Date Published: March 11, 2019
Publisher: Public Library of Science
Author(s): Alejandro Salgado-Flores, Alexander T. Tveit, Andre-Denis Wright, Phil B. Pope, Monica A. Sundset, Alex V. Chaves.
Rock ptarmigans (Lagopus muta) are gallinaceous birds inhabiting arctic and sub-arctic environments. Their diet varies by season, including plants or plant parts of high nutritional value, but also toxic plant secondary metabolites (PSMs). Little is known about the microbes driving organic matter decomposition in the cecum of ptarmigans, especially the last steps leading to methanogenesis. The cecum microbiome in wild rock ptarmigans from Arctic Norway was characterized to unveil their functional potential for PSM detoxification, methanogenesis and polysaccharides degradation. Cecal samples were collected from wild ptarmigans from Svalbard (L. m. hyperborea) and northern Norway (L. m. muta) during autumn/winter (Sept-Dec). Samples from captive Svalbard ptarmigans fed commercial pelleted feed were included to investigate the effect of diet on microbial composition and function. Abundances of methanogens and bacteria were determined by qRT-PCR, while microbial community composition and functional potential were studied using 16S rRNA gene sequencing and shotgun metagenomics. Abundances of bacteria and methanogenic Archaea were higher in wild ptarmigans compared to captive birds. The ceca of wild ptarmigans housed bacterial groups involved in PSM-degradation, and genes mediating the conversion of phenol compounds to pyruvate. Methanomassiliicoccaceae was the major archaeal family in wild ptarmigans, carrying the genes for methanogenesis from methanol. It might be related to increased methanol production from pectin degradation in wild birds due to a diet consisting of primarily fresh pectin-rich plants. Both wild and captive ptarmigans possessed a broad suite of genes for the depolymerization of hemicellulose and non-cellulosic polysaccharides (e.g. starch). In conclusion, there were no physiological and phenotypical dissimilarities in the microbiota found in the cecum of wild ptarmigans on mainland Norway and Svalbard. While substantial differences in the functional potential for PSM degradation and methanogenesis in wild and captive birds seem to be a direct consequence of their dissimilar diets.
Ptarmigans (Lagopus muta) are gallinaceous birds within the subfamily Tetraoninae. With up to 30 different subspecies recognized, these birds show a circumpolar distribution in the northern hemisphere [1, 2]. Some physiological and phenotypical differences have been described between Svalbard (L. m. hyperborea) ptarmigan and rock ptarmigan from Scandinavia (L. m. muta), with Svalbard ptarmigans having a higher average body weight and size. In addition, Svalbard ptarmigans display striking variations in body weight and food intake throughout the year [3–5].
It is concluded that wild ptarmigans in these two different geographical regions (Svalbard and Norway) share highly similar microbial communities. The presence of microbial taxa with the potential to decompose PSMs reflects an ability of ptarmigans to bypass the toxicity exerted by PSMs. The broad range of GHs found in wild and captive ptarmigans suggests the existence of a versatile cecum microbiota that allows the consumption of plants with different fiber contents. Methanol-based methanogenesis seems to constitute one of the major methanogenesis pathways in wild ptarmigans based on the dominance of Methanomassiliicoccaceae methanogens and the presence of genes for this pathway. The higher abundance of methanogens in wild ptarmigans may be linked to the ingestion of a natural diet consisting of unprocessed polysaccharides that result in longer fermentation necessary to allow growth of methanogenic Archaea.