Characterization of the cecum microbiome from wild and captive rock ptarmigans indigenous to Arctic Norway

PLoS One. 2019 Mar 11;14(3):e0213503. doi: 10.1371/journal.pone.0213503. eCollection 2019.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Wild / metabolism
  • Animals, Wild / microbiology
  • Archaea / genetics
  • Archaea / isolation & purification
  • Archaea / metabolism
  • Arctic Regions
  • Bacteria / genetics
  • Bacteria / isolation & purification
  • Bacteria / metabolism
  • Cecum / metabolism
  • Cecum / microbiology*
  • Galliformes / metabolism
  • Galliformes / microbiology*
  • Metagenome
  • Methane / metabolism
  • Microbiota
  • Norway
  • Svalbard

Substances

  • Methane

Grant support

This study was funded by UiT The Arctic University of Norway, and Nansenfondet, 2014. Author P.B. Pope is supported from The Research Council of Norway (250479) and the European Research Commission (336355 - MicroDE). Author A.T. Tveit is supported by the Research Council of Norway FRIPRO Mobility grant project Time & Energy 251027/RU, co-funded by the European Research Council (ERC) under Marie Curie grant agreement no 608695. The publication charges for this article have been funded by a grant from the publication fund of UiT The Arctic University of Norway.