Exploring the associations between preen oil bacterial, chemical and proteomic profiles of passerines

. 2025 Oct 16 ; 118 (11) : 173. [epub] 20251016

Jazyk angličtina Země Nizozemsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid41099795

Grantová podpora
OCENW.KLEIN.541 Nederlandse Organisatie voor Wetenschappelijk Onderzoek
14-16861P Grantová Agentura České Republiky
RVO: 68081766 Institutional Research Support of the Czech Academy of Sciences

Odkazy

PubMed 41099795
PubMed Central PMC12531318
DOI 10.1007/s10482-025-02182-w
PII: 10.1007/s10482-025-02182-w
Knihovny.cz E-zdroje

Preen gland bacteria are thought to be the key producers of preen oil components such as chemosignalling molecules including volatile organic compounds (VOCs) and antimicrobial compounds including peptides and antimicrobial VOCs. However, data on the preen oil bacteriome and chemical composition are limited to a small subset of bird species, and the presence of antimicrobial peptides is largely unexplored. Here, we performed an exploratory study to characterize, for the first time, the preen oil chemical and proteomic profiles and to explore the possible contribution of the bacteriome to the production of preen oil VOCs and antimicrobial peptides (bacteriocins) in eight passerine species, each represented by a single individual. Preen oil bacteriome, chemical and proteomic profiles varied among birds. The bacterial profiles were dominated by the genera Streptococcus, Lactococcus, Corynebacterium and Cutibacterium. The chemical profiles mainly consisted of alcohols, ketones and carboxylic acids. The biological functions primarily associated with the proteomic profiles were proteolysis and response to oxidative stress. Although we were unable to explore a direct association between the bacteriome and chemical profiles, the preen oil contained bacteriocin- and VOC-producing bacterial genera capable of producing detected microbially-derived VOCs (mVOCs), the relative abundance of which varied between birds. Riparian species showed the highest chemical diversity and high abundances of putative preen oil mVOC-producing bacteria, which could suggest habitat-specific adaptations. This exploratory study may significantly contribute to the formulation of hypotheses on the potential role of host ecological factors in the variation of preen oil bacterial, chemical and proteomic profiles in passerines.

Zobrazit více v PubMed

Alves Soares T, Caspers BA, Loos HM (2024) Volatile organic compounds in preen oil and feathers—a review. Biol Rev 99:1085–1099 PubMed

Biester EM, Hellenbrand J, Gruber J, Hamberg M, Frentzen M (2012) Identification of avian wax synthases. BMC Biochem 13:4. 10.1186/1471-2091-13-4 PubMed PMC

Bisignano G, Laganà MG, Trombetta D, Arena S, Nostro A, Uccella N, Mazzanti G, Saija A (2001) In vitro antibacterial activity of some aliphatic aldehydes from PubMed

Bodawatta KH, Schierbech SK, Petersen NR, Sam K, Bos N, Jønsson KA, Poulsen M (2020) Great tit ( PubMed PMC

Bolyen E, Rideout JR, Dillon MR et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. 10.1038/s41587-019-0209-9 PubMed PMC

Braun MS, Sporer F, Zimmermann S, Wink M (2018) Birds, feather-degrading bacteria and preen glands: the antimicrobial activity of preen gland secretions from turkeys ( PubMed

Buchberger A, Bukau B, Sommer T (2010) Protein quality control in the cytosol and the endoplasmic reticulum: brothers in arms. Mol Cell 40:238–252. 10.1016/j.molcel.2010.10.001 PubMed

Burger BV, Reiter B, Borzyk O, du Plessis MA (2004) Avian exocrine secretions. I. Chemical characterization of the volatile fraction of the uropygial secretion of the green woodhoopoe, PubMed

Burtt EH Jr, Ichida JM (2004) Gloger’s rule, feather-degrading bacteria, and color variation among song sparrows. Condor 106:681–686. 10.1093/condor/106.3.681

Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583 PubMed PMC

Callewaert L, Michiels CW (2010) Lysozymes in the animal kingdom. J Biosci (Bangalore) 35:127–160. 10.1007/s12038-010-0015-5

Carneiro D, Czirják GÁ, Rowe M (2020) Innate and adaptive immune proteins in the preen gland secretions of male house sparrows. J Avian Biol. 10.1111/jav.02556

Chadeganipour M, Haims A (2001) Antifungal activities of pelargonic and capric acid on PubMed

Chawawisit K, Bhoopong P, Phupong W, Lertcanawanichakul M (2015) 2, 4-Di-tert-butylphenol, the bioactive compound produced by

Czirják GÁ, Pap PL, Vágási CI, Giraudeau M, Mureşan C, Mirleau P, Heeb P (2013) Preen gland removal increases plumage bacterial load but not that of feather-degrading bacteria. Naturwissenschaften 100:145–151 PubMed

Díez-Fernández A, Martínez-de la Puente J, Martín J, Gangoso L, López P, Soriguer R, Figuerola J (2021) Sex and age, but not blood parasite infection nor habitat, affect the composition of the uropygial gland secretions in European blackbirds. J Avian Biol. 10.1111/jav.02630

Directive 2010/75/EU (2010) Directive 2010/75/EU of the European Parliament and of the Council of 24 November 2010 on industrial emissions (integrated pollution prevention and control). https://eur-lex.europa.eu/eli/dir/2010/75/oj/eng

Dormont L, Mulatier M, Carrasco D, Cohuet A (2021) Mosquito attractants. J Chem Ecol 47:351–393. 10.1007/s10886-021-01261-2 PubMed

Douglas HD (2008) Prenuptial perfume: Alloanointing in the social rituals of the crested auklet ( PubMed

Douglas HD (2013) Colonial seabird’s paralytic perfume slows lice down: an opportunity for parasite-mediated selection? Int J Parasitol 43:399–407 PubMed

Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) Uchime improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200 PubMed PMC

Engel K, Sauer J, Jünemann S, Winkler A, Wibberg D, Kalinowski J, Tauch A, Caspers BA (2018) Individual- and species-specific skin microbiomes in three different estrildid finch species revealed by 16S amplicon sequencing. Microb Ecol 76:518–529. 10.1007/s00248-017-1130-8 PubMed

Fernando WGD, Ramarathnam R, Krishnamoorthy AS, Savchuk SC (2005) Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol Biochem 37:955–964

Ferreira JP, Alves D, Neves O, Silva J, Gibbs PA, Teixeira PC (2010) Effects of the components of two antimicrobial emulsions on food-borne pathogens. Food Control 21:227–230

Fliegerova K, Tapio I, Bonin A et al (2014) Effect of DNA extraction and sample preservation method on rumen bacterial population. Anaerobe 29:80–84 PubMed

Ganesan T, Subban M, Christopher Leslee DB, Kuppannan SB, Seedevi P (2022) Structural characterization of n-hexadecanoic acid from the leaves of

Gehrke ITS, Neto AT, Pedroso M, Mostardeiro CP, Da Cruz IBM, Silva UF, Ilha V, Dalcol II, Morel AF (2013) Antimicrobial activity of PubMed

Giraudeau M, Czirják GÁ, Duval C, Bretagnolle V, Gutierrez C, Guillon N, Heeb P (2013) Effect of preen oil on plumage bacteria: an experimental test with the mallard. Behav Processes 92:1–5 PubMed

González m, Venter gJ, López s, Iturrondobeitia jC, Goldarazena a (2014) Laboratory and field evaluations of chemical and plant-derived potential repellents against PubMed

Grieves LA, Gloor GB, Kelly TR, Bernards MA, MacDougall-Shackleton EA (2021) Preen gland microbiota of songbirds differ across populations but not sexes. J Anim Ecol 90:2202–2212 PubMed

Grieves LA, Gilles M, Cuthill IC, Székely T, MacDougall-Shackleton EA, Caspers BA (2022) Olfactory camouflage and communication in birds. Biol Rev 97:1193–1209. 10.1111/brv.12837 PubMed

Grieves LA, Gloor GB (2025) Uropygial gland microbiota of nearctic−neotropical migrants vary with season and migration distance. Animal Microbiome 7:11. 10.1186/s42523-024-00367-8 PubMed PMC

Hammami R, Zouhir A, Le Lay C, Ben Hamida J, Fliss I (2010) BACTIBASE second release: a database and tool platform for bacteriocin characterization. BMC Microbiol 10:22. 10.1186/1471-2180-10-22 PubMed PMC

Heilbronner S, Krismer B, Brötz-Oesterhelt H, Peschel A (2021) The microbiome-shaping roles of bacteriocins. Nat Rev Microbiol 19:726–739. 10.1038/s41579-021-00569-w PubMed

Huang CB, Alimova Y, Myers TM, Ebersole JL (2011) Short- and medium-chain fatty acids exhibit antimicrobial activity for oral microorganisms. Arch Oral Biol 56:650–654 PubMed PMC

Inouye S, Takizawa T, Yamaguchi H (2001) Antibacterial activity of essential oils and their major constituents against respiratory tract pathogens by gaseous contact. J Antimicrob Chemother 47:565–573. 10.1093/jac/47.5.565 PubMed

Jackson DA (1995) PROTEST: a PROcrustean randomization TEST of community environment concordance. Ecoscience 2:297–303. 10.1080/11956860.1995.11682297

Jacob J, Ziswiler V (1982) The uropygial gland. Avian Biol 6:199–324

Javůrková VG, Kreisinger J, Procházka P, Požgayová M, Ševčíková K, Brlík V, Adamík P, Heneberg P, Porkert J (2019) Unveiled feather microcosm: feather microbiota of passerine birds is closely associated with host species identity and bacteriocin-producing bacteria. ISME J 13:2363–2376. 10.1038/s41396-019-0438-4 PubMed PMC

Jiang H, Lei R, Ding S-W, Zhu S (2014) Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinformatics 15:182. 10.1186/1471-2105-15-182 PubMed PMC

Kemmler E, Lemfack MC, Goede A, Gallo K, Toguem SM, Ahmed W, Millberg I, Preissner S, Piechulla B, Preissner R (2025) mVOC 4.0: a database of microbial volatiles. Nucleic Acids Res 53:D1692–D1696 PubMed PMC

Krassowski M (2021) ComplexUpset: create complex UpSet plots using “ggplot2” components. R package version 1.3.3

Kubo I, Muroi H, Kubo A (1993) Antibacterial activity of long-chain alcohols against

Lammers A, Zweers H, Sandfeld T, Bilde T, Garbeva P, Schramm A, Lalk M (2021) Antimicrobial compounds in the volatilome of social spider communities. Front Microbiol. 10.3389/fmicb.2021.700693 PubMed PMC

Law-Brown J (2001) Chemical defence in the red-billed wood hoopoe:

Lee J-H, Kim Y-G, Khadke SK, Lee J (2021) Antibiofilm and antifungal activities of medium-chain fatty acids against PubMed PMC

Liu X (2022) Understanding semi-volatile organic compounds in indoor dust. Indoor Built Environ 31:291–298 PubMed PMC

Logan JG, Seal NJ, Cook JI, Stanczyk NM, Birkett MA, Clark SJ, Pickett JA (2009) Identification of human-derived volatile chemicals that interfere with attraction of the scottish biting midge and their potential use as repellents. J Med Entomol 46(2):208–219. 10.1603/033.046.0205 PubMed

Logan JG, Stanczyk NM, Hassanali A, Kemei J, Santana AEG, Ribeiro KAL, Pickett JA, Mordue AJ (2010) Arm-in-cage testing of natural human-derived mosquito repellents. Malar J 9:239. 10.1186/1475-2875-9-239 PubMed PMC

Magallanes S, Møller AP, García-Longoria L, de Lope F, Marzal A (2016) Volume and antimicrobial activity of secretions of the uropygial gland are correlated with malaria infection in house sparrows. Parasit Vectors 9:232. 10.1186/s13071-016-1512-7 PubMed PMC

Martínez-Renau E, Mazorra-Alonso M, Ruiz-Castellano C, Martín-Vivaldi M, Martín-Platero AM, Barón MD, Soler JJ (2022) Microbial infection risk predicts antimicrobial potential of avian symbionts. Front Microbiol. 10.3389/fmicb.2022.1010961 PubMed PMC

Martín-Platero AM, Valdivia E, Ruíz-Rodríguez M, Soler JJ, Martín-Vivaldi M, Maqueda M, Martínez-Bueno M (2006) Characterization of antimicrobial substances produced by PubMed PMC

Martín-Vivaldi M, Peña A, Peralta-Sánchez JM, Sánchez L, Ananou S, Ruiz-Rodríguez M, Soler JJ (2010) Antimicrobial chemicals in hoopoe preen secretions are produced by symbiotic bacteria. Proc R Soc B 277:123–130 PubMed PMC

Meade E, Slattery MA, Garvey M (2020) Bacteriocins, potent antimicrobial peptides and the fight against multi drug resistant species: resistance is futile? Antibiotics 9:32 PubMed PMC

Møller AP, Erritzøe J, Rózsa L (2010) Ectoparasites, uropygial glands and hatching success in birds. Oecologia 163:303–311. 10.1007/s00442-009-1548-x PubMed

Moreno-Rueda G (2011) House sparrows

Moreno-Rueda G (2017) Preen oil and bird fitness: a critical review of the evidence. Biol Rev 92:2131–2143 PubMed

Muthamil S, Prasath KG, Priya A, Precilla P, Pandian SK (2020) Global proteomic analysis deciphers the mechanism of action of plant derived oleic acid against PubMed PMC

Mweresa CK, Mukabana WR, Omusula P, Otieno B, Van Loon JJA, Takken W (2016) Enhancing attraction of African malaria vectors to a synthetic odor blend. J Chem Ecol 42:508–516. 10.1007/s10886-016-0711-1 PubMed

Nandakumar R, Talapatra K (2014) Quantitative profiling of bacteriocins present in dairy-free probiotic preparations of PubMed

Oksanen J, Simpson G, Blanchet F et al. (2022) Vegan: community ecology package, R Package Version 2.6-4

Pearce DS, Hoover BA, Jennings S, Nevitt GA, Docherty KM (2017) Morphological and genetic factors shape the microbiome of a seabird species ( PubMed PMC

Peres-Neto PR, Jackson DA (2001) How well do multivariate data sets match? The advantages of a Procrustean superimposition approach over the Mantel test. Oecologia 129:169–178. 10.1007/s004420100720 PubMed

Popova AA, Koksharova OA, Lipasova VA, Zaitseva JV, Katkova-Zhukotskaya OA, Eremina SI, Mironov AS, Chernin LS, Khmel IA (2014) Inhibitory and toxic effects of volatiles emitted by strains of PubMed PMC

Potier S, Besnard MM, Schikorski D, Buatois B, Duriez O, Gabirot M, Leclaire S, Bonadonna F (2018) Preen oil chemical composition encodes individuality, seasonal variation and kinship in black kites

Puri SN, Mendki MJ, Sukumaran D, Ganesan K, Prakash S, Sekhar K (2014) Electroantennogram and behavioral responses of

Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. 10.1093/nar/gks1219 PubMed PMC

Radrova J, Seblova V, Votypka J (2013) Feeding behavior and spatial distribution of PubMed

Rappsilber J, Mann M, Ishihama Y (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using stagetips. Nat Protoc 2:1896–1906. 10.1038/nprot.2007.261 PubMed

Rodríguez-Ruano SM, Martín-Vivaldi M, Peralta-Sánchez JM, García-Martín AB, Martínez-García Á, Soler JJ, Valdivia E, Martínez-Bueno M (2018) Seasonal and sexual differences in the microbiota of the Hoopoe uropygial secretion. Genes 9:407 PubMed PMC

Roggenbuck M, Bærholm Schnell I, Blom N, Bælum J, Bertelsen MF, Sicheritz-Pontén T, Sørensen SJ, Gilbert MTP, Graves GR, Hansen LH (2014) The microbiome of New World vultures. Nat Commun 5:5498. 10.1038/ncomms6498 PubMed

Ruiz-Rodríguez M, Valdivia E, Soler JJ, Martín-Vivaldi M, Martín-Platero AM, Martínez-Bueno M (2009) Symbiotic bacteria living in the hoopoe’s uropygial gland prevent feather degradation. J Exp Biol 212:3621–3626. 10.1242/jeb.031336 PubMed

Ruiz-Rodríguez M, Valdivia E, Martín-Vivaldi M, Martín-Platero AM, Martínez-Bueno M, Méndez M, Peralta-Sánchez JM, Soler JJ (2012) Antimicrobial activity and genetic profile of PubMed PMC

Ruiz-Rodríguez M, Martínez-Bueno M, Martín-Vivaldi M, Valdivia E, Soler JJ (2013) Bacteriocins with a broader antimicrobial spectrum prevail in enterococcal symbionts isolated from the hoopoe’s uropygial gland. FEMS Microbiol Ecol 85:495–502. 10.1111/1574-6941.12138 PubMed

Ruiz-Rodríguez M, Tomás G, Martín-Gálvez D, Ruiz-Castellano C, Soler JJ (2015) Bacteria and the evolution of honest signals. The case of ornamental throat feathers in spotless starlings. Funct Ecol 29:701–709. 10.1111/1365-2435.12376

Sahin N, Kula I, Erdogan Y (2006) Investigation of antimicrobial activities of nonanoic acid derivatives. Fresenius Environ Bull 15:141–143

Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, Turner P, Parkhill J, Loman NJ, Walker AW (2014) Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol 12:87. 10.1186/s12915-014-0087-z PubMed PMC

Seidel V, Taylor PW (2004) In vitro activity of extracts and constituents of PubMed

Shaw CL, Rutter JE, Austin AL, Garvin MC, Whelan RJ (2011) Volatile and semivolatile compounds in Gray Catbird uropygial secretions vary with age and between breeding and wintering grounds. J Chem Ecol 37:329–339. 10.1007/s10886-011-9931-6 PubMed

Shawkey MD, Pillai SR, Hill GE (2003) Chemical warfare? Effects of uropygial oil on feather-degrading bacteria. J Avian Biol 34:345–349

Soini HA, Schrock SE, Bruce KE, Wiesler D, Ketterson ED, Novotny MV (2007) Seasonal variation in volatile compound profiles of preen gland secretions of the dark-eyed junco ( PubMed

Soini HA, Whittaker DJ, Wiesler D, Ketterson ED, Novotny MV (2013) Chemosignaling diversity in songbirds: chromatographic profiling of preen oil volatiles in different species. J Chromatogr 1317:186–192

Soler JJ, Martín-Vivaldi M, Ruiz-Rodríguez M, Valdivia E, Martín-Platero AM, Martínez-Bueno M, Peralta-Sánchez JM, Méndez M (2008) Symbiotic association between hoopoes and antibiotic-producing bacteria that live in their uropygial gland. Funct Ecol 22:864–871

Soler JJ, Barón MD, Martínez-Renau E, Zhang L, Liang W, Martín-Vivaldi M (2024) Nesting hoopoes cultivate in their uropygial gland the microbial symbionts with the highest antimicrobial capacity. Scientific Reports 14:30797. 10.1038/s41598-024-81062-1 PubMed PMC

Soudy M, Anwar AM, Ahmed EA, Osama A, Ezzeldin S, Mahgoub S, Magdeldin S (2020) UniprotR: retrieving and visualizing protein sequence and functional information from universal protein resource (UniProt knowledgebase). J Proteomics 213:103613 PubMed

Spanoudis CG, Wondwosen B, Isberg E, Andreadis SS, Kline DL, Birgersson G, Ignell R (2022) The chemical code for attracting

Šta̕stný K, Hudec K (2011) Fauna ČR Ptáci 3/II. 2nd edn. Academia (Středisko spol. činností AV ČR, v. v. i.), Prague

Tao N, Jia L, Zhou H (2014) Anti-fungal activity of PubMed

Tomás G, Zamora-Muñoz C, Martín-Vivaldi M, Barón MD, Ruiz-Castellano C, Soler JJ (2020) Effects of chemical and auditory cues of Hoopoes (

Tuttle EM, Sebastian PJ, Posto AL, Soini HA, Novotny MV, Gonser RA (2014) Variation in preen oil composition pertaining to season, sex, and genotype in the polymorphic white-throated sparrow. J Chem Ecol 40:1025–1038. 10.1007/s10886-014-0493-2 PubMed

van Veelen HPJ, Falcao Salles J, Tieleman BI (2017) Multi-level comparisons of cloacal, skin, feather and nest-associated microbiota suggest considerable influence of horizontal acquisition on the microbiota assembly of sympatric woodlarks and skylarks. Microbiome 5:156. 10.1186/s40168-017-0371-6 PubMed PMC

Videvall E, Marzal A, Magallanes S, Fleischer RC, Espinoza K, García-Longoria L (2021) The uropygial gland microbiome of house sparrows with malaria infection. J Avian Biol. 10.1111/jav.02686

Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267 PubMed PMC

Weldon PJ, Carroll JF, Kramer M, Bedoukian RH, Coleman RE, Bernier UR (2011) Anointing chemicals and hematophagous arthropods: responses by ticks and mosquitoes to citrus ( PubMed

Werner D, Groschupp S, Bauer C, Kampen H (2020) Breeding habitat preferences of major PubMed PMC

Whittaker DJ, Gerlach NM, Slowinski SP, Corcoran KP, Winters AD, Soini HA, Novotny MV, Ketterson ED, Theis KR (2016) Social environment has a primary influence on the microbial and odor profiles of a chemically signaling songbird. Front Ecol Evol. 10.3389/fevo.2016.00090

Whittaker DJ, Slowinski SP, Greenberg JM, Alian O, Winters AD, Ahmad MM, Burrell MJE, Soini HA, Novotny MV, Ketterson ED, Theis KR (2019) Experimental evidence that symbiotic bacteria produce chemical cues in a songbird. J Exp Biol. 10.1242/jeb.202978 PubMed

Whittaker DJ, Hagelin JC (2021) Female-Based Patterns and Social Function in Avian Chemical Communication. J Chem Ecol 47:43–62. 10.1007/s10886-020-01230-1 PubMed

Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York. 10.1007/978-3-319-24277-4

Yao M, Rosenfeld J, Attridge S, Sidhu S, Aksenov V, Rollo CD (2009) The ancient chemistry of avoiding risks of predation and disease. Evol Biol 36:267–281. 10.1007/s11692-009-9069-4

Zhang J-X, Sun L, Zuo M-X (2009) Uropygial gland volatiles may code for olfactory information about sex, individual, and species in Bengalese finches

Zhao F, Wang P, Lucardi RD, Su Z, Li S (2020) Natural sources and bioactivities of 2,4-Di-Tert-Butylphenol and its analogs. Toxins 12:35 PubMed PMC

Zhu JJ, Cermak SC, Kenar JA et al (2018) Better than DEET repellent compounds derived from coconut oil. Sci Rep 8:14053. 10.1038/s41598-018-32373-7 PubMed PMC

Zou J, Jiang H, Cheng H, Fang J, Huang G (2018) Strategies for screening, purification and characterization of bacteriocins. Int J Biol Macromol 117:781–789 PubMed

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...