Does solar irradiation drive community assembly of vulture plumage microbiotas?

Abstract

Background: Stereotyped sunning behaviour in birds has been hypothesized to inhibit keratin-degrading bacteria but there is little evidence that solar irradiation affects community assembly and abundance of plumage microbiota. The monophyletic New World vultures (Cathartiformes) are renowned for scavenging vertebrate carrion, spread-wing sunning at roosts, and thermal soaring. Few avian species experience greater exposure to solar irradiation. We used 16S rRNA sequencing to investigate the plumage microbiota of wild individuals of five sympatric species of vultures in Guyana. Results: The exceptionally diverse plumage microbiotas (631 genera of Bacteria and Archaea) were numerically dominated by bacterial genera resistant to ultraviolet (UV) light, desiccation, and high ambient temperatures, and genera known for forming desiccation-resistant endospores (phylum Firmicutes, order Clostridiales). The extremophile genera Deinococcus (phylum Deinococcus-Thermus) and Hymenobacter (phylum, Bacteroidetes), rare in vertebrate gut microbiotas, accounted for 9.1% of 2.7 million sequences (CSS normalized and log 2 transformed). Five bacterial genera known to exhibit strong keratinolytic capacities in vitro (Bacillus, Enterococcus, Pseudomonas, Staphylococcus, and Streptomyces) were less abundant (totaling 4%) in vulture plumage. Conclusions: Bacterial rank-abundance profiles from melanized vulture plumage have no known analog in the integumentary systems of terrestrial vertebrates. The prominence of UV-resistant extremophiles suggests that solar irradiation may play a significant role in the assembly of vulture plumage microbiotas. Our results highlight the need for controlled in vivo experiments to test the effects of UV on microbial communities of avian plumage.

Plumage microorganism communities of tidal marsh sparrows

“…Compared to the 22 phyla we report in our study, 15 phyla were reported across sympatric skylark ( Lullula arborea ) and woodlark ( Alauda arvensis ) integument and nest material samples, 29 and 22 phyla were reported in plumage samples from five species of sympatric Cathartiformes vultures. 30 Four phyla dominant in this study’s plumage samples – Proteobacteria, Bacteroidota, Actinobacteria, and Firmicutes – are among the dominant phyla in several metabarcoding plumage bacteria studies. 11 , 28 , 29 , 30 The total number of taxa present in our rarefied feather dataset (1,777 SVs) is lower than some studies (∼2,500 taxa in single plumage patches 11 , 30 ), but comparable to those found in lark plumage (∼1,100 29 ) and wild zebra finch ( Taeniopygia guttata) skin swabs (∼1,200 31 ).…”

“… 30 Four phyla dominant in this study’s plumage samples – Proteobacteria, Bacteroidota, Actinobacteria, and Firmicutes – are among the dominant phyla in several metabarcoding plumage bacteria studies. 11 , 28 , 29 , 30 The total number of taxa present in our rarefied feather dataset (1,777 SVs) is lower than some studies (∼2,500 taxa in single plumage patches 11 , 30 ), but comparable to those found in lark plumage (∼1,100 29 ) and wild zebra finch ( Taeniopygia guttata) skin swabs (∼1,200 31 ). Such variation could be due to biological variation or differences in sample collection and molecular methods.…”

“… 53 , 77 , 78 , 79 , 80 Potential specialization to and interaction with the integumentary environment is seen in the dominant phyla of the feather bacteria community, all of which are frequently found in association with avian feathers. 11 , 28 , 29 , 30 Also indicative of specialization to the integument, many of the genera containing keratinolytic taxa detected in this study are often isolated from avian plumage or sources of poultry waste. 2 , 41 , 63 , 81 Several of the taxa detected in the core feather bacterial community and in the genera containing keratinolytic taxa may interact commensally with feathers by regulating microbes; Caulobacter , Pseudoalteromonas , Bacillus , and Pseudomonas each have antimicrobial activity.…”

“…In comparison to plumage microorganism studies on other wild bird species, we report comparable alpha diversity and shared dominant bacterial phyla. 11 , 28 , 29 , 30 Nelson’s sparrows had higher alpha diversity and distinct community composition as compared to saltmarsh, but not seaside, sparrows. However, the differentiation of Nelson’s and saltmarsh bacterial communities was observed when considering presence-absence, and not relative abundance, of taxa.…”

A rather dry subject; investigating the study of arid-associated microbial communities

“…al. found that extremophiles tolerant of UV irradiation (and desiccation) accounted for the most abundant and third most abundant genera resident on pigmented plumage in a number of studied species [ 189 ]; Hymenobacter was the third most abundant genus, and as discussed above, also the most abundant on polar and Mediterranean solar panels as well as UV-irradiated environments in Tibet and Antarctica. Examination of the external surfaces of animals exposed to elevated UV levels, whether through altitude or relative immobility, may also find similarities between these communities and those of environments subject to significant UV irradiation.…”