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Baleen Whales Host a Unique Gut Microbiome With Similarities to Both Carnivores and Herbivores

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Baleen Whales Host a Unique Gut Microbiome With Similarities to Both Carnivores and Herbivores

Jon G Sanders et al. Nat Commun.

Abstract

Mammals host gut microbiomes of immense physiological consequence, but the determinants of diversity in these communities remain poorly understood. Diet appears to be the dominant factor, but host phylogeny also seems to be an important, if unpredictable, correlate. Here we show that baleen whales, which prey on animals (fish and crustaceans), harbor unique gut microbiomes with surprising parallels in functional capacity and higher level taxonomy to those of terrestrial herbivores. These similarities likely reflect a shared role for fermentative metabolisms despite a shift in primary carbon sources from plant-derived to animal-derived polysaccharides, such as chitin. In contrast, protein catabolism and essential amino acid synthesis pathways in baleen whale microbiomes more closely resemble those of terrestrial carnivores. Our results demonstrate that functional attributes of the microbiome can vary independently even given an animal-derived diet, illustrating how diet and evolutionary history combine to shape microbial diversity in the mammalian gut.

Figures

Figure 1
Figure 1. Baleen whales host a distinct microbiota.
(a) Taxonomic composition of 16S rRNA amplicon sequences in cetaceans and terrestrial mammals. (b) PCoA ordination of unweighted UniFrac distances among mammalian gut microbiota. Note that despite similarity at higher taxonomic levels between the microbiota of baleen whales and those of terrestrial herbivores (a), baleen whales' microbiota are quite distinct from those of all sampled terrestrial mammal microbiota when considering individual OTUs (b) (i.e. reads with 97% similarity).
Figure 2
Figure 2. The functional compositions of baleen whale microbiomes show similarity to those of both terrestrial herbivores and carnivores.
Principal components analysis ordinations of predicted metagenomic functional potential show baleen whales microbiomes are distinct from those of terrestrial mammals when considering all pathways (a) or pathways involved in carbohydrate metabolism (e). Pathways involved in energy (b) and lipid (c) metabolism are more similar to those of terrestrial herbivores, and pathways involved in the synthesis of essential amino acids (d) are more similar to those of terrestrial carnivores. Sub-pathways previously shown to separate herbivore and carnivore metagenomes show a similar split, with baleen whale metagenomes showing a pattern of enrichment similar to herbivores in central pyruvate metabolism (f) and to carnivores in glutamate metabolism (g). Distributions of normalized abundances are shown as box plots for each gene, coloured according to dietary category (green=herbivore, red=carnivore, purple=omnivore, blue=whale). Box plot whiskers extend to 1.5 times the interquartile range. Genes relatively enriched in terrestrial herbivores and carnivores in the analysis of data from ref. have headers coloured green and red, respectively. Those enriched in whale microbiomes are outlined in blue, and the proposed direction of metabolite flux for each dietary category given as coloured arrows between metabolites.
Figure 3
Figure 3. The composition of CAZymes in baleen whale microbiomes is distinct and enriched in genes predicted to have activity on chitin.
(a) UPGMA-clustering dendrogram of CAZyme abundances. Dietary compositions are indicated by tip label colour. (b) Box plots showing distribution in normalized abundance of the five most abundant chitin-related CAZymes significantly enriched in baleen whale relative to terrestrial microbiomes. Note that CBM5 and CBM37 are binding domains rather than enzymes and CBM37 has activity against a broad spectrum of polysaccharides in addition to chitin.

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