Great Tit (Parus major) Uropygial Gland Microbiomes and Their Potential Defensive Roles.

Katerina Sam,Knud A Jønsson,Nanna R Petersen,Kasun H Bodawatta,Michael Poulsen,Nick Bos,Signe K Schierbech

doi:10.3389/fmicb.2020.01735

Katerina Sam, Knud A Jønsson + Show 5 more

Open Access

https://doi.org/10.3389/fmicb.2020.01735

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Abstract

The uropygial gland (preen gland) of birds plays an important role in maintaining feather integrity and hygiene. Although a few studies have demonstrated potential defensive roles of bacteria residing within these glands, the diversity and functions of the uropygial gland microbiota are largely unknown. Therefore, we investigated the microbiota of great tit (Parus major) uropygial glands through both isolation of bacteria (culture-dependent) and 16S rRNA amplicon sequencing (culture-independent). Co-culture experiments of selected bacterial isolates with four known feather-degrading bacteria (Bacillus licheniformis, Kocuria rhizophila, Pseudomonas monteilii, and Dermacoccus nishinomiyaensis), two non-feather degrading feather bacteria, one common soil bacterial pathogen and two common fungal pathogens enabled us to evaluate the potential antimicrobial properties of these isolates. Our results show major differences between bacterial communities characterized using culture-dependent and -independent approaches. In the former, we were only able to isolate 12 bacterial genera (dominated by members of the Firmicutes and Actinobacteria), while amplicon sequencing identified 110 bacterial genera (dominated by Firmicutes, Bacteroidetes, and Proteobacteria). Uropygial gland bacterial isolates belonging to the genera Bacillus and Kocuria were able to suppress the growth of four of the nine tested antagonists, attesting to potential defensive roles. However, these bacterial genera were infrequent in our MiSeq results suggesting that the isolated bacteria may not be obligate gland symbionts. Furthermore, bacterial functional predictions using 16S rRNA sequences also revealed the ability of uropygial gland bacteria to produce secondary metabolites with antimicrobial properties, such as terpenes. Our findings support that uropygial gland bacteria may play a role in feather health and that bacterial symbionts might act as defensive microbes. Future investigations of these bacterial communities, with targeted approaches (e.g., bacterial isolation and chemical analyses), are thus warranted to improve our understanding of the evolution and function of these host-microbe interactions.

Highlights

Bird feathers provide a plethora of functions varying from flight, insulation and mate attraction (Stettenheim, 1972)
To improve our understanding of uropygial gland microbiomes and their proposed defensive functions against microbial antagonists, we explored P. major uropygial gland microbiomes through culture-dependent and -independent methods and tested for putative antimicrobial properties of a set of uropygial gland bacterial isolates
MiSeq amplicon sequencing revealed a diverse uropygial gland microbiome with representation of the bacterial phyla Firmicutes, Bacteroidetes, and Proteobacteria, and we found high individual variation in these microbiomes, comparable to what has been found in other uropygial microbiome studies (Pearce et al, 2017; Rodríguez-Ruano et al, 2018)

Summary

Introduction

Bird feathers provide a plethora of functions varying from flight, insulation and mate attraction (Stettenheim, 1972). Preening (Delius, 1988), dust bathing (van Liere and Bokma, 1987), and anting (utilization of ants for removal of feather parasites) (Craig, 1999) are all used to keep feathers healthy and free of parasites. Of these feather care strategies, preening is most common, and it includes smearing of secretions from the uropygial (preen) gland onto feathers (Kolattukudy, 1981). There is contradicting evidence on antimicrobial properties (Moreno-Rueda, 2017; Verea et al, 2017; Jacob et al, 2018), a few studies have documented defensive roles of uropygial gland chemical compounds against featherdegrading bacteria (Shawkey et al, 2003; Reneerkens et al, 2008; Møller et al, 2009; Martín-Vivaldi et al, 2010; RuizRodríguez et al, 2015; Fülöp et al, 2016; Verea et al, 2017; Braun et al, 2018a)

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