Molecular characterization of the microbial communities in the subcaudal gland secretion of the European badger (Meles meles)

FEMS Microbiology Ecology

Volumn 81, Issue 3, 2012, Pages 648-659

  Sin, Yung Wa ^a,b   Buesching, Christina D ^a   Burke, Terry ^b   MacDonald, David W ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Actinobacteria; Mustelid; Scent mark; Semiochemical; Symbiotic bacteria; Terminal restriction fragment length polymorphism

Indexed keywords

BACTERIAL RNA; RNA 16S;

BACTERIUM; MICROBIAL COMMUNITY; MOLECULAR ANALYSIS; MUSTELID; ONTOGENY; POLYMORPHISM; SCENT MARKING; SECRETION; SEMIOCHEMICAL; SYMBIOSIS;

ADULT; ANIMAL; ARTICLE; BACTERIUM; CLASSIFICATION; FEMALE; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MALE; METAGENOME; MICROBIOLOGY; MUSTELIDAE; PHYLOGENY; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SCENT GLAND; SECRETION (PROCESS);

ADULT; ANIMALS; BACTERIA; FEMALE; HUMANS; MALE; METAGENOME; MUSTELIDAE; PHYLOGENY; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; SCENT GLANDS;

ACTINOBACTERIA; BACTERIA (MICROORGANISMS); BACTEROIDETES; FIRMICUTES; MAMMALIA; MELES MELES; MUSTELIDAE; PROTEOBACTERIA;

EID: 84864603559     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2012.01396.x     Document Type: Article

References (58)

1. Albone ES & Perry GC (1975) Anal sac secretion of the red fox, Vulpes vulpes; volatile fatty acids and diamines: implications for a fermentation hypothesis of chemical recognition. J Chem Ecol 2: 101-111.
2. Albone ES & Shirley SG (1984) Mammalian Semiochemistry: The Investigation of Chemical Signals Between Mammals. Wiley, Chichester.
3. Albone ES, Eglinton G, Walker JM & Ware GC (1974) The anal sac secretion of red fox (Vulpes vulpes); its chemistry and microbiology. A comparison with the anal sac secretion of the lion (Panthera leo). Life Sci 14: 387-400.
4. Alexy K, Gassett J, Osborn D, Miller K & Russell S (2003) Bacterial fauna of the tarsal tufts of white-tailed deer (Odocoileus virginianus). Am Midl Nat 149: 237-240.
5. Altschul SF, Gish W, Miller W, Myers EW & Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
6. Amann RI, Ludwig W & Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59: 143-169.
7. Archie EA & Theis KR (2011) Animal behaviour meets microbial ecology. Anim Behav 82: 425-436.
8. Bent SJ, Pierson JD & Forney LJ (2007) Measuring species richness based on microbial community fingerprints: the emperor has no clothes. Appl Environ Microbiol 73: 2399-2401.
9. Brown RE & Macdonald DW (1985) Social Odours in Mammals. Clarendon Press, Oxford.
10. Buesching CD & Macdonald DW (2001) Scent-marking behaviour of the European badger (Meles meles): Resource defence or individual advertisement? Chemical Signals in Vertebrates 9 (Marchlewska-Koj A, Lepri JJ & Müller-Schwarze D, eds), pp. 321-327. Plenum Publishers, New York.
11. Buesching CD & Macdonald DW (2004) Variations in scent-marking behaviour of European badgers Meles meles in the vicinity of their setts. Acta Theriol 49: 235-246.
12. Buesching CD, Newman C & Macdonald DW (2002a) Variations in colour and volume of the subcaudal gland secretion of badgers (Meles meles) in relation to sex, season and individual-specific parameters. Mamm Biol 67: 147-156.
13. Buesching CD, Waterhouse JS & Macdonald DW (2002b) Gas-chromatographic analyses of the subcaudal gland secretion of the European badger (Meles meles) Part I: chemical differences related to individual parameters. J Chem Ecol 28: 41-56.
14. Buesching CD, Waterhouse JS & Macdonald DW (2002c) Gas-chromatographic analyses of the subcaudal gland secretion of the European badger (Meles meles) Part II: time-related variation in the individual-specific composition. J Chem Ecol 28: 57-69.
15. Buesching CD, Stopka P & Macdonald DW (2003) The social function of allo-marking in the European badger (Meles meles). Behaviour 140: 965-980.
16. Buesching CD, Heistermann M & Macdonald DW (2009) Seasonal and inter-individual variation in testosterone levels in badgers Meles meles: evidence for the existence of two endocrinological phenotypes. J Comp Physiol A 195: 865-871.
17. Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Aust J Ecol 18: 117-143.
18. Clarke KR & Gorley RN (2001) Primer v5: User Manual/Tutorial. PRIMER-E, Plymouth, UK.
19. Deplancke B, Hristova KR, Oakley HA, McCracken VJ, Aminov R, Mackie RI & Gaskins HR (2000) Molecular ecological analysis of the succession and diversity of sulfate-reducing bacteria in the mouse gastrointestinal tract. Appl Environ Microbiol 66: 2166-2174.
20. Dugdale HL, Davison D, Baker SE, Ellwood SA, Newman C, Buesching CD & Macdonald DW (2011a) Female teat size is a reliable indicator of annual breeding success in European badgers: genetic validation. Mamm Biol 76: 716-721.
21. Dugdale HL, Pope LC, Newman C, Macdonald DW & Burke T (2011b) Age-specific breeding success in a wild mammalian population: selection, constraint, restraint and senescence. Mol Ecol 20: 3261-3274.
22. Engebretson JJ & Moyer CL (2003) Fidelity of select restriction endonucleases in determining microbial diversity by terminal restriction fragment length polymorphism. Appl Environ Microbiol 69: 4823-4829.
23. Favier CF, Vaughan EE, Vos WMD & Akkermans ADL (2002) Molecular monitoring of succession of bacterial communities in human neonates. Appl Environ Microbiol 68: 219-226.
24. Fell RJ, Buesching CD & Macdonald DW (2006) The social integration of European badger (Meles meles) cubs into their natal group. Behaviour 148: 683-700.
25. Gorman ML (1976) A mechanism for individual recognition by odour in Herpestes auropunctatus (Carnivora: Viverridae). Anim Behav 24: 141-145.
26. Gorman ML, Kruuk H & Leitch A (1984) Social functions of the sub-caudal scent gland secretion of the European badger (Meles meles) (Carnivora: Mustelidae). J Zool 203: 549-559.
27. Gower DB, Nixon A, Jackman PJH & Mallett AI (1986) Transformation of steroids by axillary coryneform bacteria. Int J Cosmet Sci 8: 149-158.
28. Hugenholtz P, Goebel BM & Pace NR (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 476: 5-4774.
29. Kaplan CW, Astaire JC, Sanders ME, Reddy BS & Kitts CL (2001) 16S ribosomal DNA terminal restriction fragment pattern analysis of bacterial communities in feces of rats fed Lactobacillus acidophilus NCFM. Appl Environ Microbiol 67: 1935-1939.
30. Kohl JV, Atzmueller M, Fink B & Grammer K (2001) Human pheromones: integrating neuroendocrinology and ethology. Neuro Endocrinol Lett 22: 309-321.
31. Kruuk H, Gorman ML & Leitch A (1984) Scent-marking with the subcaudal gland by the European badger, Meles meles L. Anim Behav 32: 899-907.
32. Kuhn F & Natsch A (2009) Body odour of monozygotic human twins: a common pattern of odorant carboxylic acids released by a bacterial aminoacylase from axilla secretions contributing to an inherited body odour type. J R Soc Interface 6: 377-392.
33. Lanyon CV, Rushton SP, O'Donnell AG, Goodfellow M, Ward AC, Petrie M, Jensen SP, Gosling LM & Penn DJ (2007) Murine scent mark microbial communities are genetically determined. FEMS Microbiol Ecol 59: 576-583.
34. Liu WT, Marsh TL, Cheng H & Forney LJ (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63: 4516-4522.
35. Lu J, Idris U, Harmon B, Hofacre C, Maurer JJ & Lee MD (2003) Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl Environ Microbiol 69: 6816-6824.
36. Macdonald DW & Newman C (2002) Population dynamics of badgers (Meles meles) in Oxfordshire, UK: numbers, density and cohort life histories, and a possible role of climate change in population growth. J Zool 256: 121-138.
37. Macdonald DW, Newman C, Nouvellet PM & Buesching CD (2009) An analysis of Eurasian badger (Meles meles) population dynamics: implications for regulatory mechanisms. J Mammal 90: 1392-1403.
38. Messing J (1983) New M13 vectors for cloning. Methods Enzymol 101: 20-78.
39. Muyzer G, de Waal EC & Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59: 695-700.
40. Muyzer G, Teske A & Wirsen CO (1995) Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164: 165-172.
41. Natsch A, Derrer S, Flachsmann F & Schmid J (2006) A broad diversity of volatile carboxylic acids, released by a bacterial aminoacylase from axilla secretions, as candidate molecules for the determination of human-body odor type. Chem Biodivers 3: 1-20.
42. Nordstrom NKM & Noble WC (1984) Colonization of the axilla by Propionibacterium avidum in relation to age. Appl Environ Microbiol 47: 1360-1362.
43. Orcutt B, Bailey B, Staudigel H, Tebo BM & Edwards KJ (2009) An interlaboratory comparison of 16S rRNA gene-based terminal restriction fragment length polymorphism and sequencing methods for assessing microbial diversity of seafloor basalts. Environ Microbiol 11: 1728-1735.
44. Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276: 734-740.
45. Ronquist F & Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
46. Roze U, Leung KT, Nix E, Burton G & Chapman DM (2010) Microanatomy and bacterial flora of the perineal glands of the North American porcupine. Can J Zool 88: 59-68.
47. Santelli CM, Orcutt BN, Banning E, Bach W, Moyer CL, Sogin ML, Staudigel H & Edwards KJ (2008) Abundance and diversity of microbial life in ocean crust. Nature 453: 653-656.
48. Schloss PD & Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71: 1501-1506.
49. Sin YW, Dugdale HL, Newman C, Macdonald DW & Burke T (2012a) MHC class II genes in the European badger (Meles meles): characterization, patterns of variation, and transcription analysis. Immunogenetics 64: 313-327.
50. Sin YW, Dugdale HL, Newman C, Macdonald DW, & Burke T (2012b) Evolution of MHC class I genes in the European badger (Meles meles). Ecol & Evol in press.
51. Smith CJ, Danilowicz BS, Clear AK, Costello FJ, Wilson B & Meijer WG (2005) T-Align, a web-based tool for comparison of multiple terminal restriction fragment length polymorphism profiles. FEMS Microbiol Ecol 54: 375-380.
52. Stubbe M (1971) Die analen Markierungsorgane des Dachses (Meles meles). Zool Gart 40: 125-135.
53. Thody AJ & Shuster S (1989) Control and function of sebaceous glands. Physiol Rev 69: 383-408.
54. Ware GC & Gosden PE (1980) Anaerobic microflora of the anal sac of the red fox (Vulpes vulpes). J Chem Ecol 6: 97-102.
55. Weisfeld GE, Czilli T, Phillips KA, Gall JA & Lichtman CM (2003) Possible olfaction-based mechanisms in human kin recognition and inbreeding avoidance. J Exp Child Psychol 85: 279-295.
56. Xu Y, Brereton RG, Trebesius K, Bergmaier I, Oberzaucher E, Grammerc K & Penn DJ (2007) A fuzzy distance metric for measuring the dissimilarity of planar chromatographic profiles with application to denaturing gradient gel electrophoresis data from human skin microbes: demonstration of an individual and gender-based fingerprint. Analyst 132: 638-646.
57. Yamaguchi N, Dugdale HL & Macdonald DW (2006) Female receptivity, embryonic diapause, and superfetation in the European badger (Meles meles): implications for the reproductive tactics of males and females. Q Rev Biol 81: 33-48.
58. Zomer S, Dixon SJ, Xu Y et al. (2009) Consensus multivariate methods in gas chromatography mass spectrometry and denaturing gradient gel electrophoresis: MHC-congenic and other strains of mice can be classified according to the profiles of volatiles and microflora in their scent-marks. Analyst 134: 114-123.