Abstract
BackgroundAnimals are thought to achieve lignocellulose digestion via symbiotic associations with gut microbes; this view leads to significant focus on bacteria and fungi for lignocellulolytic systems. The presence of biomass conversion systems hardwired into animal genomes has not yet been unequivocally demonstrated.ResultsWe perform an exhaustive search for glycoside hydrolase (GH) genes from 21 genomes representing major bilaterian (Ecdysozoa, Spiralia, Echinodermata and Chordata) and basal metazoan (Porifera and Cnidaria) lineages. We also assessed the genome of a unicellular relative of Metazoa, Capsaspora owczarzaki and together with comparative analyses on 126 crustacean transcriptomes, we found that animals are living bioreactors at a microscale as they encode enzymatic suites for biomass decomposition. We identified a total of 16,723 GH homologs (2373 genes from animal genomes and 14,350 genes from crustacean transcriptomes) that are further classified into 60 GH families. Strikingly, through phylogenetic analyses, we observed that animal lignocellulosic enzymes have multiple origins, either inherited vertically over millions of years from a common ancestor or acquired more recently from non-animal organisms.ConclusionWe have conducted a systematic and comprehensive survey of GH genes across major animal lineages. The ability of biomass decay appears to be determined by animals’ dietary strategies. Detritivores have genes that accomplish broad enzymatic functions while the number of GH families is reduced in animals that have evolved specialized diets. Animal GH candidates identified in this study will not only facilitate future functional genomics research but also provide an analysis platform to identify enzyme candidates with industrial potential.
Highlights
Animals are thought to achieve lignocellulose digestion via symbiotic associations with gut microbes; this view leads to significant focus on bacteria and fungi for lignocellulolytic systems
The traditional dogma that animals rely on endosymbionts for lignocellulose digestive capabilities because they lack endogenous cellulases has steered researchers to focus on fungi and bacteria
Carbohydrate-Active Enzymes (CAZy) glycoside hydrolase (GH) entries are dominated by Bacteria sequences (81%) with the rest distributed across other major taxa: Archaea (1.1%), Viridiplantae (3.8%), Fungi (10.1%) and Metazoa (3.3%; 2.1% from Ecdysozoa, 0.2% from Spiralia and 1% from Deuterostomia) (Additional file 1: Figure S1; Additional file 2: Figure S2)
Summary
Animals are thought to achieve lignocellulose digestion via symbiotic associations with gut microbes; this view leads to significant focus on bacteria and fungi for lignocellulolytic systems. As one of the most abundant reserves of photosynthetically fixed carbon on earth, plant lignocellulose provides a sustainable source of polysaccharides for fermentation to biofuels that may be harnessed to meet industrial and domestic needs. Successful digestion of lignocellulosic tissues requires partial breakdown of lignin, which is achieved by fungi through the release of oxidizing free radicals that target woody cell wall components [1,2,3]. The traditional dogma that animals rely on endosymbionts for lignocellulose digestive capabilities because they lack endogenous cellulases has steered researchers to focus on fungi and bacteria. Using metagenomics approaches, genes involved in lignocellulose digestion have been identified from gut commensal microbes in insects [8,9,10] and mammals [11, 12]
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