Comparative Study of the Gut Microbiota Among Four Different Marine Mammals in an Aquarium

Abstract

Despite an increasing appreciation in the importance of host-microbe interactions in ecological and evolutionary processes, information on the gut microbial communities of some marine mammals is still lacking. Moreover, whether diet, environment, or host phylogeny has the greatest impact on microbial community structure is still unknown. To fill part of this knowledge gap, we exploited a natural experiment provided by an aquarium with belugas (Delphinapterus leucas) affiliated with family Monodontidae, Pacific white-sided dolphins (Lagenorhynchus obliquidens) and common bottlenose dolphin (Tursiops truncatus) affiliated with family Delphinidae, and Cape fur seals (Arctocephalus pusillus pusillus) affiliated with family Otariidae. Results show significant differences in microbial community composition of whales, dolphins, and fur seals and indicate that host phylogeny (family level) plays the most important role in shaping the microbial communities, rather than food and environment. In general, the gut microbial communities of dolphins had significantly lower diversity compared to that of whales and fur seals. Overall, the gut microbial communities were mainly composed of Firmicutes and Gammaproteobacteria, together with some from Bacteroidetes, Fusobacteria, and Epsilonbacteraeota. However, specific bacterial lineages were differentially distributed among the marine mammal groups. For instance, Lachnospiraceae, Ruminococcaceae, and Peptostreptococcaceae were the dominant bacterial lineages in the gut of belugas, while for Cape fur seals, Moraxellaceae and Bacteroidaceae were the main bacterial lineages. Moreover, gut microbial communities in both Pacific white-sided dolphins and common bottlenose dolphins were dominated by a number of pathogenic bacteria, including Clostridium perfringens, Vibrio fluvialis, and Morganella morganii, reflecting the poor health condition of these animals. Although there is a growing recognition of the role microorganisms play in the gut of marine mammals, current knowledge about these microbial communities is still severely lacking. Large-scale research studies should be undertaken to reveal the roles played by the gut microbiota of different marine mammal species.

Keywords: Cape fur seal; Pacific white-sided dolphin; beluga; common bottlenose dolphin; gut microbial communities.

Figure 1

Comparisons of four α-diversity indices, Shannon index (A), Inverse Simpson index (B), observed richness (C), and Chao1 index (D), of the 35 fecal specimens from belugas, Pacific white-sided dolphins, common bottlenose dolphin, and Cape fur seals. Based on Wilcoxon rank-sum test, *difference is significant at 0.05 level, **difference is significant at 0.01 level. The results are based on the ASVs datasets.

Figure 2

NMDS analysis of the gut microbial communities separated the samples into three principal groups, the first group composed of the fecal samples of belugas, the second group composed of fecal samples from the Pacific white-sided dolphins and common bottlenose dolphin, and the third group composed of fecal samples from Cape fur seals. The results are based on the ASVs datasets, and the left (A) and right (B) plots were calculated based on Bray-Curtis distance and Jaccard distance, respectively.

Figure 3

Gut microbial community members of belugas, Pacific white-sided dolphins, common bottlenose dolphin, and Cape fur seals at the phylum level.

Figure 4

Gut microbial community members of belugas, Pacific white-sided dolphins, common bottlenose dolphin, and Cape fur seals at the family level.

Figure 5

Gut microbial community members of belugas, Pacific white-sided dolphins, common bottlenose dolphin, and Cape fur seals at the genus level.

Figure 6

Distribution of ASVs in the gut of belugas, Pacific white-sided dolphins, common bottlenose dolphin, and Cape fur seals.

Figure 7

Stacked bar chart showing relative abundance of indicator ASVs in the gut of belugas, Pacific white-sided dolphins, common bottlenose dolphin, and Cape fur seals. The indicator organisms being shown was at the genus level.

Figure 8

Heatmap diagram showing the distribution of indicator ASVs of belugas, Pacific white-sided dolphins, common bottlenose dolphin, and Cape fur seals. Each row and column of the heatmap diagram corresponds to a single indicator and samples, respectively. The row data for each indicator were z-score transformed. Dendrograms were constructed based on Pearson correlation clustering.