Unraveling the Gut Microbiome of the Invasive Small Indian Mongoose (Urva auropunctata) in the Caribbean

Abstract

Small Indian mongooses (Urva auropunctata) are among the most pervasive predators to disrupt the native ecology on Caribbean islands and are strongly entrenched in their areas of introduction. Few studies, however, have considered the microbial ecology of such biological invasions. In this study, we investigated the gut microbiota of invasive small Indian mongooses in terms of taxonomic diversity and functional potential. To this end, we collected fecal samples from 60 free-roaming mongooses trapped in different vegetation zones on the island Saint Kitts. The core gut microbiome, assessed by 16S rRNA amplicon gene sequencing on the Ion S5^TM XL platform, reflects a carnivore-like signature with a dominant abundance of Firmicutes (54.96%), followed by Proteobacteria (13.98%) and Fusobacteria (12.39%), and a relatively minor contribution of Actinobacteria (10.4%) and Bacteroidetes (6.40%). Mongooses trapped at coastal sites exhibited a higher relative abundance of Fusobacterium spp. whereas those trapped in scrubland areas were enriched in Bacteroidetes, but there was no site-specific difference in predicted metabolic properties. Between males and females, beta-diversity was not significantly different and no sex-specific strategies for energy production were observed. However, the relative abundance of Gammaproteobacteria, and more specifically, Enterobacteriaceae, was significantly higher in males. This first description of the microbial profile of small Indian mongooses provides new insights into their bioecology and can serve as a springboard to further elucidating this invasive predator's impact throughout the Caribbean.

Keywords: Caribbean; Herpestes; Urva auropunctata; carnivore; gut microbiota; invasive species; microbial profiling; small Indian mongoose.

Figure 1

The rarefaction and extrapolation sampling curves based on the 16S rRNA gene sequencing data from 60 fecal samples of small Indian mongooses (sample codes: M_n): (A) Rank-abundance distribution curve; (B) Specaccum curve; (C) Rarefaction curves.

Figure 2

Relative abundance of the 10 most abundant bacterial phyla (A) and families (B) in 60 fecal samples of small Indian mongooses, determined by 16S rRNA gene sequencing.

Figure 3

Phylogenetic evolutionary tree of the gut microbiota at genus level from small Indian mongooses. Different colors of the branches represent different phyla (pink: Fusobacteria, brown: Firmicutes, purple: Bacteroidetes, blue: Proteobacteria, dark pink: Actinobacteria, green: Deferribacteres). The relative abundance of each genus is displayed outside the circle with different colors representing different fecal samples from each animal that has a unique Mx number.

Figure 4

Principal component analysis (PCoA) of the gut microbiota of male (red, n = 28) and female (green, n = 32) small Indian mongooses, based on weighted UniFrac distances.

Figure 5

Relative abundance of the 5 most abundant bacterial phyla of each group (male, female) expressed as average ± SEM (A): the significantly different relative abundance of Gammaproteobacteria between male and female small Indian mongooses (p < 0.05, between-group Welch’s t-test analysis); (B,C): the eight discriminating genera significantly different in abundance between male and female small Indian mongooses (p < 0.05, between-group Welch’s t-test analysis).

Figure 6

Boxplots based on Observed Species (A) and Shannon Diversity indices (B) showing the difference in alpha diversity between sampling locations. Significant differences between groups are marked with * (Wilcoxon, p < 0.05) and ** (Wilcoxon, p < 0.01) and solid dots represent outlier points.

Figure 7

Discriminating taxa significantly different in relative abundance (average ± SEM) at phylum (A) and family (B) level between fecal samples from small Indian mongooses trapped in a protected open wood- and scrubland (GR.PH, blue) and trapped in a dense inhabited and commercialized area (GR.FB, red) (p < 0.05, between-group t-test analysis).

Figure 8

Extended error bar plot indicating the functional differences of gut microbiota in male and female small Indian mongooses. KEGG categories were obtained from 16S rRNA gene sequences using PICRUSt. Only significant differences between two groups for pathways contributing to amino acid metabolism and carbohydrate metabolism are depicted (Welch’s t-test, p < 0.05).