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Symbiotic digestion of lignocellulose in termite guts

Key Points

  • The symbiotic digestion of lignocellulose by termites involves the sequential activities of the host and its gut microbiota.

  • The hindgut of termites is a microbial bioreactor that efficiently converts polymeric substrates to acetate and variable amounts of methane, with hydrogen as a central intermediate. The metabolic processes are strongly affected by the influx of oxygen into the gut periphery.

  • Whereas primitive termites digest wood with the help of cellulolytic protists, the more advanced lineages have an entirely prokaryotic gut microbiota. Major shifts in the gut microbial community seem to reflect changes in digestive strategies and diet.

  • The majority of termites are soil-feeding and mineralize peptides and other nitrogen-rich humus components. The consequences of the microbial processes in their highly alkaline guts for nitrogen cycling in tropical soils and greenhouse gas production are only scarcely investigated.

  • It is becoming increasingly evident that the association of termites with gut bacteria not only functions in digestion but also enables the host to use the biosynthetic capacities of its symbionts as a nutritional resource.

  • Termites are promising sources of novel microorganisms and catalytic capacities for the production of biofuels from lignocellulosic feedstock. However, the nature of the activities that are involved in the efficient digestion of lignified cell walls remains unclear.

Abstract

Their ability to degrade lignocellulose gives termites an important place in the carbon cycle. This ability relies on their partnership with a diverse community of bacterial, archaeal and eukaryotic gut symbionts, which break down the plant fibre and ferment the products to acetate and variable amounts of methane, with hydrogen as a central intermediate. In addition, termites rely on the biosynthetic capacities of their gut microbiota as a nutritional resource. The mineralization of humus components in the guts of soil-feeding species also contributes to nitrogen cycling in tropical soils. Lastly, the high efficiency of their minute intestinal bioreactors makes termites promising models for the industrial conversion of lignocellulose into microbial products and the production of biofuels.

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Figure 1: The dual-cellulolytic systems of termites.
Figure 2: Diversity of the bacterial microbiota in termite guts.
Figure 3: Increasing gut compartmentation in higher termites.
Figure 4: Major microbial processes in the hindgut of lower termites.
Figure 5: Nitrogen cycling in lower termites.

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Acknowledgements

The current concept of symbiotic digestion in termite guts is based on countless contributions from many colleagues. The author tried his best to identify the mentors of important advances but regrets that space restrictions did not always permit references to the original work.

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Glossary

Hydrogenosomes

The hydrogen-producing organelles of many anaerobic protists; they share a common origin with mitochondria but only generate ATP by substrate-level phosphorylation.

Endoglucanases

Cellulases that randomly hydrolyse β-1,4-glycosidic bonds within the amorphous regions of cellulose. This generates additional chain ends, which increases the activity of exoglucanases in a synergistic manner.

β-glucosidases

Enzymes that hydrolyse cellobiose and the oligomeric degradation products of cellulose (such as cellotriose and cellotetraose).

Glycoside hydrolase family

(GHF). A family of glycosidases or related enzymes. There are more than 130 different GHFs, and many of them comprise enzymes that are involved in the digestion of plant fibre (for example, cellulases, hemicellulases, pectinases and carbohydrate esterases).

Cellobiohydrolases

Cellulases that act unidirectionally from the ends of the cellulose chain (and thus are exoglucanases), yielding cellobiose as a product; they are more active than endoglucanases against crystalline cellulose.

Cellulosomes

Extracellular multi-enzyme complexes of anaerobic cellulolytic bacteria that are composed of cellulases, other glycoside hydrolases and carbohydrate-binding modules, which are held together and adhere to the cell surface via scaffold proteins that have cohesin and dockerin domains.

Fenton reactions

Iron-mediated reactions in which hydroxyl radicals are formed (Fe2+ + H2O2 → Fe3+ + HO· + HO). These non-selectively oxidize many organic compounds.

Proctodeal trophallaxis

A social behaviour of termites, which solicit and imbibe droplets of hindgut fluid from nestmates.

nifH genes

Genes that encode the catalytic subunit of nitrogenase reductase; they are commonly used as a molecular marker for studying the diversity and community structure of nitrogen-fixing bacteria (also known as diazotrophs).

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Brune, A. Symbiotic digestion of lignocellulose in termite guts. Nat Rev Microbiol 12, 168–180 (2014). https://doi.org/10.1038/nrmicro3182

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