Abstract
In addition to evolving eusocial lifestyles, two equally fascinating aspects of termite biology are their mutualistic relationships with gut symbionts and their use of lignocellulose as a primary nutrition source. Termites are also considered excellent model systems for studying the production of bioethanol and renewable bioenergy from 2nd generation (non-food) feedstocks. While the idea that gut symbionts are the sole contributors to termite lignocellulose digestion has remained popular and compelling, in recent years host contributions to the digestion process have become increasingly apparent. However, the degree to which host and symbiont, and host enzymes, collaborate in lignocellulose digestion remain poorly understood. Also, how digestive enzymes specifically collaborate (i.e., in additive or synergistic ways) is largely unknown. In the present study we undertook translational-genomic studies to gain unprecedented insights into digestion by the lower termite Reticulitermes flavipes and its symbiotic gut flora. We used a combination of native gut tissue preparations and recombinant enzymes derived from the host gut transcriptome to identify synergistic collaborations between host and symbiont, and also among enzymes produced exclusively by the host termite. Our findings provide important new evidence of synergistic collaboration among enzymes in the release of fermentable monosaccharides from wood lignocellulose. These monosaccharides (glucose and pentoses) are highly relevant to 2nd-generation bioethanol production. We also show that, although significant digestion capabilities occur in host termite tissues, catalytic tradeoffs exist that apparently favor mutualism with symbiotic lignocellulose-digesting microbes. These findings contribute important new insights towards the development of termite-derived biofuel processing biotechnologies and shed new light on selective forces that likely favored symbiosis and, subsequently, group living in primitive termites and their cockroach ancestors.
Highlights
Termites are well-known for their roles in nutrient cycling in natural ecosystems, as pests of human crops and structures, and as models for renewable energy systems
In initial validations of these assays, the glucose assay was highly specific to glucose, the pentose assay to xylose and arabinose, and no interference occurred from mono- and disaccharides which can potentially be present in gut homogenates (Fig. S1)
Despite early evidence suggesting that termite lignocellulose digestion occurs as a collaboration between host and symbionts [3,4,5,6], the idea that this process is mediated exclusively by hindgut symbionts has proliferated and remained popular [2,4,8]
Summary
Termites (order Isoptera) are well-known for their roles in nutrient cycling in natural ecosystems, as pests of human crops and structures, and as models for renewable energy systems. The order Isoptera is divided into lower and higher termites based mostly on the presence or absence of protozoan gut symbionts [1,2,3]. Recent metagenomic and metatranscriptomic studies have corroborated long-standing hypotheses [3,4,5,6,7] of gut symbionts playing important roles in lignocellulose digestion in higher [8] and lower [9] termites. Proteomic investigations of the lumen contents of higher termite hindguts revealed limited protein-level evidence of prokaryotic symbiont-assisted digestion relative to that suggested by earlier transcriptomic studies [8,16]
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