Adaptation to herbivory by the Tammar wallaby includes bacterial and glycoside hydrolase profiles different from other herbivores

Abstract

Metagenomic and bioinformatic approaches were used to characterize plant biomass conversion within the foregut microbiome of Australia's "model" marsupial, the Tammar wallaby (Macropus eugenii). Like the termite hindgut and bovine rumen, key enzymes and modular structures characteristic of the "free enzyme" and "cellulosome" paradigms of cellulose solubilization remain either poorly represented or elusive to capture by shotgun sequencing methods. Instead, multigene polysaccharide utilization loci-like systems coupled with genes encoding β-1,4-endoglucanases and β-1,4-endoxylanases-which have not been previously encountered in metagenomic datasets-were identified, as were a diverse set of glycoside hydrolases targeting noncellulosic polysaccharides. Furthermore, both rrs gene and other phylogenetic analyses confirmed that unique clades of the Lachnospiraceae, Bacteroidales, and Gammaproteobacteria are predominant in the Tammar foregut microbiome. Nucleotide composition-based sequence binning facilitated the assemblage of more than two megabase pairs of genomic sequence for one of the novel Lachnospiraceae clades (WG-2). These analyses show that WG-2 possesses numerous glycoside hydrolases targeting noncellulosic polysaccharides. These collective data demonstrate that Australian macropods not only harbor unique bacterial lineages underpinning plant biomass conversion, but their repertoire of glycoside hydrolases is distinct from those of the microbiomes of higher termites and the bovine rumen.cellulases | marsupials | metagenomics | plant biomass conversion | polysaccharide utilization loci A ustralia possesses the largest share of the world's extant marsupial species, which diverged from other eutherian mammals ≈150 million years ago. Most likely, the most widely recognized members of this group are the macropods (kangaroos and wallabies). The macropods also evolved in geographical isolation of other eutherian herbivores, and although they are often compared with ruminants, the various macropod species show a wide range of unique adaptations to herbivory. These differences include their dentition and mastication of food, as well as the anatomical adaptations of the forestomach that supports a cooperative host-microbe association that efficiently derives nutrients from plant biomass rich in lignocellulose (1). Compared with ruminant species, the hydrolytic and fermentative processes these microbes provide must be relatively rapid because of the continuous transit of plant biomass through the herbivore gut (2, 3). There is also a widespread belief-developed from several studies during the late 1970s-that Australian macropods generate less methane during feed digestion than ruminant herbivores (4, 5), indicative of some novel host and microbe adaptations of the macropods to herbivory. Indeed, the limited studies published to date suggest the foregut microbiomes of macropods possess unique protozoal, bacterial, and archaeal microorganisms (6-8); however, very little is currently known about the genetic potential and ...

Whole-genome sequencing of the snub-nosed monkey provides insights into folivory and evolutionary history

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Phylogeny, classification and metagenomic bioprospecting of microbial acetyl xylan esterases

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