Coordinated\xa0transformation of the gut microbiome and lipidome of bowhead whales provides novel insights into digestion

Carolyn A Miller,Henry C Holm,John C George,Amy Apprill,Lara Horstmann,Benjamin A S Van Mooy,Helen F Fredricks

doi:10.1038/s41396-019-0549-y

Carolyn A Miller, Henry C Holm + Show 5 more

Open Access

https://doi.org/10.1038/s41396-019-0549-y

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Abstract

Whale digestion plays an integral role in many ocean ecosystems. By digesting enormous quantities of lipid-rich prey, whales support their energy intensive lifestyle, but also excrete nutrients important to ocean biogeochemical cycles. Nevertheless, whale digestion is poorly understood. Gastrointestinal microorganisms play a significant role in vertebrate digestion, but few studies have examined them in whales. To investigate digestion of lipids, and the potential contribution of microbes to lipid digestion in whales, we characterized lipid composition (lipidomes) and bacterial communities (microbiotas) in 126 digesta samples collected throughout the gastrointestinal tracts of 38 bowhead whales (Balaena mysticetus) harvested by Alaskan Eskimos. Lipidomes and microbiotas were strongly correlated throughout the gastrointestinal tract. Lipidomes and microbiotas were most variable in the small intestine and most similar in the large intestine, where microbiota richness was greatest. Our results suggest digestion of wax esters, the primary lipids in B. mysticetus prey representing more than 80% of total dietary lipids, occurred in the mid- to distal small intestine and was correlated with specific microorganisms. Because wax esters are difficult to digest by other marine vertebrates and constitute a large reservoir of carbon in the ocean, our results further elucidate the essential roles that whales and their gastrointestinal microbiotas play in the biogeochemical cycling of carbon and nutrients in high-latitude seas.

Highlights

As the largest animals in the ocean, each feeding on tons of smaller prey each day, whales are a stabilizing force in the global ocean ecosystem
Nonmetric multidimensional scaling of Bray–Curtis dissimilarity indices of the Minimum entropy decomposition (MED) nodes demonstrated significant partitioning of the bacterial communities according to anatomy (Fig. 1B) (PERMANOVA: Pseudo-F = 12.803, SS = 1.693E + 05, df = 8, P = 0.001)
NMDS of Bray–Curtis dissimilarity indices of the lipidome richness, the number of observed minimum entropy decomposition (MED) nodes, in 121 samples of gastrointestinal (GI) contents collected from 38 bowhead whales

Summary

Methods

Sample collectionDigesta (luminal contents) were opportunistically collected from up to nine anatomical locations in the GI tracts of 38 bowhead whales, 20 females and 18 males, harvested during the fall Native Alaskan subsistence hunts in Utqiaġvik, AK, USA, 2009 and 2011–2013 (Table S1). The nine GI sampling locations comprised three stomach chambers, four locations in the small intestine and two locations in the large intestine (Fig. 1A). Stomach chambers sampled were (n microbiota, lipidome) the forestomach (18, 16), the fundic (10, 8), and the pyloric (8, 2) chambers. Small intestine samples were collected from the duodenal ampulla (the chamber that connects the pyloric stomach chamber with the small intestine) (5, 5), duodenum (16, 15), jejunum (14, 13), and ileum (9, 8). Digesta was collected in sterile 2 mL cryovials, frozen in a liquid nitrogen vapor shipper, and transferred to −80 °C until processing. Digesta was collected in 50 mL centrifuge tubes and frozen at −20 °C until processing

Results

Discussion

Conclusion