Temporal and Regional Variability in the Skin Microbiome of Humpback Whales along the Western Antarctic Peninsula

Abstract

The skin is the first line of defense between an animal and its environment, and disruptions in skin-associated microorganisms can be linked to an animal's health and nutritional state. To better understand the skin microbiome of large whales, high-throughput sequencing of partial small subunit rRNA genes was used to study the skin-associated bacteria of 89 seemingly healthy humpback whales (Megaptera novaeangliae) sampled along the Western Antarctic Peninsula (WAP) during early (2010) and late (2013) austral summers. Six core groups of bacteria were present in 93% or more of all humpback skin samples. A shift was observed in the average relative abundances of these core bacteria over time, with the emergence of four additional core groups of bacteria that corresponded to a decrease in water temperature, possibly caused by season- or foraging-related changes in skin biochemistry that influenced microbial growth, or other temporal factors. The skin microbiome differed between whales sampled at several regional locations along the WAP, suggesting that environmental factors or population may also influence the whale skin microbiome. Overall, the skin microbiome of humpback whales appears to provide insight into animal- and environment-related factors and may serve as a useful indicator for animal health or ecosystem alterations.IMPORTANCE The microbiomes of wild animals are currently understudied but may provide information about animal health and/or animal-environment interactions. In the largest sampling of any marine mammal microbiome, this study demonstrates conservation in the skin microbiome of 89 seemingly healthy humpback whales sampled in the Western Antarctic Peninsula, with shifts in the bacterial community composition related to temporal and regional variability. This study is important because it suggests that the skin microbiome of humpback whales could provide insight into animal nutritional or seasonal/environment-related factors, which are becoming increasingly important to recognize due to unprecedented rates of climate change and anthropogenic impact on ocean ecosystems.

Host‐derived population genomics data provides insights into bacterial and diatom composition of the killer whale skin

“…In contrast, the microbiome of the two humpback whales sampled late in the Antarctic foraging season was dominated by Southern Ocean taxa (both >95%). This is consistent with the temporal variation in the complete humpback whale data set reported by Bierlich et al., (). Overall, the detailed analyses of contributing sources of the killer whale skin microbiome revealed a large proportion of taxa that are also found on the skin of other marine mammals and an important contribution of environmental ocean water taxa.…”

“…Type B1 killer whales in apparently poor health and with heavy diatom loads have been observed with severe skin conditions (skin peeling and lesions; Figure f); however, Tenacibaculum sp. have been reported in up to 95% of humpback whales sampled in recent studies, which included apparently healthy individuals (Apprill, Mooney, Lyman, Stimpert, & Rappé, , Apprill et al., ; Bierlich et al., ). Skin maintenance may thus represent a balancing act for Antarctic killer whales of managing the costs of pathogen load, thermal regulation, reduced foraging time and long‐range movement.…”

“…This approach allowed us to compare the composition of the free‐ranging killer whale skin microbiome to other marine mammal skin microbiota and to a number of potential contaminating and environmental sources. We obtained data from public repositories and included microbial communities reflecting the marine environment (ocean water from Southern Ocean and the North Pacific, Sunagawa et al., ), other marine mammal skin (captive bottlenose dolphins Tursiops truncatus and killer whales along with the respective pool water samples and free‐ranging humpback whales, Bierlich et al., ; Chiarello et al., ), likely contaminants such as human skin and gut (Lloyd‐Price et al., ; Meisel et al., ; Oh et al., ) and laboratory contamination from commonly used reagents (sterile water, Salter et al., ) (Supporting Information Table ). We attempted to specifically select sources that were obtained with the shotgun sequencing approach to avoid potential locus‐specific effects that can produce distinct microbiome profiles in amplicon‐based studies.…”

Geography, seasonality, and host‐associated population structure influence the fecal microbiome of a genetically depauparate Arctic mammal

“…Previously, population‐level variation of microbiomes had been studied in marine mammals (Bierlich et al, ), primates (Degnan et al, ; Stumpf et al, ), ponies (Antwis et al, ), amphibians (Griffiths et al, ), reptiles (Yuan et al, ), and fishes (Webster, Consuegra, Hitchings, & de Leaniz, ). To our knowledge, this is the first study to relate population structure to the microbiome of muskoxen.…”

“…The gastrointestinal microbiome is a complex microecosystem that plays a significant role in food breakdown and digestion, with profound effects on host health, development, adaptation, and evolution (Bahrndorff, Alemu, Alemneh, & Lund Nielsen, ; Hampton‐Marcell, Lopez, & Gilbert, ; Kohl, ; Zhang et al, ). The presence and diversity of different microbial types within microbiomes can be partially explained by spatial and temporal variation between species, populations, and individuals (Bierlich et al, ; Gerber, ; West et al, ). Differences within the microbiome of the same species reflect variable external environmental factors, such as habitat, disease, food availability, and food quality (Amato, ; Bahrndorff et al, ; Girard, Tromas, Amyot, & Shapiro, ).…”