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The effect of diet on the gastrointestinal microbiome of juvenile rehabilitating green turtles (Chelonia mydas)


Autoři: Jennifer C. G. Bloodgood aff001;  Sonia M. Hernandez aff001;  Anitha Isaiah aff003;  Jan S. Suchodolski aff003;  Lisa A. Hoopes aff004;  Patrick M. Thompson aff005;  Thomas B. Waltzek aff005;  Terry M. Norton aff006
Působiště autorů: Daniel B. Warnell School of Forestry and Natural Resources, University of Georgia, Athens, Georgia, United States of America aff001;  Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, University of Georgia, Athens, Georgia, United States of America aff002;  Gastrointestinal Laboratory, College of Veterinary Medicine and Biomedical Science, Texas A&M University, College Station, Texas, United States of America aff003;  Georgia Aquarium, Atlanta, Georgia, United States of America aff004;  Department of Infectious Diseases and Immunology, College of Veterinary Medicine, University of Florida, Gainesville, Florida, United States of America aff005;  Georgia Sea Turtle Center, Jekyll Island Authority, Jekyll Island, Georgia, United States of America aff006
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227060

Souhrn

Threatened and endangered green turtles (Chelonia mydas) are unique because as juveniles they recruit from pelagic to near-shore waters and shift from an omnivorous to primarily herbivorous diet (i.e. seagrass and algae). Nevertheless, when injured and ill animals are admitted to rehabilitation, animal protein (e.g. seafood) is often offered to combat poor appetite and emaciation. We examined how the fecal microbiome of juvenile green turtles changed in response to a dietary shift during rehabilitation. We collected fecal samples from January 2014 –January 2016 from turtles (N = 17) in rehabilitation at the Georgia Sea Turtle Center and used next generation sequencing to analyze bacterial community composition. Samples were collected at admission, mid-rehabilitation, and recovery, which entailed a shift from a mixed seafood–vegetable diet at admission to a primarily herbivorous diet at recovery. The dominant phyla changed over time, from primarily Firmicutes (55.0%) with less Bacteroidetes (11.4%) at admission, to primarily Bacteroidetes (38.4%) and less Firmicutes (31.8%) at recovery. While the microbiome likely shifts with the changing health status of individuals, this consistent inversion of Bacteroidetes and Firmicutes among individuals likely reflects the increased need for protein digestion, for which Bacteroidetes are important. Firmicutes are significant in metabolizing plant polysaccharides; thus, fewer Firmicutes may result in underutilization of wild diet items in released individuals. This study demonstrates the importance of transitioning rehabilitating green turtles to an herbivorous diet as soon as possible to afford them the best probability of survival.

Klíčová slova:

Antibiotics – Clostridium – Diet – Herbivory – Microbiome – Shannon index – Trophic interactions – Turtles


Zdroje

1. Robinson CJ, Bohannan BJ, Young VB. From structure to function: the ecology of host-associated microbial communities. Microbiol Mol Biol Rev. 2010;74(3):453–476. doi: 10.1128/MMBR.00014-10 20805407

2. Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol. 2013;13(11):790–801. doi: 10.1038/nri3535 24096337

3. Pflughoeft KJ, Versalovic J. Human microbiome in health and disease. Annu Rev Pathol. 2012;7:99–122. doi: 10.1146/annurev-pathol-011811-132421 21910623

4. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, et al. Evolution of mammals and their gut microbes. Science. 2008;320(5883):1647–1651. doi: 10.1126/science.1155725 18497261

5. Rafii F, Sutherland JB, Cerniglia CE. Effects of treatment with antimicrobial agents on the human colonic microflora. Ther Clin Risk Manag. 2008;4(6):1343–1357. doi: 10.2147/tcrm.s4328 19337440

6. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–563. doi: 10.1038/nature12820 24336217

7. Albenberg LG, Wu GD. Diet and the intestinal microbiome: associations, functions, and implications for health and disease. Gastroenterology. 2014;146(6):1564–1572. doi: 10.1053/j.gastro.2014.01.058 24503132

8. Colston TJ, Jackson CR. Microbiome evolution along divergent branches of the vertebrate tree of life: what is known and unknown. Mol Ecol. 2016;25:3776–3800 doi: 10.1111/mec.13730 27297628

9. Seminoff JA. Chelonia mydas. 2004 [cited 24 November 2019]. In: The IUCN Red List of Threatened Species [internet]. Southwest Fisheries Science Center, U.S. Available from: https://www.iucnredlist.org/species/4615/11037468.

10. Abdelrhman KFA, Bacci G, Mancusi C, Mengoni A, Serena F, Ugolini A. A First Insight into the Gut Microbiota of the Sea Turtle Caretta caretta. Front Microbiol. 2016;7:1060. doi: 10.3389/fmicb.2016.01060 27458451

11. Ahasan MS, Waltzek TB, Huerlimann R, Ariel E. Fecal bacterial communities of wild-captured and stranded green turtles (Chelonia mydas) on the Great Barrier Reef. FEMS Microbiol Ecol. 2017;93(12):fix139.

12. Ahasan MS, Waltzek TB, Huerlimann R, Ariel E. Comparative analysis of gut bacterial communities of green turtles (Chelonia mydas) pre-hospitalization and post-rehabilitation by high-throughput sequencing of bacterial 16S rRNA gene. Microbiol Res. 2018;207:91–99. doi: 10.1016/j.micres.2017.11.010 29458874

13. Campos P, Guivernau M, Prenafeta-Boldú FX, Cardona L. Fast acquisition of a polysaccharide fermenting gut microbiome by juvenile green turtles Chelonia mydas after settlement in coastal habitats. Microbiome. 2018;6(1):69. doi: 10.1186/s40168-018-0454-z 29636094

14. Price JT, Paladino FV, Lamont MM, Witherington BE, Bates ST, Soule T. Characterization of the juvenile green turtle (Chelonia mydas) microbiome throughout an ontogenetic shift from pelagic to neritic habitats. PloS One. 2017;12(5):e0177642. doi: 10.1371/journal.pone.0177642 28493980

15. Arizza V, Vecchioni L, Caracappa S, Sciurba G, Berlinghieri F, Gentile A, et al. New insights into the gut microbiome in loggerhead sea turtles Caretta caretta stranded on the Mediterranean coast. PloS one. 2019;14(8):e0220329. doi: 10.1371/journal.pone.0220329 31412070

16. Biagi E, D'Amico F, Soverini M, Angelini V, Barone M, Turroni S, et al. Faecal bacterial communities from Mediterranean loggerhead sea turtles (Caretta caretta). Environ Microbiol Rep. 2019;11(3):361–371. doi: 10.1111/1758-2229.12683 30047254

17. Bjorndal KA, Bolten AB, Chaloupka MY. Green turtle somatic growth model: evidence for density dependence. Ecol Appl. 2000;10(1):269–282.

18. Arthur KE, Boyle MC, Limpus CJ. Ontogenetic changes in diet and habitat use in green sea turtle (Chelonia mydas) life history. Mar Ecol Prog Ser. 2008;362:303–311. doi: 10.3354/meps07440

19. Reich KJ, Bjorndal KA, Bolten AB. The 'lost years' of green turtles: using stable isotopes to study cryptic lifestages. Biol Lett. 2007;3(6):712–714. doi: 10.1098/rsbl.2007.0394 17878144

20. Cardona L, Aguilar A, Pazos L. Delayed ontogenic dietary shift and high levels of omnivory in green turtles (Chelonia mydas) from the NW coast of Africa. Mar Biol. 2009;156(7):1487–1495. doi: 10.1007/s00227-009-1188-z

21. Cardona L, Campos P, Levy Y, Demetropoulos A, Margaritoulis D. Asynchrony between dietary and nutritional shifts during the ontogeny of green turtles (Chelonia mydas) in the Mediterranean. J Exp Mar Bio Ecol. 2010;393(1–2):83–89. doi: 10.1016/j.jembe.2010.07.004

22. González Carman V, Falabella V, Maxwell S, Albareda D, Campagna C, Mianzan H. Revisiting the ontogenetic shift paradigm: the case of juvenile green turtles in the SW Atlantic. J Exp Mar Bio Ecol. 2012;429:64–72.

23. Howell LN, Reich KJ, Shaver DJ, Landry AM Jr, Gorga CC. Ontogenetic shifts in diet and habitat of juvenile green sea turtles in the northwestern Gulf of Mexico. Mar Ecol Prog Ser. 2016;559:217–229.

24. Bjorndal KA, Bolten AB, Chaloupka MY. Green turtle somatic growth model: evidence for density dependence. Ecol Appl. 2000;10(1):269–282.

25. Bloodgood JCG, Norton TM, Hoopes LA, Stacy NI, Hernandez SM. Comparison of hematological, plasma biochemical, and nutritional analytes of rehabilitating and apparaently healthy free-ranging Atlanta green turtles (Chelonia mydas). J Zoo Wildl Med. 2019;50(1):69–81. doi: 10.1638/2017-0250 31120664

26. 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. 2010;7(5):335–336. doi: 10.1038/nmeth.f.303 20383131

27. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72(7):5069–5072. doi: 10.1128/AEM.03006-05 16820507

28. Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R. UniFrac: an effective distance metric for microbial community comparison. ISME J. 2011;5(2):169. doi: 10.1038/ismej.2010.133 20827291

29. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12(6):R60. doi: 10.1186/gb-2011-12-6-r60 21702898

30. Julliand V, Grimm P. Horse Species Symposium: The microbiome of the horse hindgut: History and current knowledge. J Anim Sci. 2016;94(6):2262–2274. doi: 10.2527/jas.2015-0198 27285903

31. Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol. 2008;6(10):776–788. doi: 10.1038/nrmicro1978 18794915

32. Merson SD, Ouwerkerk D, Gulino L-M, Klieve A, Bonde RK, Burgess EA, et al. Variation in the hindgut microbial communities of the Florida manatee, Trichechus manatus latirostris over winter in Crystal River, Florida. FEMS Microbiol Ecol. 2014;87(3):601–615. doi: 10.1111/1574-6941.12248 24215517

33. Hong P-Y, Wheeler E, Cann IK, Mackie RI. Phylogenetic analysis of the fecal microbial community in herbivorous land and marine iguanas of the Galápagos Islands using 16S rRNA-based pyrosequencing. ISME J. 2011;5(9):1461–1470. doi: 10.1038/ismej.2011.33 21451584

34. Eigeland KA, Lanyon JM, Trott DJ, Ouwerkerk D, Blanshard W, Milinovich GJ, et al. Bacterial community structure in the hindgut of wild and captive dugongs (Dugong dugon). Aquat Mamm. 2012;38(4):402–411.

35. Yuan ML, Dean SH, Longo AV, Rothermel BB, Tuberville TD, Zamudio KR. Kinship, inbreeding and fine‐scale spatial structure influence gut microbiota in a hindgut‐fermenting tortoise. Mol Ecol. 2015;24(10):2521–2536. doi: 10.1111/mec.13169 25809385

36. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI. The effect of diet on the human gut microbiome: A metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med. 2009;1(6):6ra14–6ra. doi: 10.1126/scitranslmed.3000322 20368178

37. Zhang X, Peng L, Wang Y, Liang Q, Deng B, Li W, et al. Effect of dietary supplementation of probiotic on performance and intestinal microflora of Chinese soft‐shelled turtle (Trionyx sinensis). Aquac Nutr. 2014;20(6):667–674.

38. Rawski M, Kierończyk B, Świątkiewicz S, Józefiak D. Long-term study on single and multiple species probiotic preparations for Florida softshell turtle (Apalone ferox) nutrition. Anim Sci Pap Rep. 2018;36(1):87–98.

39. Suez J, Zmora N, Zilberman-Schapira G, Mor U, Dori-Bachash M, Bashiardes S, et al. Post-antibiotic gut mucosal microbiome reconstitution is impaired by probiotics and improved by autologous FMT. Cell. 2018;174(6):1406–1423. doi: 10.1016/j.cell.2018.08.047 30193113


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