Microbiota composition of the dorsal patch of reproductive male Leptonycteris yerbabuenae


Autoři: Osiris Gaona aff001;  Daniel Cerqueda-García aff003;  Luisa I. Falcón aff002;  Guillermo Vázquez-Domínguez aff004;  Patricia M. Valdespino-Castillo aff005;  Carla-Ximena Neri-Barrios aff002
Působiště autorů: Posgrado en Ciencias Biológicas de la Universidad Nacional Autonóma de México, Instituto de Ecología, UNAM, Mexico City, México aff001;  Laboratorio de Ecología Bacteriana, Instituto de Ecología, UNAM, Parque Científico y Tecnológico de Yucatán, Mérida, Yucatán, México aff002;  Consorcio de Investigación del Golfo de México (CIGOM), Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, Departamento de Recursos del Mar, Mérida, Yucatán, México aff003;  Laboratorio de Ecología Funcional, Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Morelia, Michoacán, México aff004;  Climate and Ecosystem Sciences Division, Lawrence Berkeley National Laboratory, University of California, Berkeley, California, United States of America aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226239

Souhrn

Bacteria and other types of microbes interact with their hosts in several ways, including metabolic pathways, development, and complex behavioral processes such as mate recognition. During the mating season, adult males of the lesser long-nosed agave pollinator bat Leptonycteris yerbabuenae (Phyllostomidae: Glossophaginae) develop a structure called the dorsal patch, which is located in the interscapular region and may play a role in kin recognition and mate selection. Using high-throughput sequencing of the V4 region of the 16S rRNA gene, we identified a total of 2,847 microbial phylotypes in the dorsal patches of eleven specimens. Twenty-six phylotypes were shared among all the patches, accounting for 30 to 75% of their relative abundance. These shared bacteria are distributed among 13 families, 10 orders, 6 classes and 3 phyla. Two of these common bacterial components of the dorsal patch are Lactococcus and Streptococcus. Some of them—Helcococcus, Aggregatibacter, Enterococcus, and Corynebacteriaceae—include bacteria with pathogenic potential. Half of the shared phylotypes belong to Gallicola, Anaerococcus, Peptoniphilus, Proteus, Staphylococcus, Clostridium, and Peptostreptococcus and specialize in fatty acid production through fermentative processes. This work lays the basis for future symbiotic microbe studies focused on communication and reproduction strategies in wildlife.

Klíčová slova:

Bacteria – Bats – Fatty acids – Host-pathogen interactions – Mammals – Microbiome – Polymerase chain reaction – Sequence databases


Zdroje

1. Lederberg J, McCray AT. ‘Ome Sweet ‘Omics—A Genealogical Treasury of Words. Scientist. 2001;15(7):8.

2. Marchesi JR, Ravel J. The vocabulary of microbiome research: a proposal. Microbiome [Internet]. 2015;3(1). Available from: http://dx.doi.org/10.1186/s40168-015-0094-5

3. Sharpton TJ. Role of the Gut Microbiome in Vertebrate Evolution. mSystems [Internet]. 2018;3(2):e00174–17. Available from: http://dx.doi.org/10.1128/msystems.00174-17 29629413

4. Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes [Internet]. 2012;3(4):289–306. Available from: http://dx.doi.org/10.4161/gmic.19897 22572875

5. Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol [Internet]. 2008;6(10):776–88. Available from: http://dx.doi.org/10.1038/nrmicro1978 18794915

6. Lee YK, Mazmanian SK. Has the Microbiota Played a Critical Role in the Evolution of the Adaptive Immune System? Science (80-) [Internet]. 2010;330(6012):1768–73. Available from: http://dx.doi.org/10.1126/science.1195568

7. Hird SM. Evolutionary Biology Needs Wild Microbiomes. Front Microbiol [Internet]. 2017;8. Available from: http://dx.doi.org/10.3389/fmicb.2017.00725

8. Yeoman CJ, Chia N, Yildirim S, Miller MEB, Kent A, Stumpf R, et al. Towards an Evolutionary Model of Animal-Associated Microbiomes. Entropy [Internet]. 2011;13(3):570–94. Available from: http://dx.doi.org/10.3390/e13030570

9. Christian LM, Galley JD, Hade EM, Schoppe-Sullivan S, Kamp Dush C, Bailey MT. Gut microbiome composition is associated with temperament during early childhood. Brain Behav Immun [Internet]. 2015;45:118–27. Available from: http://dx.doi.org/10.1016/j.bbi.2014.10.018 25449582

10. Moeller AH, Caro-Quintero A, Mjungu D, Georgiev AV, Lonsdorf E V, Muller MN, et al. Cospeciation of gut microbiota with hominids. Science (80-) [Internet]. 2016;353(6297):380–2. Available from: http://dx.doi.org/10.1126/science.aaf3951

11. Ross AA, Rodrigues Hoffmann A, Neufeld JD. The skin microbiome of vertebrates. Microbiome. 2019;7(79):1–14.

12. Archie EA, Tung J. Social behavior and the microbiome. Curr Opin Behav Sci [Internet]. 2015;6:28–34. Available from: http://dx.doi.org/10.1016/j.cobeha.2015.07.008

13. Lizé A, McKay R, Lewis Z. Gut microbiota and kin recognition. Trends Ecol Evol [Internet]. 2013;28(6):325–6. Available from: http://dx.doi.org/10.1016/j.tree.2012.10.013 23141109

14. Archie EA, Theis KR. Animal behaviour meets microbial ecology. Anim Behav [Internet]. 2011;82(3):425–36. Available from: http://dx.doi.org/10.1016/j.anbehav.2011.05.029

15. Bullard RW. Wild canid associations with fermentation products. Ind Eng Chem Prod Res Dev [Internet]. 1982;21(4):646–55. Available from: http://dx.doi.org/10.1021/i300008a028

16. Voigt CC, Caspers B, Speck S. Bats, bacteria, and bat smell: Sex-specific diversity of microbes in a sexually selected scent organ. J Mammal [Internet]. 2005;86(4):745–9. Available from: http://dx.doi.org/10.1644/1545-1542(2005)086[0745:bbabss]2.0.co

17. 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 [Internet]. 1974;14(2):387–400. Available from: http://dx.doi.org/10.1016/0024-3205(74)90069-1 4813597

18. Leclaire S, Nielsen JF, Drea CM. Bacterial communities in meerkat anal scent secretions vary with host sex, age, and group membership. Behav Ecol. 2014;1–9.

19. Theis KR, Schimid TM, Holekamp KE. Evidence for a bacterial mechanism for group-specific social odors among hyenas. Sci Rep. 2012;2(615):1–8.

20. Bloss J, Acree TE, Bloss JM, Hood WR, Kunz TH. Potential use of chemical cues for colony-mate recognition in the big brown bat, Eptesicus fuscus. J Chem Ecol [Internet]. 2002;28(4):819–34. Available from: http://dx.doi.org/10.1023/a:1015296928423 12035929

21. Muñoz-Romo M, Kunz TH. Dorsal Patch and Chemical Signaling in Males of the Long-Nosed Bat, Leptonycteris curasoae (Chiroptera: Phyllostomidae). J Mammal [Internet]. 2009 Oct 15;90(5):1139–47. Available from: http://dx.doi.org/10.1644/08-MAMM-A-324.1

22. Rincón-Vargas F, Stoner KE, Vigueras-Villaseñor RM, Nassar JM, Chaves ÓM, Hudson R. Internal and external indicators of male reproduction in the lesser long-nosed bat Leptonycteris yerbabuenae. J Mammal [Internet]. 2013;94(2):488–96. Available from: http://dx.doi.org/10.1644/11-mamm-a-357.1

23. Martínez-Coronel M, Hortelano-Moncada Y, Corral V, Cuevas LR. Relationship Between Subcutaneous Fat and Reproductive Activity in Males of Leptonycteris yerbabuenae in Los Laguitos Cave, Chiapas, Mexico. Front Reprod Sci Reprod Biol Physiol Biochem male bats [Internet]. 2017;27(1):36–48. Available from: http://dx.doi.org/10.2174/9781681085548117010006

24. Voigt CC, Schwarzenberger F. Reproductive Endocrinology of a Small Tropical Bat (Female Saccopteryx bilineata; Emballonuridae) Monitored by Fecal Hormone Metabolites. J Mammal [Internet]. 2008;89(1):50–7. Available from: http://dx.doi.org/10.1644/06-mamm-a-432.1

25. Muñoz-Romo M, Burgos J, Kunz T. Smearing behaviour of male Leptonycteris curasoae (Chiroptera) and female responses to the odour of dorsal patches. Behaviour [Internet]. 2011;148(4):461–83. Available from: http://dx.doi.org/10.1163/000579511x564287

26. Nassar JM, Salazar MV, Quintero A, Stoner KE, Gómez M, Cabrera A, et al. Seasonal sebaceous patch in the nectar-feeding bats Leptonycteris curasoae and L. yerbabuenae (Phyllostomidae: Glossophaginae): phenological, histological, and preliminary chemical characterization. Zoology [Internet]. 2008;111(5):363–76. Available from: http://dx.doi.org/10.1016/j.zool.2007.10.006 18602804

27. Nassar JM, Galicia R, Ibarra A, Medellin RA. Tracking the origin of the smearing behavior in long-nosed bats (Leptonycteris spp.). Mamm Biol. 2016;81(6):623–7.

28. Muñoz-Romo M, Nielsen LT, Nassar JM, Kunz TH. Chemical Composition of the Substances from Dorsal Patches of Males of the Curaçaoan Long-Nosed Bat, Leptonycteris curasoae (Phyllostomidae: Glossophaginae). Acta Chiropterologica [Internet]. 2012;14(1):213–24. Available from: http://dx.doi.org/10.3161/150811012x654411

29. Morales-Garza MR, Arizmendi M del C, Campos JE, Martínez-Garcia M, Valiente-Banuet A. Evidences on the migratory movements of the nectar-feeding bat Leptonycteris curasoae in Mexico using random amplified polymorphic DNA (RAPD). J Arid Environ [Internet]. 2007;68(2):248–59. Available from: http://dx.doi.org/10.1016/j.jaridenv.2006.05.009

30. Rojas-Martínez A, Valiente-Banuet A, del Coro Arizmendi M, Alcántara-Eguren A, Arita HT. Seasonal distribution of the long-nosed bat (Leptonycteris curasoae) in North America: does a generalized migration pattern really exist? J Biogeogr [Internet]. 1999;26(5):1065–77. Available from: http://dx.doi.org/10.1046/j.1365-2699.1999.00354.x

31. Rzedowski J. Vegetación de México. Mexico City: Limusa; 1978.

32. García E. Modificaciones al sistema de clasificación climática de Koppen. Universidad Nacional Autónoma de México; 1978.

33. Dávila P, Villaseñor JL, Medina R, Ramírez A, Salinas A, Sánchez-Ken J, et al. Flora del Valle de Tehuacán-Cuicatlán. Listados florísticos de México X. Mexico City; 1993.

34. Kunz TH, Betke M, Hristov NI, Vonhof MJ. Methods for assessing colony size, population size, and relative abundance of bats. In: Kunz TH, Parsons S, editors. Ecological and behavioral methods for the study of bats. 2nd ed. Baltimore, Maryland: Johns Hopkins University Press; 2009. p. 133–57.

35. Gannon WL, Sikes RS. Guidelines of the American Society of Mammalogists for the Use of Wild Mammals in Research. J Mammal [Internet]. 2007;88(3):809–23. Available from: http://dx.doi.org/10.1644/06-mamm-f-185r1.1

36. Gardner AL. Feeding habits. In: Baker RJ, Jones J, Knox J, Carter DC, editors. Biology of bats of the New World Family Phyllostomatidae, Part II. Lubbock, TX: Special Publications of The Museum of Texas Tech University; 1979. p. 293–350.

37. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J [Internet]. 2012;6(8):1621–4. Available from: http://dx.doi.org/10.1038/ismej.2012.8 22402401

38. Magoc T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics [Internet]. 2011;27(21):2957–63. Available from: http://dx.doi.org/10.1093/bioinformatics/btr507 21903629

39. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods [Internet]. 2010;7(5):335–6. Available from: http://dx.doi.org/10.1038/nmeth.f.303 20383131

40. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, et al. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods [Internet]. 2013;10(1):57–9. Available from: http://dx.doi.org/10.1038/nmeth.2276 23202435

41. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics [Internet]. 2010;26(19):2460–1. Available from: http://dx.doi.org/10.1093/bioinformatics/btq461 20709691

42. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics [Internet]. 2011;27(16):2194–200. Available from: http://dx.doi.org/10.1093/bioinformatics/btr381 21700674

43. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, et al. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J [Internet]. 2012;6(3):610–8. Available from: http://dx.doi.org/10.1038/ismej.2011.139 22134646

44. McMurdie PJ, Holmes S. phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS One [Internet]. 2013;8(4):e61217. Available from: http://dx.doi.org/10.1371/journal.pone.0061217 23630581

45. Wickham H. Ggplot2: elegant graphics for data analysis. Berlin: Springer Science and Business Media; 2009.

46. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res [Internet]. 2004;32(5):1792–7. Available from: http://dx.doi.org/10.1093/nar/gkh340 15034147

47. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0. Syst Biol [Internet]. 2010;59(3):307–21. Available from: http://dx.doi.org/10.1093/sysbio/syq010 20525638

48. Caliendo AM, Jordan CD, Ruoff KL. Helcococcus, a new genus of catalase-negative, gram-positive cocci isolated from clinical specimens. J Clin Microbiol. 1995;33:1638–9. 7650202

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 [Internet]. 1999;5(5):555–9. Available from: http://dx.doi.org/10.1006/anae.1999.0197

50. Smit G, Smit B, Engels W. Flavour formation by lactic acid bacteria and biochemical flavour profiling of cheese products. FEMS Microbiol Rev [Internet]. 2005;29(3):591–610. Available from: http://dx.doi.org/10.1016/j.femsre.2005.04.002 15935512

51. Ezaki T, Li N, Shu S, Zhao L, Kawamura Y, Li ZY. 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 [Internet]. 2001;51(4):1521–8. Available from: http://dx.doi.org/10.1099/00207713-51-4-1521

52. 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 [Internet]. 2013;110(49):19832–7. Available from: http://dx.doi.org/10.1073/pnas.1306477110 24218592

53. Soso SB, Koziel JA. Characterizing the scent and chemical composition of Panthera leo marking fluid using solid-phase microextraction and multidimensional gas chromatography–mass spectrometry-olfactometry. Sci Rep [Internet]. 2017;7(1). Available from: http://dx.doi.org/10.1038/s41598-017-04973-2

54. González-Quiñonez N, Fermin G, Muñoz-Romo M. Diversity of bacteria in the sexually selected epaulettes of the little yellow-shouldered bat Sturnira lilium (Chiroptera: Phyllostomidae). Interciencia. 2014;39(12):882–9.

55. Bienenstock J, Kunze WA, Forsythe P. Disruptive physiology: olfaction and the microbiome-gut-brain axis. Biol Rev [Internet]. 2018;93(1):390–403. Available from: http://dx.doi.org/10.1111/brv.12348 28675687


Článek vyšel v časopise

PLOS One


2019 Číslo 12