Distinct microbiotas of anatomical gut regions display idiosyncratic seasonal variation in an avian folivore

Sergei V. Drovetski,Kenan O. Matterson,Michael J. V. O’Mahoney,Gary R. Graves,Brian K. Schmidt

doi:10.1186/s42523-019-0002-6

Abstract

BackgroundCurrent knowledge about seasonal variation in the gut microbiota of vertebrates is limited to a few studies based on mammalian fecal samples. Seasonal changes in the microbiotas of functionally distinct gut regions remain unexplored. We investigated seasonal variation (summer versus winter) and regionalization of the microbiotas of the crop, ventriculus, duodenum, cecum, and colon of the greater sage-grouse (Centrocercus urophasianus), an avian folivore specialized on the toxic foliage of sagebrush (Artemesia spp.) in western North America.ResultsWe sequenced the V4 region of the 16S rRNA gene on an Illumina MiSeq and obtained 6,639,051 sequences with a median of 50,232 per sample. These sequences were assigned to 457 bacterial and 4 archaeal OTUs. Firmicutes (53.0%), Bacteroidetes (15.2%), Actinobacteria (10.7%), and Proteobacteria (10.1%)were the most abundant and diverse phyla. Microbial composition and richness showed significant differences among gut regions and between summer and winter. Gut region explained almost an order of magnitude more variance in our dataset than did season or the gut region × season interaction. The effect of season was uneven among gut regions. Microbiotas of the crop and cecum showed the greatest seasonal differences.ConclusionsOur data suggest that seasonal differences in gut microbiota reflect seasonal variation in the microbial communities associated with food and water. Strong differentiation and uneven seasonal changes in the composition and richness of the microbiota among functionally distinct gut regions demonstrate the necessity of wider anatomical sampling for studies of composition and dynamics of the gut microbiota.

Highlights

Current knowledge about seasonal variation in the gut microbiota of vertebrates is limited to a few studies based on mammalian fecal samples
Filtered sequences from the pooled samples of crop, ventriculus, duodenum, cecum, and colon were assigned to 461 Operational taxonomic unit (OTU) (Additional file 2)
Four OTUs were classified as Archaea (Euryarchaeota; Thermoplasmata; Thermoplasmatales; [Thermoplasmatales]) and 457 as Bacteria

Summary

Introduction

Current knowledge about seasonal variation in the gut microbiota of vertebrates is limited to a few studies based on mammalian fecal samples. Seasonal changes in the microbiotas of functionally distinct gut regions remain unexplored. We investigated seasonal variation (summer versus winter) and regionalization of the microbiotas of the crop, ventriculus, duodenum, cecum, and colon of the greater sage-grouse (Centrocercus urophasianus), an avian folivore specialized on the toxic foliage of sagebrush (Artemesia spp.) in western North America. The rapidly growing appreciation of the microbial contribution to digestion, immune function, development, and reproduction in vertebrates is primarily based on studies of humans and a relatively small number of domestic and captive species of mammals and birds [2,3,4]. The generality of this pattern has not been investigated in non-mammalian vertebrates

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