Unveiled feather microcosm: feather microbiota of passerine birds is closely associated with host species identity and bacteriocin-producing bacteria

Abstract

The functional relevance of microbiota is a key aspect for understanding host–microbiota interactions. Mammalian skin harbours a complex consortium of beneficial microorganisms known to provide health and immune-boosting advantages. As yet, however, little is known about functional microbial communities on avian feathers, including their co-evolution with the host and factors determining feather microbiota (FM) diversity. Using 16S rRNA profiling, we investigated how host species identity, phylogeny and geographic origin determine FM in free-living passerine birds. Moreover, we estimated the relative abundance of bacteriocin-producing bacteria (BPB) and keratinolytic feather damaging bacteria (FDB) and evaluated the ability of BPB to affect FM diversity and relative abundance of FDB. Host species identity was associated with feather bacterial communities more strongly than host geographic origin. FM functional properties differed in terms of estimated BPB and FDB relative abundance, with both showing interspecific variation. FM diversity was negatively associated with BPB relative abundance across species, whereas BPB and FDB relative abundance was positively correlated. This study provides the first thorough evaluation of antimicrobial peptides-producing bacterial communities inhabiting the feather integument, including their likely potential to mediate niche-competition and to be associated with functional species-specific feather microbiota in avian hosts.

An introduction to phylosymbiosis

“…Matrix correlation methods identify phylosymbiosis by comparing the similarities between host-derived and microbial-derived distance matrices. Methods implemented in phylosymbiosis studies [20,21,39,50,[65][66][67][68][69][70][71][72] include variations of the Mantel test, which statistically evaluates the linear correlation between all corresponding elements from two independent matrices by permutation [73] and the more powerful Procrustean superimposition approach, which rotates and fits two matrices to minimize their differences association [74]. Partial Mantel tests [75] measuring correlations between two matrices while controlling for the effects of a third variable described in another matrix are also used to evaluate associations between microbial communities and multiple aspects of host characteristics, such as phylogeny, identity, genetic distances and geographical distances [39,66,67,69].…”

Does solar irradiation drive community assembly of vulture plumage microbiotas?

“…A significant fraction (13.5%) of the 631 bacterial and archaeal genera detected in the 16S rRNA survey were taxonomically unclassified in SILVA database [51]. More than 70% of the bacterial and archaeal genera detected in our analyses have not been previously reported in the associated tables and appendices of published papers that investigated plumage microbiota with 16S rRNA sequencing [5,6,[17][18][19][20][21][22][23][24]27]. Vulture plumage microbiotas can accurately be described as hyper-diverse and taxonomically cryptic.…”

“…Microbial keratinases target cross-linked structural peptides that make feather keratin insoluble [15]. The continued focus on domestic poultry and keratinolytic bacteria has resulted in a substantial void in our knowledge of the taxonomic diversity, host specificity, and assembly of microbial communities in the plumage of the 10,135 wild bird species [5,6,[17][18][19][20][21][22][23][24][25][26][27][28].…”

Interspecific variation in deterioration and degradability of avian feathers: the evolutionary role of microorganisms

“…Feather degradation by keratinolytic bacteria occurs in wild birds (Leclaire et al , Kent and Burtt , but see Cristol et al ), which for instance, might have consequences in scenarios of sexual selection (Shawkey et al , , Ruiz‐Rodríguez et al ) and survival (Møller et al ). Moreover, bacterial communities of avian feathers vary interspecifically (Javůrková et al ). Detecting evidence of interspecific variation in feather wear in standard conditions could suggest the existence of interspecific variation in environmental factors associated with the risk of feather deterioration, including bacterial environment (Kent and Burtt ).…”

“…Detecting evidence of interspecific variation in feather wear in standard conditions could suggest the existence of interspecific variation in environmental factors associated with the risk of feather deterioration, including bacterial environment (Kent and Burtt ). Moreover, since these environmental factors likely vary among species (see above), natural selection could have favoured the evolution of characteristics that counteract or reduce feather degradation by keratinolytic bacteria in environments that are distinctive of each species (Burtt , Burtt et al , Javůrková et al ). If this was the case, we should find interspecific variation in traits functioning in preventing feathers’ wear (Burtt ) such as feather susceptibility to degradation by keratinolytic bacteria (hereafter, feather degradability) (Ruiz‐De‐Castañeda et al , , Ruiz‐Rodríguez et al ).…”