Marine mammal skin microbiotas are influenced by host phylogeny.

Amy Apprill,Gordon Waring,Amy M Van Cise,Scott Landry,Robin W Baird,Matthew S Leslie,Jooke Robbins,Andrea Bogomolni,Carolyn A Miller,Jana M U'Ren,Laura Weber

doi:10.1098/rsos.192046

Abstract

Skin-associated microorganisms have been shown to play a role in immune function and disease of humans, but are understudied in marine mammals, a diverse animal group that serve as sentinels of ocean health. We examined the microbiota associated with 75 epidermal samples opportunistically collected from nine species within four marine mammal families, including: Balaenopteridae (sei and fin whales), Phocidae (harbour seal), Physeteridae (sperm whales) and Delphinidae (bottlenose dolphins, pantropical spotted dolphins, rough-toothed dolphins, short-finned pilot whales and melon-headed whales). The skin was sampled from free-ranging animals in Hawai‘i (Pacific Ocean) and off the east coast of the United States (Atlantic Ocean), and the composition of the bacterial community was examined using the sequencing of partial small subunit (SSU) ribosomal RNA genes. Skin microbiotas were significantly different among host species and taxonomic families, and microbial community distance was positively correlated with mitochondrial-based host genetic divergence. The oceanic location could play a role in skin microbiota variation, but skin from species sampled in both locations is necessary to determine this influence. These data suggest that a phylosymbiotic relationship may exist between microbiota and their marine mammal hosts, potentially providing specific health and immune-related functions that contribute to the success of these animals in diverse ocean ecosystems.

Highlights

Marine mammals play essential roles in marine ecosystems as predators and primary and secondary consumers, and can be sentinels of ocean health [1]
Analysis of the composition of the bacterial small subunit (SSU) rRNA genes using non-metric multidimensional scaling (nMDS) comparison of Bray–Curtis dissimilarity Minimum entropy decomposition (MED) node groupings demonstrated that the skin microbiotas clustered according to the host family level of taxonomy
PERMANOVA analysis of these MED nodes verified that the marine mammal families possessed significantly distinct skin microbiotas ( p = 0.001), and the PERMDISP analysis provided confidence that this result was not due to differences in dispersion among groups ( p = 0.794; table 2)

Summary

Introduction

Marine mammals play essential roles in marine ecosystems as predators and primary and secondary consumers, and can be sentinels of ocean health [1]. Many marine mammal species were hunted to very low numbers [3] and some populations, especially certain large baleen whales, have been slow to recover from extreme levels of exploitation. Microbiotas, are composed of a diverse assemblage of cells, including bacteria, archaea, fungi and protists, which can play vital and active roles in maintaining normal functioning and health of humans and other animals [5,6]. Studies in a handful of marine mammal species show evidence of highly diverse gut, oral and respiratory bacterial assemblages that vary in concordance with host species, as well as diet and habitat [7,8,9]. Similar to connections between human gut microbiota and diet [10], the microbiotas associated with marine mammals may provide critical insights into animal health and ecology; the microbial communities of most marine mammals are unexplored [8]

Methods

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Discussion

Conclusion