Bacteria isolated from Bengal cat (Felis catus × Prionailurus bengalensis) anal sac secretions produce volatile compounds potentially associated with animal signaling


Autoři: Mei S. Yamaguchi aff001;  Holly H. Ganz aff002;  Adrienne W. Cho aff002;  Thant H. Zaw aff002;  Guillaume Jospin aff002;  Mitchell M. McCartney aff001;  Cristina E. Davis aff001;  Jonathan A. Eisen aff002;  David A. Coil aff002
Působiště autorů: Department of Mechanical and Aerospace Engineering, University of California, Davis, California, United States of America aff001;  Genome Center, University of California, Davis, California, United States of America aff002;  Department of Evolution and Ecology, University of California, Davis, California, United States of America aff003;  Department of Medical Microbiology and Immunology, University of California, Davis, Davis, California, United States of America aff004
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0216846

Souhrn

In social animals, scent secretions and marking behaviors play critical roles in communication, including intraspecific signals, such as identifying individuals and group membership, as well as interspecific signaling. Anal sacs are an important odor producing organ found across the carnivorans (species in the mammalian Order Carnivora). Secretions from the anal sac may be used as chemical signals by animals for behaviors ranging from defense to species recognition to signaling reproductive status. In addition, a recent study suggests that domestic cats utilize short-chain free fatty acids in anal sac secretions for individual recognition. The fermentation hypothesis is the idea that symbiotic microorganisms living in association with animals contribute to odor profiles used in chemical communication and that variation in these chemical signals reflects variation in the microbial community. Here we examine the fermentation hypothesis by characterizing volatile organic compounds (VOC) and bacteria isolated from anal sac secretions collected from a male Bengal cat (Felis catus × Prionailurus bengalensis), a cross between the domestic cat and the leopard cat. Both left and right anal sacs of a male Bengal cat were manually expressed (emptied) and collected. Half of the material was used to culture bacteria or to extract bacterial DNA and the other half was used for VOC analysis. DNA was extracted from the anal sac secretions and used for a 16S rRNA gene PCR amplification and sequencing based characterization of the microbial community. Additionally, some of the material was plated out in order to isolate bacterial colonies. Three taxa (Bacteroides fragilis, Tessaracoccus, and Finegoldia magna) were relatively abundant in the 16S rRNA gene sequence data and also isolated by culturing. Using Solid Phase Microextraction (SPME) gas chromatography-mass spectrometry (GC-MS), we tentatively identified 52 compounds from the Bengal cat anal sac secretions and 67 compounds from cultures of the three bacterial isolates chosen for further analysis. Among 67 compounds tentatively identified from bacterial isolates, 51 were also found in the anal sac secretion. We show that the bacterial community in the anal sac consists primarily of only a few abundant taxa and that isolates of these taxa produce numerous volatiles that are found in the combined anal sac volatile profile. Several of these volatiles are found in anal sac secretions from other carnivorans, and are also associated with known bacterial biosynthesis pathways. This is consistent with the fermentation hypothesis and the possibility that the anal sac is maintained at least in part to house bacteria that produce volatiles for the host.

Klíčová slova:

Biology and life sciences – Physiology – Physiological processes – Secretion – Organisms – Eukaryota – Animals – Vertebrates – Amniotes – Mammals – Cats – Animal types – Domestic animals – Bacteria – Anaerobic bacteria – Gut bacteria – Bacteroides – Biochemistry – Nucleic acids – RNA – Non-coding RNA – Ribosomal RNA – Ribosomes – Lipids – Fatty acids – Cell biology – Cellular structures and organelles – Psychology – Behavior – Animal behavior – Animal communication – Zoology – Medicine and health sciences – Social sciences


Zdroje

1. Feldman HN. Methods of scent marking in the domestic cat. Can J Zool. 1994;72: 1093–1099.

2. Nordstrom NK, Noble WC. Colonization of the axilla by Propionibacterium avidum in relation to age. Appl Environ Microbiol. 1984;47: 1360–1362. 6742846

3. Gorman ML, Trowbridge BJ. The Role of Odor in the Social Lives of Carnivores. Carnivore Behavior, Ecology, and Evolution. 1989. pp. 57–88.

4. McColl I. The comparative anatomy and pathology of anal glands. Arris and Gale lecture delivered at the Royal College of Surgeons of England on 25th February 1965. Ann R Coll Surg Engl. 1967;40: 36–67. 6016560

5. Wood WF, Sollers BG, Dragoo GA, Dragoo JW. Volatile components in defensive spray of the hooded skunk, Mephitis macroura. J Chem Ecol. 2002;28: 1865–1870. 12449512

6. Begg CM, Begg KS, Du Toit JT, Mills MGL. Scent-marking behaviour of the honey badger, Mellivora capensis (Mustelidae), in the southern Kalahari. Anim Behav. 2003;66: 917–929.

7. Drea CM, Vignieri SN, Sharon Kim H, Weldele ML, Glickman SE. Responses to olfactory stimuli in spotted hyenas (Crocuta crocuts): II. Discrimination of conspecific scent. J Comp Psychol. 2002;116: 342–349. 12539929

8. Raymer J, Wiesler D, Novotny M, Asa C, Seal US, Mech LD. Chemical investigations of wolf (Canis lupus) anal-sac secretion in relation to breeding season. J Chem Ecol. 1985;11: 593–608. doi: 10.1007/BF00988570 24310125

9. Asa CS, David Mech L, Seal US. The use of urine, faeces, and anal-gland secretions in scent-marking by a captive wolf (Canis lupus) pack. Anim Behav. 1985;33: 1034–1036.

10. Clapperton BK, Kay Clapperton B, Minot EO, Crump DR. An olfactory recognition system in the ferret Mustela furo L. (Carnivora: Mustelidae). Anim Behav. 1988;36: 541–553.

11. Zhang JX, Soini HA, Bruce KE, Wiesler D, Woodley SK, Baum MJ, et al. Putative chemosignals of the ferret (Mustela furo) associated with individual and gender recognition. Chem Senses. 2005;30: 727–737. doi: 10.1093/chemse/bji065 16221798

12. Gorman ML. A mechanism for individual recognition by odour in Herpestes auropunctatus (Carnivora: Viverridae). Anim Behav. 1976;24: 141–145.

13. Zhang J-X, Liu D, Sun L, Wei R, Zhang G, Wu H, et al. Potential chemosignals in the anogenital gland secretion of giant pandas, Ailuropoda melanoleuca, associated with sex and individual identity. J Chem Ecol. 2008;34: 398–407. doi: 10.1007/s10886-008-9441-3 18293041

14. Theis KR, Venkataraman A, Dycus JA, Koonter KD, Schmitt-Matzen EN, Wagner AP, et al. Symbiotic bacteria appear to mediate hyena social odors. Proc Natl Acad Sci U S A. 2013;110: 19832–19837. doi: 10.1073/pnas.1306477110 24218592

15. Burgener N, Dehnhard M, Hofer H, East ML. Does anal gland scent signal identity in the spotted hyaena? Anim Behav. 2009;77: 707–715.

16. Rosell F, Jojola SM, Ingdal K, Lassen BA, Swenson JE, Arnemo JM, et al. Brown bears possess anal sacs and secretions may code for sex. J Zool. 2010;283: 143–152.

17. Yuan H, Liu D, Sun L, Wei R, Zhang G, Sun R. Anogenital gland secretions code for sex and age in the giant panda, Ailuropoda melanoleuca. Can J Zool. 2004;82: 1596–1604.

18. Zhang J-X, Sun L, Zhang Z-B, Wang Z-W, Chen Y, Wang R. Volatile compounds in anal gland of Siberian weasels (Mustela sibirica) and steppe polecats (M. eversmanni). J Chem Ecol. 2002;28: 1287–1297. 12184403

19. Leclaire S, Jacob S, Greene LK, Dubay GR, Drea CM. Social odours covary with bacterial community in the anal secretions of wild meerkats. Sci Rep. 2017;7: 3240. doi: 10.1038/s41598-017-03356-x 28607369

20. Miyazaki M, Miyazaki T, Nishimura T, Hojo W, Yamashita T. The Chemical Basis of Species, Sex, and Individual Recognition Using Feces in the Domestic Cat. J Chem Ecol. 2018;44: 364–373. doi: 10.1007/s10886-018-0951-3 29637491

21. Bininda-Emonds ORP, Decker-Flum DM, Gittleman JL. The utility of chemical signals as phylogenetic characters: an example from the Felidae. Biol J Linn Soc Lond. 2001;72: 1–15.

22. Albone ES, Perry GC. 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. 1976;2: 101–111.

23. Apps P, Mmualefe L, Weldon McNutt J. Identification of volatiles from the secretions and excretions of African wild dogs (Lycaon pictus). J Chem Ecol. 2012;38: 1450–1461. doi: 10.1007/s10886-012-0206-7 23129124

24. Decker DM, Ringelberg D, White DC. Lipid components in anal scent sacs of three mongoose species (Helogale parvula, Crossarchus obscurus, Suricata suricatta). J Chem Ecol. 1992;18: 1511–1524. doi: 10.1007/BF00993225 24254283

25. Preti G. Volatile constituents of dog (Canis Familiaris) and coyote (Canis Latrans) anal sacs. J Chem Ecol. 1976;2: 177–186.

26. Raymer J, Wiesler D, Novotny M, Asa C, Seal US, Mech LD. Chemical investigations of wolf (Canis lupus) anal-sac secretion in relation to breeding season. J Chem Ecol. 1985;11: 593–608. doi: 10.1007/BF00988570 24310125

27. Albone ES, Eglinton G, Walker JM, Ware GC. The anal sac secretion of the red fox (Vulpes vulpes); its chemistry and microbiology. A comparison with the anal sac secretion of the lion (Panthera leo). Life Sci. 1974;14: 387–400. doi: 10.1016/0024-3205(74)90069-1 4813597

28. Poddar-Sarkar M, Brahmachary RL. Putative semiochemicals in the African cheetah (Acinonyx jubatus). J Lipid Mediat Cell Signal. 1997;15: 285–287. 9041477

29. Hefetz A, Ben-Yaacov R, Yom-Tov Y. Sex specificity in the anal gland secretion of the Egyptian mongoose Herpestes ichneumon. J Zool. 2009;203: 205–209.

30. Gorman M, Nedwell DB, Smith RM. An analysis of the contents of the anal scent pockets of Herpestes auropunctatus (Carnivora: Viverridae). J Zool. 2009;172: 389–399.

31. Albone ES, Shirley SG. Mammalian semiochemistry: the investigation of chemical signals between mammals. John Wiley & Son Ltd; 1984.

32. Li Q, Korzan WJ, Ferrero DM, Chang RB, Roy DS, Buchi M, et al. Synchronous evolution of an odor biosynthesis pathway and behavioral response. Curr Biol. 2013;23: 11–20. doi: 10.1016/j.cub.2012.10.047 23177478

33. al-Waiz M, Mikov M, Mitchell SC, Smith RL. The exogenous origin of trimethylamine in the mouse. Metabolism. 1992;41: 135–136. doi: 10.1016/0026-0495(92)90140-6 1736035

34. Martín-Vivaldi M, Peña A, Peralta-Sánchez JM, Sánchez L, Ananou S, Ruiz-Rodríguez M, et al. Antimicrobial chemicals in hoopoe preen secretions are produced by symbiotic bacteria. Proc Biol Sci. 2010;277: 123–130. doi: 10.1098/rspb.2009.1377 19812087

35. Comeau AM, Douglas GM, Langille MGI. Microbiome Helper: a Custom and Streamlined Workflow for Microbiome Research. mSystems. 2017;2: pii: e00127–16.

36. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13: 581–583. doi: 10.1038/nmeth.3869 27214047

37. Edgar RC, Flyvbjerg H. Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics. 2015;31: 3476–3482. doi: 10.1093/bioinformatics/btv401 26139637

38. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41: D590–6. doi: 10.1093/nar/gks1219 23193283

39. Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E, Quast C, et al. The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res. 2014;42: D643–8. doi: 10.1093/nar/gkt1209 24293649

40. Glöckner FO, Yilmaz P, Quast C, Gerken J, Beccati A, Ciuprina A, et al. 25 years of serving the community with ribosomal RNA gene reference databases and tools. J Biotechnol. 2017;261: 169–176. doi: 10.1016/j.jbiotec.2017.06.1198 28648396

41. Lee DW, Lee SD. Tessaracoccus flavescens sp. nov., isolated from marine sediment. Int J Syst Evol Microbiol. 2008;58: 785–789. doi: 10.1099/ijs.0.64868-0 18398170

42. Cai M, Wang L, Cai H, Li Y, Wang Y-N, Tang Y-Q, et al. Salinarimonas ramus sp. nov. and Tessaracoccus oleiagri sp. nov., isolated from a crude oil-contaminated saline soil. Int J Syst Evol Microbiol. 2011;61: 1767–1775. doi: 10.1099/ijs.0.025932-0 20802058

43. Seck E, Traore SI, Khelaifia S, Beye M, Michelle C, Couderc C, et al. Tessaracoccus massiliensis sp. nov., a new bacterial species isolated from the human gut. New Microbes New Infect. 2016;13: 3–12. doi: 10.1016/j.nmni.2016.05.002 27358740

44. Li G-D, Chen X, Li Q-Y, Xu F-J, Qiu S-M, Jiang Y, et al. Tessaracoccus rhinocerotis sp. nov., isolated from the faeces of Rhinoceros unicornis. Int J Syst Evol Microbiol. 2016;66: 922–927. doi: 10.1099/ijsem.0.000812 26621119

45. Finster KW, Cockell CS, Voytek MA, Gronstal AL, Kjeldsen KU. Description of Tessaracoccus profundi sp.nov., a deep-subsurface actinobacterium isolated from a Chesapeake impact crater drill core (940 m depth). Antonie Van Leeuwenhoek. 2009;96: 515–526. doi: 10.1007/s10482-009-9367-y 19669589

46. Xu J, Bjursell MK, Himrod J, Deng S, Carmichael LK, Chiang HC, et al. A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science. 2003;299: 2074–2076. doi: 10.1126/science.1080029 12663928

47. Slots J, Listgarten MA. Bacteroides gingivalis, Bacteroides intermedius and Actinobacillus actinomycetemcomitans in human periodontal diseases. J Clin Periodontol. 1988;15: 85–93. doi: 10.1111/j.1600-051x.1988.tb00999.x 3279073

48. Song Y, Finegold SM. Peptostreptococcus, Finegoldia, Anaerococcus, Peptoniphilus, Veillonella, and other anaerobic cocci. Manual of Clinical Microbiology, 10th Edition. American Society of Microbiology; 2011. pp. 803–816.

49. Murdoch DA, Shah HN. Reclassification of Peptostreptococcus magnus (Prevot 1933) Holdeman and Moore 1972 as Finegoldia magna comb. nov. and Peptostreptococcus micros (Prevot 1933) Smith 1957 as Micromonas micros comb. nov. Anaerobe. Elsevier; 1999;5: 555–559.

50. Ezaki T, Kawamura Y, Li N, Li ZY, Zhao L, Shu S. Proposal of the genera Anaerococcus gen. nov., Peptoniphilus gen. nov. and Gallicola gen. nov. for members of the genus Peptostreptococcus. Int J Syst Evol Microbiol. 2001;51: 1521–1528. doi: 10.1099/00207713-51-4-1521 11491354

51. Jang SS, Breher JE, Dabaco LA, Hirsh DC. Organisms isolated from dogs and cats with anaerobic infections and susceptibility to selected antimicrobial agents. J Am Vet Med Assoc. 1997;210: 1610–1614. 9170087

52. Lawhon SD, Taylor A, Fajt VR. Frequency of resistance in obligate anaerobic bacteria isolated from dogs, cats, and horses to antimicrobial agents. J Clin Microbiol. 2013;51: 3804–3810. doi: 10.1128/JCM.01432-13 24025899

53. Kämpfer P, Lodders N, Warfolomeow I, Busse H-J. Tessaracoccus lubricantis sp. nov., isolated from a metalworking fluid. Int J Syst Evol Microbiol.; 2009;59: 1545–1549. doi: 10.1099/ijs.0.006841-0 19502351

54. Maszenan AM, Seviour RJ, Patel BK, Schumann P, Rees GN. Tessaracoccus bendigoensis gen. nov., sp. nov., a gram-positive coccus occurring in regular packages or tetrads, isolated from activated sludge biomass. Int J Syst Bacteriol.; 1999;49 Pt 2: 459–468.

55. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215: 403–410. doi: 10.1016/S0022-2836(05)80360-2 2231712

56. Whitman WB, Rainey F, Kämpfer P, Trujillo M, Chun J, DeVos P, et al., editors. Bacteroides. Bergey’s Manual of Systematics of Archaea and Bacteria. Chichester, UK: John Wiley & Sons, Ltd; 2015. pp. 1–24.

57. Love DN, Johnson JL, Moore LV. Bacteroides species from the oral cavity and oral-associated diseases of cats. Vet Microbiol. 1989;19: 275–281. doi: 10.1016/0378-1135(89)90073-4 2718354

58. Kirchoff NS, Udell MAR, Sharpton TJ. The gut microbiome correlates with conspecific aggression in a small population of rescued dogs (Canis familiaris). PeerJ. 2019;7: e6103. doi: 10.7717/peerj.6103 30643689

59. Dewhirst FE, Klein EA, Bennett M-L, Croft JM, Harris SJ, Marshall-Jones ZV. The feline oral microbiome: a provisional 16S rRNA gene based taxonomy with full-length reference sequences. Vet Microbiol. 2015;175: 294–303. doi: 10.1016/j.vetmic.2014.11.019 25523504

60. Gnanandarajah JS, Johnson TJ, Kim HB, Abrahante JE, Lulich JP, Murtaugh MP. Comparative faecal microbiota of dogs with and without calcium oxalate stones. J Appl Microbiol. 2012;113: 745–756. doi: 10.1111/j.1365-2672.2012.05390.x 22788835

61. Albone ES, Grönnerberg TO. Lipids of the anal sac secretions of the red fox, Vulpes vulpes and of the lion, Panthera leo. J Lipid Res. 1977;18: 474–479. 894139

62. Parales RE, Parales JV, Pelletier DA, Ditty JL. Chapter 1 Diversity of Microbial Toluene Degradation Pathways. Advances in Applied Microbiology. 2008. pp. 1–73.

63. Heider J. Anaerobic bacterial metabolism of hydrocarbons. FEMS Microbiol Rev. 1998;22: 459–473.

64. Schulz S, Dickschat JS. Bacterial volatiles: the smell of small organisms. Nat Prod Rep. 2007;24: 814–842. doi: 10.1039/b507392h 17653361

65. Stirling LA, Watkinson RJ, Higgins IJ. Microbial Metabolism of Alicyclic Hydrocarbons: Isolation and Properties of a Cyclohexane-degrading Bacterium. J Gen Microbiol. 1977;99: 119–125.

66. Tonzetich J, McBride BC. Characterization of volatile sulphur production by pathogenic and non-pathogenic strains of oral Bacteroides. Arch Oral Biol. 1981;26: 963–969. doi: 10.1016/0003-9969(81)90104-7 6122435

67. Kiviranta H, Tuomainen A, Reiman M, Laitinen S, Liesivuori J, Nevalainen A. Qualitative identification of volatile metabolites from two fungi and three bacteria species cultivated on two media. Cent Eur J Public Health. 1998;6: 296–299. 9919382

68. Dickschat JS. Identification, Synthesis, and Biosynthesis of Volatiles from Diverse Bacteria. PhD Thesis, TU Braunschweig, 2005.

69. Haslam E. Metabolites of the Shikimate Pathway. The Shikimate Pathway. London: Butterworths. 1974. pp. 80–127.


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