Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite Reticulitermes flavipes

By A. Tartar, Marsha M Wheeler, Xuguo Zhou, Monique R. Coy, D. Boucias, Michael E. Scharf. Biotechnology for Biofuels, 2009

616 citations recorded by the source corpus.

BackgroundTermite lignocellulose digestion is achieved through a collaboration of host plus prokaryotic and eukaryotic symbionts. In the present work, we took a combined host and symbiont metatranscriptomic approach for investigating the digestive contributions of host and symbiont in the lower termite Reticulitermes flavipes. Our approach consisted of parallel high-throughput sequencing from (i) a host gut cDNA library and (ii) a hindgut symbiont cDNA library. Subsequently, we undertook functional analyses of newly identified phenoloxidases with potential importance as pretreatment enzymes in industrial lignocellulose processing.ResultsOver 10,000 expressed sequence tags (ESTs) were sequenced from the 2 libraries that aligned into 6,555 putative transcripts, including 171 putative lignocellulase genes. Sequence analyses provided insights in two areas. First, a non-overlapping complement of host and symbiont (prokaryotic plus protist) glycohydrolase gene families known to participate in cellulose, hemicellulose, alpha carbohydrate, and chitin degradation were identified. Of these, cellulases are contributed by host plus symbiont genomes, whereas hemicellulases are contributed exclusively by symbiont genomes. Second, a diverse complement of previously unknown genes that encode proteins with homology to lignase, antioxidant, and detoxification enzymes were identified exclusively from the host library (laccase, catalase, peroxidase, superoxide dismutase, carboxylesterase, cytochrome P450). Subsequently, functional analyses of phenoloxidase activity provided results that were strongly consistent with patterns of laccase gene expression. In particular, phenoloxidase activity and laccase gene expression are mostly restricted to symbiont-free foregut plus salivary gland tissues, and phenoloxidase activity is inducible by lignin feeding.ConclusionTo our knowledge, this is the first time that a dual host-symbiont transcriptome sequencing effort has been conducted in a single termite species. This sequence database represents an important new genomic resource for use in further studies of collaborative host-symbiont termite digestion, as well as development of coevolved host and symbiont-derived biocatalysts for use in industrial biomass-to-bioethanol applications. Additionally, this study demonstrates that: (i) phenoloxidase activities are prominent in the R. flavipes gut and are not symbiont derived, (ii) expands the known number of host and symbiont glycosyl hydrolase families in Reticulitermes, and (iii) supports previous models of lignin degradation and host-symbiont collaboration in cellulose/hemicellulose digestion in the termite gut. All sequences in this paper are available publicly with the accession numbers FL634956-FL640828 (Termite Gut library) and FL641015-FL645753 (Symbiont library).

Subfields: Genetics, Insect Science

View Paper: https://www.semanticscholar.org/paper/0fc526d81bca414780da7bfd784f9118598f3fa6

How researchers see this paper

The researchers whose trusted networks rank it highest, strongest advocate first. Every researcher gets a different order.

In Genetics

1. Rolf Daniel
2. B. B. Finlay
3. Carola Simon
4. L. Antunes
5. I. Sekirov
6. Shannon L. Russell

Citations in the corpus

• Insect Gut Bacterial Diversity Determined by Environmental Habitat, Diet, Developmental Stage, and Phylogeny of Host (2014, neutral): “, detritus, phloem, sap, wood, and xylem) (28, 63, 64).”
• Molecular approaches to study the insect gut symbiotic microbiota at the ‘omics’ age (2010, background): “In particular, enzymes C© 2010 The Authors Journal compilation C© Institute of Zoology, Chinese Academy of Sciences, Insect Science, 17, 199–219 secreted by host insect species play particularly important roles in lignin degradation (Tartar et al., 2009).”
• Gut microbiota in health and disease. (2010, background): “Metatranscriptomics has been successfully used to study complex microbial communities in soil (315) and aquatic environments (78), as well as the host-symbiont interactions in the termite gut (305).”
• Animal digestive strategies versus anaerobic digestion bioprocesses for biogas production from lignocellulosic biomass (2011, neutral): “However, endogenous laccases, phenoloxidases and esterases/carboxylesterases were presumed to be involved in lignin degradation, without direct evidence of degradation, on the basis of transcriptome analysis of termite Reticulitermes flavipes (Scharf and Tartar 2008; Tartar et al. 2009 ).”
• Metagenomic Analyses: Past and Future Trends (2010, background): “ysis of mRNA-derived cDNA clone libraries (90, 119).”