Skin Microbiome and its Interplay with the Environment.

Advances in sequencing, bioinformatics and analytics now allow the structure, function and interrelations of whole microbial communities to be studied in greater detail. Collaborative efforts and multidisciplinary studies, crossing the boundary between environmental and medical microbiology, have allowed specific environmental, animal and human microbiomes to be characterized. One of the main challenges for microbial ecology is to link the phylogenetic diversity of host-associated microbes to their functional roles within the community. Much remains to be learned on the way microbes colonize the skin of different living organisms and the way the skin microbiome reacts to the surrounding environment (air, water, etc.). In this review, we discuss examples of recent studies that have used modern technology to provide insights into microbial communities in water and on skin, such as those in natural resources (thermal spring water), large mammals (humpback whales) and humans (the skin microbiome). The results of these studies demonstrate how a greater understanding of the structure and functioning of microbiota, together with their interactions with the environment, may facilitate the discovery of new probiotics or postbiotics, provide indicators for the quality of the environment, and show how changes in lifestyle and living environment, such as urbanization, can impact on the skin microbiome and skin health and disease in humans.

Respiratory microbiota of humpback whales may be reduced in diversity and richness the longer they fast.

Humpback whales endure several months of fasting while undertaking one of the longest annual migrations of any mammal, which depletes the whales' energy stores and likely compromises their physiological state. Airway microbiota are linked to respiratory health in mammals. To illuminate the dynamics of airway microbiota in a physiologically challenged mammal, we investigated the bacterial communities in the blow of East Australian humpback whales at two stages of their migration: at the beginning (n = 20) and several months into their migration (n = 20), using barcoded tag sequencing of the bacterial 16S rRNA gene. We show that early in the fasting the whale blow samples had a higher diversity and richness combined with a larger number of core taxa and a different bacterial composition than later in the fasting. This study provides some evidence that the rich blow microbiota at the beginning of their fasting might reflect the whales' uncompromised physiology and that changes in the microbiota occur during the whales' migration.

Does sociality drive diversity and composition of airway microbiota in cetaceans?

The number of social contacts of mammals is positively correlated with the diversity of their gut microbes. There is some evidence that sociality also affects microbes in the respiratory tract. We tested whether the airway microbiota of cetacean species differ depending on the whales' level of sociality. We sampled the blow of blue (Balaenoptera musculus), grey (Eschrichtius robustus), humpback (Megaptera novaeangliae) and long-finned pilot whales (PWs) (Globicephala melas) and analysed the blow microbiota by barcode tag sequencing targeting the V4 region of the bacterial 16S rRNA gene. Humpback whales (HWs) show higher levels of sociality than blue (BW) and grey (GW), while PWs are the most gregarious among the four species. The blow samples of the HWs showed the highest richness and diversity. HWs were also the only species with a species-specific clustering of their microbial community composition and a relatively large number of core taxa. Therefore, we conclude that it cannot be sociality alone shaping the diversity and composition of airway microbiota. We suggest the whale species' lung volume and size of the plume of exhaled air as an additional factor impacting the transmission potential of blow microbiota from one individual whale to another.

Interannual comparison of core taxa and community composition of the blow microbiota from East Australian humpback whales.

Cetacean represent vulnerable species impacted by multiple stressors, including reduction in prey species, habitat destruction, whaling and infectious disease. The composition of blow microbiota has been claimed to provide a promising tool for non-invasive health monitoring aiming to inform conservation management. Still, little is known about the temporal stability and composition of blow microbiota in whales. We used East Australian humpback whales (Megaptera novaeangliae) as a model species and collected blow and control samples in August 2016 and 2017 for an interannual comparison. We analysed the blow by barcode tag sequencing of the bacterial 16S rRNA gene. We found that the microbial communities in 2016 and 2017 were statistically similar regarding alpha and beta diversity but distinct to seawater. Zero-radius operational taxonomic units (zOTUs) shared by both groups accounted for about 50% of all zOTUs present. Still, the large individual variability in the blow microbiota resulted in a small number of core taxa (defined as present in at least 60% of whales). We conclude that the blow microbiota of humpback whales is either generally limited and of transient nature or the reduced airway microbiota is the symptom of a compromised physiological state potentially due to the challenges of the whales' annual migration.

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

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.

Humpback whale populations share a core skin bacterial community: towards a health index for marine mammals?

Microbes are now well regarded for their important role in mammalian health. The microbiology of skin--a unique interface between the host and environment--is a major research focus in human health and skin disorders, but is less explored in other mammals. Here, we report on a cross-population study of the skin-associated bacterial community of humpback whales (Megaptera novaeangliae), and examine the potential for a core bacterial community and its variability with host (endogenous) or geographic/environmental (exogenous) specific factors. Skin biopsies or freshly sloughed skin from 56 individuals were sampled from populations in the North Atlantic, North Pacific and South Pacific oceans and bacteria were characterized using 454 pyrosequencing of SSU rRNA genes. Phylogenetic and statistical analyses revealed the ubiquity and abundance of bacteria belonging to the Flavobacteria genus Tenacibaculum and the Gammaproteobacteria genus Psychrobacter across the whale populations. Scanning electron microscopy of skin indicated that microbial cells colonize the skin surface. Despite the ubiquity of Tenacibaculum and Psychrobater spp., the relative composition of the skin-bacterial community differed significantly by geographic area as well as metabolic state of the animals (feeding versus starving during migration and breeding), suggesting that both exogenous and endogenous factors may play a role in influencing the skin-bacteria. Further, characteristics of the skin bacterial community from these free-swimming individuals were assembled and compared to two entangled and three dead individuals, revealing a decrease in the central or core bacterial community members (Tenacibaculum and Psychrobater spp.), as well as the emergence of potential pathogens in the latter cases. This is the first discovery of a cross-population, shared skin bacterial community. This research suggests that the skin bacteria may be connected to humpback health and immunity and could possibly serve as a useful index for health and skin disorder monitoring of threatened and endangered marine mammals.