Termites
There is a distinction between lower termites and higher termites, mentioned throughout many studies of termite guts. Lower termites have many species of bacteria along with protozoa, while higher termites usually just have the bacteria population. (3) The protozoa in the hindguts of the lower termites are important for cellulose digestion, but the termites also can produce cellulase components themselves, as suggested by the existence of higher termite. Both higher and lower termites have the enzymes needed for the first stage of the TCA cycle, but they lack an enzyme capable to convert pyruvate to acetyl CoA or acetate. This suggests the importance of the microbes in the hindgut producing actetate in their process of lignocellulose breakdown. (3)
Many studies on termite gut cellulose digestion have been conducted using carboxymethyl-cellulose as the substrate to measure cellulase activity in termites, but carboxymethyl-cellulose can be hydrolyzed in ways that aren’t specific to digestion in the gut, such as activity in salivary glands. Therefore, Tokuda et. al looked at the digestion of crystalline cellulose in termites and compared the different types of cellulase activity. (4) Their investigation found that most cellulose digestion occurs in the hindgut for termites that have flagellates, and the midgut for termites without the presence of flagellates in their gut. They also describe evidence of hingdgut bacteria containing ‘cellulosome’ complexes, explaining how they digest the food substrates with their cell wall by surrounding the food substrates. (4)
Acetogenesis and Methanogenesis The termite gut is not a simple anoxic environment, as it actually has a complex structure of different microenivronments. (5) As opposed to the bovine rumen and human colon, which only have anaerobic bacteria, the termite gut has the presence of oxygen and this effects the processes that occur. (6) Part of what makes certain termite guts so interesting is the preference the bacteria have for acetogenesis over methanogenesis. (3) Termites that have fungi in their gut and feed on soil seem to perform methanogenesis more often than acetogenesis, but the higher termites that just feed on wood are the ones that prefer acetogenesis. (6) The connection between the wood feeding termites and acetogenesis is still unknown.
It is also unclear how higher termites are able to degrade the lignin and get to the cellulose, as lower termites do this with the fungi in their gut. It is suggested that higher termites loosen the lignin in their salivary glands (2). Additionally, the mechanisms of these symbioses are still mysterious, but research is turning to techniques such as genomics and metaproteomics in order to try to understand it better. The diversity of the bacterial species still creates difficulty in analysis. Nevertheless, Treponema from the phylum Spirochaetes has been identified as the predominant bacterial group in both higher and lower termites, and an uncultured lineage from the phylum Fibrobaceres has also been identified as a dominant group in higher termites. Both these bacterial groups are generally considered to be very important to lignocellulose hydrolysis and therefore digestion in termites (2). Burnum et. al used metaproteomics to examine the hindgut of Nasutitermes corniger, a higher termite, and found almost a quarter of the 886 proteins they identified were enzymes and 36 were glycoside hydrolases. (7)
Efforts to identify more of the bacteria in the termite guts would be helpful, and genomics seem to be a good route in that it is impossible to culture some of these bacterias outside of the unique environment of the termite gut. This will still be difficult as many of the species are specific to termite guts. There is also room for more research on degradation of lignin and cellulose, and the differences between lower and higher termites in the way that they perform these actions, as well as the differences in preferences for acetogenesis and methanogenesis.
(2) Hongoh, Yuichi. “Toward the Functional Analysis of Uncultivable, Symbiotic Microorganisms in the Termite Gut.” Cellular and Molecular Life Sciences 68, no. 8 (April 2011): 1311–1325. doi:10.1007/s00018-011-0648-z.
(3) Breznak, Ja, and A. Brune. “Role of Microorganisms in the Digestion of Lignocellulose by Termites.” Annual Review of Entomology 39 (1994): 453–487. doi:10.1146/annurev.en.39.010194.002321.
(4) Tokuda, G., N. Lo, and H. Watanabe. “Marked Variations in Patterns of Cellulase Activity Against Crystalline- Vs. Carboxymethyl-cellulose in the Digestive Systems of Diverse, Wood-feeding Termites.” Physiological Entomology 30, no. 4 (December 2005): 372–380. doi:10.1111/j.1365-3032.2005.00473.x.
(5) Ohkuma, M. “Termite Symbiotic Systems: Efficient Bio-recycling of Lignocellulose.” Applied Microbiology and Biotechnology 61, no. 1 (March 2003): 1–9. doi:10.1007/s00253-002-1189-z.
(6) Brune, A. “Termite Guts: The World’s Smallest Bioreactors.” Trends in Biotechnology 16, no. 1 (January 1998): 16–21. doi:10.1016/S0167-7799(97)01151-7.
(7) Burnum KE, Callister SJ, Nicora CD, Purvine SO, Hugenholtz P, Warnecke F, Scheffrahn RH, Smith RD, Lipton MS (2011) Proteome insights into the symbiotic relationship between a captive colony of Nasutitermes corniger and its hindgut microbiome. ISME J 5:161–164.
Edited by Diana McDonnell, a student of Nora Sullivan in BIOL168L (Microbiology) in The Keck Science Department of the Claremont Colleges Spring 2014.