Eukaryotic composition across seasons and social groups in the gut microbiota of wild baboons

Abstract

Background: Animals coexist with complex microbiota, including bacteria, viruses, and eukaryotes (e.g., fungi, protists, and helminths). While high-throughput sequencing is commonly used to characterize bacterial communities in animal microbiota, these methods are less often applied to gut eukaryotic composition. Here we used shotgun metagenomic sequencing to characterize eukaryotic diversity in the microbiomes of wild baboons and tested the degree to which eukaryotic community composition was predicted by host social group membership, sex, age, sequencing depth, and season of sample collection.

Results: We analyzed a total of 75 fecal samples collected in 2012 and 2014 from 73 wild baboons in the Amboseli ecosystem in Kenya. DNA from these samples was subjected to shotgun metagenomic sequencing, revealing members of the kingdoms Protista, Chromista, and Fungi in 90.7%, 46.7%, and 20.3% of all samples, respectively (percentages indicate the percent of samples in which each kingdom was observed). Social group membership explained 11.2% of the global diversity in gut eukaryotic species composition, but we did not detect statistically significant effects of season, host age, or host sex. Across samples, the most prevalent protists were Entamoeba coli (74.66% of samples), Enteromonas hominis (53.33% of samples), and Blastocystis subtype 3 (38.66% of samples), while the most prevalent fungi included Pichia manshurica (14.66% of samples), and Ogataea naganishii (6.66% of samples).

Conclusions: Protista, Chromista, and Fungi are common members of the gut microbiome of wild baboons. More work on eukaryotic members of primate gut microbiota is important for primate health monitoring and management strategies.

Keywords: Eukaryotes; Fungi; Gut Microbiome; Protists; Social groups; Wild baboons.

Fig. 1

Schematic of the two sets of fecal samples investigated in this study (Supplementary Table 1). Shotgun metagenomic data for the first set of samples on social group membership was published in 2015 by Tung et al. [52]; these data are publicly available in the NCBI’s Short Read Archive (Bioproject PRJNA271618). Shotgun metagenomic data for the second set of samples on seasonality were generated for the present study; these data are publicly available on NCBI’s Short Read Archive (Bioproject PRJEB81717). Data on host sex and age were available for samples in both data sets

Fig. 2

Social group membership is correlated with baboon gut eukaryotic composition. (A) Eukaryotic species richness in Viola’s and Mica’s social groups. A linear model was used to calculate statistical significance. (B) Non-metric multidimensional scaling (NMDS) plot of gut eukaryotic composition as measured using Jaccard index dissimilarity matrices. (C) Number of eukaryotic taxa per sample in Mica and Viola’s social groups and (D) prevalence of eukaryotic taxa in the two social groups. (E) Heatmap of the eukaryotic taxonomic composition of samples used to test for social group membership. Each column represents one fecal sample and its associated metadata on social group, age class, and sex of the host. Samples are clustered using Euclidean distance of eukaryotic community composition

Fig. 3

Season did not predict baboon gut eukaryotic diversity and composition. (A) Eukaryotic species richness in the wet and dry seasons. A linear model was used to calculate statistical significance. (B) Non-metric multidimensional scaling (NMDS) plot of gut eukaryotic microbiome composition as measured using Jaccard index dissimilarity matrices. (C) Number of eukaryotic taxa per sample in the dry and wet season. (D) prevalence of eukaryotic taxa in the wet and dry seasons. (E) Heatmap of the eukaryotic taxonomic composition of samples used to test for the effects of seasonality, with metadata on season, age class, and sex of the host. Each column represents one fecal sample; samples are clustered using Euclidean distance of eukaryotic community composition