Phylogenetic Analysis of Cellulolytic Enzyme Genes from Representative Lineages of Termites and a Related Cockroach

Abstract

The relationship between xylophagous termites and the protists resident in their hindguts is a textbook example of symbiosis. The essential steps of lignocellulose degradation handled by these protists allow the host termites to thrive on a wood diet. There has never been a comprehensive analysis of lignocellulose degradation by protists, however, as it has proven difficult to establish these symbionts in pure culture. The trends in lignocellulose degradation during the evolution of the host lineage are also largely unknown. To clarify these points without any cultivation technique, we performed meta-expressed sequence tag (EST) analysis of cDNA libraries originating from symbiotic protistan communities in four termite species and a wood-feeding cockroach. Our results reveal the establishment of a degradation system with multiple enzymes at the ancestral stage of termite-protistan symbiosis, especially GHF5 and 7. According to our phylogenetic analyses, the enzymes comprising the protistan lignocellulose degradation system are coded not only by genes innate to the protists, but also genes acquired by the protists via lateral transfer from bacteria. This gives us a fresh perspective from which to understand the evolutionary dynamics of symbiosis.

Diversity of Glycosyl Hydrolases from Cellulose-Depleting Communities Enriched from Casts of Two Earthworm Species

“…Apart from two new GHs, the GH domains revealed in the present work were also found in microbial communities from lower and higher wood-feeding termites and Cryptocercus cockroaches (69,75), whereas GHF6 from Cellvibrio spp. appeared to be specific to the earthworm-derived communities studied.…”

“…However, compared to other invertebrates, e.g., marine bivalves (21) or termites (19,48,56,68,69,75), little is known about the enzymatic machinery of earthworm-associated microorganisms that allows them to deplete diverse polymeric lignocellulosic substrates at high rates. In this work, we established enrichment cultures in a minimal mineral medium with cellulose as the sole carbon and energy source and with fresh casts from earthworms as inocula.…”

Diversity and Genomes of Uncultured Microbial Symbionts in the Termite Gut

“…59,60) Approximately 1,000 cDNA clones per host species were sequenced, and it was found that about 10% of the clones in each sample belonged to the glycosyl hydrolase families (GHFs) such as GHF5, 7, 10, and 45. These included cellulases (endoglucanase and cellobiohydrolase) and hemicellulases.…”

Development of an ecophysiological model for Diplosphaera colotermitum TAV2, a termite hindgut Verrucomicrobium

“…Although, we have yet to identify specific conditions allowing strain TAV2 to grow in xylan as a sole C source (Wertz et al, 2012), our integrated approach identified genes and proteins involved in lignocellulose degradation, specifically the enzymes acetylxylan esterase, xylan a-1,2-glucuronosidase and xylose isomerase, the later being responsible for converting xylose into xylulose, which enters the PPP (White, 2007). Because much of investigation in termite guts have targeted cellulose degradation through biochemical characterization of host celullases (Watanabe and Tokuda, 2010), gene expression of glycosyl hydrolases by protists (Todaka et al, 2007(Todaka et al, , 2010, and metagenomic (Warnecke et al, 2007) and proteomic (Burnum et al, 2011) approaches, the understanding of xylan hydrolysis remains virtually unexplored. Our results reveal an important and perhaps compartmentalized, ecological role for the TAV2 population on the debranching of xylan residues.…”