Protective role of the vulture facial skin and gut microbiomes aid adaptation to scavenging

Abstract

BackgroundVultures have adapted the remarkable ability to feed on carcasses that may contain microorganisms that would be pathogenic to most other animals. The holobiont concept suggests that the genetic basis of such adaptation may not only lie within their genomes, but additionally in their associated microbes. To explore this, we generated shotgun DNA sequencing datasets of the facial skin and large intestine microbiomes of the black vulture (Coragyps atratus) and the turkey vulture (Cathartes aura). We characterized the functional potential and taxonomic diversity of their microbiomes, the potential pathogenic challenges confronted by vultures, and the microbial taxa and genes that could play a protective role on the facial skin and in the gut.ResultsWe found microbial taxa and genes involved in diseases, such as dermatitis and pneumonia (more abundant on the facial skin), and gas gangrene and food poisoning (more abundant in the gut). Interestingly, we found taxa and functions with potential for playing beneficial roles, such as antilisterial bacteria in the gut, and genes for the production of antiparasitics and insecticides on the facial skin. Based on the identified phages, we suggest that phages aid in the control and possibly elimination, as in phage therapy, of microbes reported as pathogenic to a variety of species. Interestingly, we identified Adineta vaga in the gut, an invertebrate that feeds on dead bacteria and protozoans, suggesting a defensive predatory mechanism. Finally, we suggest a colonization resistance role through biofilm formation played by Fusobacteria and Clostridia in the gut.ConclusionsOur results highlight the importance of complementing genomic analyses with metagenomics in order to obtain a clearer understanding of the host-microbial alliance and show the importance of microbiome-mediated health protection for adaptation to extreme diets, such as scavenging.Electronic supplementary materialThe online version of this article (10.1186/s13028-018-0415-3) contains supplementary material, which is available to authorized users.

Blood Parasites in Sympatric Vultures: Role of Nesting Habits and Effects on Body Condition

“…A scavenger diet may expose vultures to multiple pathogens in carcasses, although several mechanisms have evolved to cope with them [ 9 , 10 , 11 ]. Vultures have many necrotizing and potentially pathogenic bacteria in their food, and gastrointestinal and skin microbiome, which may be kept at bay by a potentially highly evolved and upregulated immunity [ 11 , 12 ]. However, this balance may be broken by pollutants such as food-born pharmaceuticals, used in livestock for fighting against pathogens and their effects [ 13 , 14 , 15 , 16 ].…”

Reviewing the Role of Vultures at the Human-Wildlife-Livestock Disease Interface: An African Perspective

“…Their highly acidic stomachs (with a pH that can be as low as 1.0) aid in the digestion of tougher food items such as ligaments and bone, but also ensure that most pathogens passing through the gut are destroyed (Houston and Cooper 1975). Studies on the Black (Coragyps atratus) and Turkey (Cathartes aura) Vultures suggest that New World vultures' ability to feed on carcasses that may contain harmful pathogens may not merely lie in their genetic adaptations, but also with a range of associated microbes that reside on their facial skin and in their large intestines (Roggenbuck et al 2014, Zepeda Mendoza et al 2018. Similar studies are lacking on Old World vultures, but it is possible that convergent evolution may have resulted in similar adaptations.…”

“…Similar studies are lacking on Old World vultures, but it is possible that convergent evolution may have resulted in similar adaptations. These protective mechanisms resident in the vulture microbiome highlight the important role that vultures may play in cleaning up carcasses that contain microbes that are pathogenic to other vertebrates (Zepeda Mendoza et al 2018).…”

“…Direct Prevention: Pathogens and the Carcass Environment. A decomposing carcass is a nutrientrich resource for a variety of organisms (Zepeda Mendoza et al 2018, Anderson et al 2019. The first colonizers of a fresh carcass originate foremost from the microbiome carried within the living animal, which may be followed by post-mortem settlement by a range of soil-dwelling bacteria, nematodes, fungi, and insects (Loeffler and Hart 2014, Metcalf et al 2016, Zepeda Mendoza et al 2018.…”

“…A decomposing carcass is a nutrientrich resource for a variety of organisms (Zepeda Mendoza et al 2018, Anderson et al 2019. The first colonizers of a fresh carcass originate foremost from the microbiome carried within the living animal, which may be followed by post-mortem settlement by a range of soil-dwelling bacteria, nematodes, fungi, and insects (Loeffler and Hart 2014, Metcalf et al 2016, Zepeda Mendoza et al 2018. Once it dies, an animal's internal microbiome may become pathogenic, with the resultant toxins being a possible adaptation to outcompete other microbes in the carcass environment (Anzen 1970, Vollaard and Clasener 1994, Zepeda Mendoza et al 2018.…”