Microbial detoxification in the gut of a specialist avian herbivore, the Greater Sage-Grouse

Abstract

One function of the gut microbiota gaining recent attention, especially in herbivorous mammals and insects, is the metabolism of plant secondary metabolites (PSMs). We investigated whether this function exists within the gut communities of a specialist avian herbivore. We sequenced the cecal metagenome of the Greater Sage-Grouse (Centrocercus urophasianus), which specializes on chemically defended sagebrush (Artemisia spp.). We predicted that the cecal metagenome of the sage-grouse would be enriched in genes associated with the metabolism of PSMs when compared to the metagenome of the domestic chicken. We found that representation of microbial genes associated with 'xenobiotic degradation and metabolism' was 3-fold higher in the sage-grouse cecal metagenomes when compared to that of the domestic chicken. Further, we identified a complete metabolic pathway for the degradation of phenol to pyruvate, which was not detected in the metagenomes of the domestic chicken, bovine rumen or 14 species of mammalian herbivores. Evidence of monoterpene degradation (a major class of PSMs in sagebrush) was less definitive, although we did detect genes for several enzymes associated with this process. Overall, our results suggest that the gut microbiota of specialist avian herbivores plays a similar role to the microbiota of mammalian and insect herbivores in degrading PSMs.

Evolutionary Biology Needs Wild Microbiomes

“…The (relatively) rapid generation time of microbes and the ability of the community to change in response to stimuli may contribute to acclimation in hosts, which in turn could facilitate adaptation of a host to new or changing environments (Alberdi et al, 2016). The microbiome facilitated the mammalian expansion from carnivory to herbivory (Ley et al, 2008) and it contributes to more minor ecological shifts as well (like the ability to consume toxic plants; Kohl et al, 2014, 2016). Host migration and population structure may drive the extinction of distinct microbial taxa (Domínguez-Bello et al, 2008).…”

Metagenomics reveals diet-specific specialization of bacterial communities in fungus gardens of grass- and dicot-cutter ants

“…Herbivore microbial symbionts, often residing in the guts of animals, have been implicated in aiding plant biomass breakdown (Hess et al , 2011; Kudo, 2009; Talbot, 1977; Adams et al , 2011), plant defense compound remediation (Wang et al , 2010; Adams et al , 2013; Boone et al , 2013), and nutrient supplementation (Warnecke et al , 2007; Hansen and Moran, 2011; LeBlanc et al , 2013). Microbial communities differ between hosts that specialize on different substrates (Muegge et al , 2011) and changes in these communities and their functional capacity are integral to their hosts’ transition to utilizing novel substrates (Hammer and Bowers, 2015; Delsuc et al , 2013; Li et al , 2015; Kohl et al , 2014; 2016). This phenomenon is not isolated to herbivores – in many systems, gut microbial communities are influence by the inputs of their hosts (Goffredi et al , 2005; Roman et al , 2015; Muegge et al , 2011; Youngblut et al , 2019; Wang et al , 2011; Li et al , 2016).…”

A place for host–microbe symbiosis in the comparative physiologist's toolbox

“…Remarkably, the toxin-degrading functions bestowed upon hosts by the gut microbiota can be readily transferred across populations and host species through microbial transplants (Kohl et al, 2016b,c;Miller et al, 2016a). There is evidence that similar detoxifying abilities also occur in the guts of avian herbivores, such as the hoatzin (Garcia-Amado et al, 2007) and sage-grouse (Kohl et al, 2016a), as well as in insect hosts (Ceja-Navarro et al, 2015;Hammer and Bowers, 2015). Together, the presence of fiberdegrading and/or toxin-degrading microbes in animal guts may determine the breadth of plant resources that an animal can consume.…”