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Ninety-Nine De Novo Assembled Genomes from the Moose (Alces Alces) Rumen Microbiome Provide New Insights Into Microbial Plant Biomass Degradation

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Ninety-Nine De Novo Assembled Genomes from the Moose (Alces Alces) Rumen Microbiome Provide New Insights Into Microbial Plant Biomass Degradation The ISME Journal (2017) 11, 2538–2551 © 2017 International Society for Microbial Ecology All rights reserved 1751-7362/17 www.nature.com/ismej ORIGINAL ARTICLE Ninety-nine de novo assembled genomes from the moose (Alces alces) rumen microbiome provide new insights into microbial plant biomass degradation Olov Svartström1, Johannes Alneberg2, Nicolas Terrapon3,4, Vincent Lombard3,4, Ino de Bruijn2, Jonas Malmsten5,6, Ann-Marie Dalin6, Emilie EL Muller7, Pranjul Shah7, Paul Wilmes7, Bernard Henrissat3,4,8, Henrik Aspeborg1 and Anders F Andersson2 1School of Biotechnology, Division of Industrial Biotechnology, KTH Royal Institute of Technology, Stockholm, Sweden; 2School of Biotechnology, Division of Gene Technology, KTH Royal Institute of Technology, Science for Life Laboratory, Stockholm, Sweden; 3CNRS UMR 7257, Aix-Marseille University, 13288 Marseille, France; 4INRA, USC 1408 AFMB, 13288 Marseille, France; 5Department of Pathology and Wildlife Diseases, National Veterinary Institute, Uppsala, Sweden; 6Division of Reproduction, Department of Clinical Sciences, Swedish University of Agricultural Sciences, Uppsala, Sweden; 7Luxembourg Centre for Systems Biomedicine, University of Luxembourg, Esch-sur-Alzette, Luxembourg and 8Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia The moose (Alces alces) is a ruminant that harvests energy from fiber-rich lignocellulose material through carbohydrate-active enzymes (CAZymes) produced by its rumen microbes. We applied shotgun metagenomics to rumen contents from six moose to obtain insights into this microbiome. Following binning, 99 metagenome-assembled genomes (MAGs) belonging to 11 prokaryotic phyla were reconstructed and characterized based on phylogeny and CAZyme profile. The taxonomy of these MAGs reflected the overall composition of the metagenome, with dominance of the phyla Bacteroidetes and Firmicutes. Unlike in other ruminants, Spirochaetes constituted a significant proportion of the community and our analyses indicate that the corresponding strains are primarily pectin digesters. Pectin-degrading genes were also common in MAGs of Ruminococcus, Fibrobacteres and Bacteroidetes and were overall overrepresented in the moose microbiome compared with other ruminants. Phylogenomic analyses revealed several clades within the Bacteriodetes without previously characterized genomes. Several of these MAGs encoded a large numbers of dockerins, a module usually associated with cellulosomes. The Bacteroidetes dockerins were often linked to CAZymes and sometimes encoded inside polysaccharide utilization loci, which has never been reported before. The almost 100 CAZyme-annotated genomes reconstructed in this study provide an in-depth view of an efficient lignocellulose-degrading microbiome and prospects for developing enzyme technology for biorefineries. The ISME Journal (2017) 11, 2538–2551; doi:10.1038/ismej.2017.108; published online 21 July 2017 Introduction could contribute substantially to fuel supplies. A key process open to improvement is the enzymatic Improved processing of lignocellulose from plant hydrolysis of lignocellulose into fermentable sugars. biomass is considered a promising avenue for By enhancing enzyme activities and tailoring production of alternative biofuels, green chemicals enzyme cocktails for complete breakdown of ligno- and biomaterials. Lignocellulose is a highly abun- celluloses, the cost of this rate-limiting step could be dant renewable resource that can be obtained from lowered substantially (Mohanram et al., 2013; agricultural and forestry residues and energy crops, Goldbeck et al., 2014). as well as from industrial and household wastes. In The Carbohydrate-Active enZyme database forest-rich countries, biofuel from forest residues (CAZy) organizes enzymes required for lignocellu- lose polysaccharide degradation into sequence-based Correspondence: H Aspeborg or AF Andersson, School of families covering large classes, in particular glyco- Biotechnology, Division of Gene Technology, KTH Royal Institute side hydrolases (GHs), polysaccharide lyases (PLs) of Technology, Science for Life Laboratory, Stockholm SE-171 21, and carbohydrate esterases (CEs) (Lombard et al., Sweden. 2014). The action of these enzymes is further E-mail: [email protected] or anders.andersson@scili enhanced in nature by anchoring a carbohydrate- felab.se Received 14 February 2017; revised 5 May 2017; accepted 30 May binding module (CBM) to the catalytic module. 2017; published online 21 July 2017 Many microbes living in plant biomass-degrading Moose (Alces alces) rumen shotgun metagenomics O Svartström et al 2539 environments such as soil, composts and herbivore 2011; Muegge et al., 2011; Patel et al., 2014). digestive tracts express large pools of carbohydrate- Furthermore, shotgun metagenomics in combination active enzymes (CAZymes) for lignocellulose with binning methods enable reconstruction of conversion. nearly complete single genomes that could be Ruminants (for example, cattle, sheep, goats, explored for new lignocellulose-degrading CAZymes cervids) have a vast enlargement of their gastro- (Herlemann et al., 2013; Kishi et al., 2015). intestinal tract, known as the forestomachs, which The moose (Alces alces) is the largest browsing are comprised of the rumen, reticulum and omasum. wild ruminant of Northern Europe (referred to as the The rumen contains large amounts of anaerobic ‘King of the Forest’ in Nordic countries) and microorganisms (bacteria, protists and fungi) and according to physiological and anatomical character- functions as a highly efficient bioreactor for ligno- istics of the rumen, classified as a ‘concentrate cellulose conversion. The microbial community selector’ (Hofmann, 1989). The moose diet varies composition varies with diet and host, but a core with season but is in winter dominated by woody rumen microbiome is found that include Prevotella, plants where Scots pine (Pinus sylvestris) ranks as Butyrivibrio, Ruminococcus, Bacteriodales and Clos- the quantitatively most important during the coldest tridiales (Henderson et al., 2015). The rumen season (Cederlund et al., 1980; Bergström and microbes ferment feed to form volatile fatty acids Hjeljord, 1987). Pine residues found in the rumen that are the major energy source for all ruminants. include needles, twigs and bark. During the rest of Different bacterial taxa utilize different cellulose- the year, the diet is complex and is composed mainly degradative strategies in the ruminal ecosystem of leaves from deciduous trees such as rowan (Flint, 2008). The firmicute Ruminococcus flavefa- (Sorbus aucuparia), aspen (Populus tremula), wil- ciens uses the cellulosome, an extracellular lows (Salix spp.) and birches (Betula spp.). Also multienzyme complex. The typical cellulosome shrubs and herbaceous plants, for example, heather architecture is composed of dockerin-bearing (Calluna vulgaris), European blueberry (Vaccinium enzymes that bind the multiple cohesin domains myrtillus) and fireweed (Chamaenerion angustifo- found on a scaffoldin subunit (Bayer et al., 2004). lium), are important components of the diet. More- The latter is attached to the cell-surface, exposing the over, small quantities of grasses, ferns, mosses and catalytic domains to the substrate. The efficient fungi are consumed over the year. Consequently, cellulolytic machinery of the Gram-negative bacter- microbial communities of the moose rumen are ium Fibrobacter succinogenes represents a less expected to be able to process cellulose, pectins, understood system for cellulose depolymerization, arabinogalactan and different types of hemicellu- involving attachment to the substrate by a yet loses found in diverse plant families such as unknown protein followed by cleavage of the galactomannan, glucomannan, galactoglucomannan, polymer by a distinct set of cellulases (Wilson, arabinoglucuronoxylan, glucuronoxylan, xyloglucan 2009; Suen et al., 2011b; Ransom-Jones et al., and mixed-linkage glucan. Although it has been 2014). Recent enzyme characterization efforts have shown that the moose rumen harbors bacterial also shed light on cellulolytic functions in species families that include fibrolytic species (Ishaq and from the Bacteroidetes phylum (Naas et al., 2014; Wright, 2012, 2014), the actual CAZyme content of Mackenzie et al., 2015). Within the Bacteroidetes, the moose rumen remains to be explored. The fact including the rumen-based Prevotella ruminicola, that the moose manages to utilize energy from fiber- CAZymes are organized in physically linked gene rich twigs and branches of pine and birch is critical clusters that encode the entire functional chain for its survival in harsh winter conditions. It also involving binding, degrading and importing defined motivates the detailed exploration of its rumen glycan structures. These gene clusters are referred to microbiome, as presented in this study. as polysaccharide utilization loci (PULs) (Bjursell et al., 2006; Terrapon and Henrissat, 2014). A PUL can be dedicated to breakdown of a specific poly- Materials and methods saccharide, such as mannan or xylan (Cuskin et al., 2015; Rogowski et al., 2015). Sampling, DNA extraction and sequencing Genome sequencing of the isolated rumen species Rumen content was collected during October 2011 F. succinogenes and R. albus has successfully from six individual moose. The moose were shot by revealed sequence-encoding enzymes for the break- licensed hunters during Swedish hunting season. No down of plant material
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