Abstract
The North American beaver (Castor canadensis) has long been considered an engineering marvel, transforming landscapes and shaping biological diversity through its dam building behavior. While the beaver possesses conspicuous morphological features uniquely adapted for the use of woody plants as construction materials and dietary staples, relatively little is known about the specialized microorganisms inhabiting the beaver gastrointestinal tract and their functional roles in determining host nutrition. Here we use a combination of shotgun metagenomics, functional screening and carbohydrate biochemistry to chart the community structure and metabolic power of the beaver fecal microbiome. We relate this information to the metabolic capacity of other wood feeding and hindgut fermenting organisms and profile the functional repertoire of glycoside hydrolase (GH) families distributed among and between population genome bins. Metagenomic screening revealed novel mechanisms of xylan oligomer degradation involving GH43 enzymes from uncharacterized subfamilies and divergent polysaccharide utilization loci, indicating the potential for synergistic biomass deconstruction. Together, these results open a functional metagenomic window on less conspicuous adaptations enabling the beaver microbiome to efficiently convert woody plants into host nutrition and point toward rational design of enhanced enzyme mixtures for biorefining process streams.
Highlights
Microbial communities inhabiting the mammalian digestive tract, gut microbiomes, affect host health and mediate essential services including dietary access to recalcitrantThese authors contributed : Zachary Armstrong and Keith Mewis.Electronic supplementary material The online version of this article contains supplementary material, which is available to authorized users.Genome Science and Technology Program, University of British Columbia, 2329 West Mall, Vancouver, BC V6T 1Z4, CanadaDepartment of Chemistry, University of British Columbia, 2036 Main Mall, Vancouver V6T 1Z1 BC, CanadaDepartment of Microbiology & Immunology, University of British Columbia, Vancouver V6T 1Z1 BC, CanadaCentre for High-Throughput Biology, University of British glycans such as starches and fibers [1]
Multiple studies indicate that mammalian gut microbiomes consist of specialized communities that respond to complex glycans derived from specific dietary sources such as lignocellulosic biomass and release products that can be absorbed into the digestive tract [2,3,4,5,6]
The North American beaver, Castor canadensis, provides a useful animal model for the study of xylotrophic microbiomes, as its diet is largely composed of bark, shoots, leaves, and other fibers from hardwood deciduous trees such as poplar, aspen, and cottonwood, which have commercial value in the forestry sector [14, 15]
Summary
Microbial communities inhabiting the mammalian digestive tract, gut microbiomes, affect host health and mediate essential services including dietary access to recalcitrant. Peter Wall Institute for Advanced Studies, University of British Columbia, Vancouver V6T 1Z1, Canada biocatalysts and polysaccharide utilization systems [7,8,9,10,11,12] These communities provide a frame of reference for understanding how lignocellulosic biomass is converted into dietary macronutrients, as well as a deep reservoir of genomic information with potential biotechnological applications [13]. The North American beaver, Castor canadensis, provides a useful animal model for the study of xylotrophic microbiomes, as its diet is largely composed of bark, shoots, leaves, and other fibers from hardwood deciduous trees such as poplar, aspen, and cottonwood, which have commercial value in the forestry sector [14, 15] Hardwoods such as poplar typically have a total polysaccharide content comprising 60–80% of the dry mass of the wood [16]. Given that the proclivity of beavers to consume wood differentiates them from other hindgut fermenting herbivores, several questions arise from the initial microbiome study: At what taxonomic level does the beaver microbiome differ from other xylotrophic and hindgut fermenting organisms? Does the microbiome encode specialized genes or gene cassettes mediating complete conversion of lignocellulosic biomass? Are some components of the lignocellulose targeted for digestion more than others? To what extent are these functions distributed at the population and community levels? Could analysis of these differences reveal new insight into sequential biomass deconstruction of woodbased fibers transferrable to industrial process streams? To begin answering these questions, we used a combination of SSU rRNA gene sequencing, shotgun metagenomics and functional screening to evaluate the community structure and metabolic potential of the beaver microbiome in relation to other wood-feeding organisms and to recover activities mediating lignocellulosic biomass deconstruction
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