Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: Implications for conservation

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Barelli, Claudia ^a,b,c   Albanese, Davide ^a   Donati, Claudio ^a   Pindo, Massimo ^a   Dallago, Chiara ^a   Rovero, Francesco ^b   Cavalieri, Duccio ^a   Michael Tuohy, Kieran ^a   Christine Hauffe, Heidi ^a   De Filippo, Carlotta ^a,d  

^a RESEARCH AND INNOVATION CENTRE   (Italy)

^b MUSE Museo delle Scienze   (Italy)

^c GERMAN PRIMATE CENTER   (Germany)

^d CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AGRICULTURE; ANIMAL; BACTEROIDETES; BIODIVERSITY; CHEMISTRY; CLASSIFICATION; COLOBUS; DIET; ECOSYSTEM; ENDANGERED SPECIES; ENVIRONMENTAL PROTECTION; FECES; FIRMICUTES; HUMAN; INTESTINE FLORA; MICROBIOLOGY; PHYLOGENY; PHYSIOLOGY; PLANT; PROTEOBACTERIA; SPIROCHAETA; TANZANIA; VERRUCOMICROBIA;

AGRICULTURE; ANIMALS; BACTEROIDETES; BIODIVERSITY; COLOBUS; CONSERVATION OF NATURAL RESOURCES; DIET; ECOSYSTEM; ENDANGERED SPECIES; FECES; FIRMICUTES; GASTROINTESTINAL MICROBIOME; HUMANS; PHYLOGENY; PLANTS; PROTEOBACTERIA; SPIROCHAETA; TANZANIA; VERRUCOMICROBIA;

EID: 84943338759     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep14862     Document Type: Article

References (62)

1. Ley, R. E., Peterson, D. A., Gordon, J. I. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124, 837-848, doi: 10.1016/j.cell.2006.02.017 (2006).
2. Ley, R. E. et al. Evolution of mammals and their gut microbes. Science 320, 1647-1651, doi: 10.1126/science.1155725 (2008).
3. Ley, R. E., Lozupone, C. A., Hamady, M., Knight, R., Gordon, J. I. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6, 776-788, doi: 10.1038/nrmicro1978 (2008).
4. Turnbaugh, P. J. et al. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 1, 6ra14, doi: 10.1126/scitranslmed.3000322 (2009).
5. Russell, J. A. et al. Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc Natl Acad Sci USA 106, 21236-21241, doi: 10.1073/pnas.0907926106 (2009).
6. Sekirov, I., Russell, S. L., Antunes, L. C., Finlay, B. B. Gut microbiota in health and disease. Physiol Rev 90, 859-904, doi: 10.1152/physrev.00045.2009 (2010).
7. Sharon, G. et al. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci USA 107, 20051-20056, doi: 10.1073/pnas.1009906107 (2010).
8. Koch, H., Schmid-Hempel, P. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci USA 108, 19288-19292, doi: 10.1073/pnas.1110474108 (2011).
9. Tsunemoto, H. et al. [A case report of redo A-C bypass for MCLS performed 13 years after initial surgery]. Kokyu To Junkan 38, 1031-1034 (1990).
10. McFall-Ngai, M. et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA 110, 3229-3236, doi: 10.1073/pnas.1218525110 (2013).
11. De Filippo, C. et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 107, 14691-14696, doi: 10.1073/pnas.1005963107 (2010).
12. Muegge, B. D. et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332, 970-974, doi: 10.1126/science.1198719 (2011).
13. Wu, G. D. et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105-108, doi: 10.1126/science.1208344 (2011).
14. Ochman, H. et al. Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol 8, e1000546, doi: 10.1371/journal.pbio.1000546 (2010).
15. Moeller, A. H. et al. Rapid changes in the gut microbiome during human evolution. Proc Natl Acad Sci USA 111, 16431-16435, doi: 10.1073/pnas.1419136111 (2014).
16. Sullam, K. E. et al. Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Mol Ecol 21, 3363-3378, doi: 10.1111/j.1365-294X.2012.05552.x (2012).
17. Lankau, E. W., Hong, P. Y., Mackie, R. I. Ecological drift and local exposures drive enteric bacterial community differences within species of Galapagos iguanas. Mol Ecol 21, 1779-1788, doi: 10.1111/j.1365-294X.2012.05502.x (2012).
18. Hird, S. M., Carstens, B. C., Cardiff, S. W., Dittmann, D. L., Brumfield, R. T. Sampling locality is more detectable than taxonomy or ecology in the gut microbiota of the brood-parasitic Brown-headed Cowbird (Molothrus ater). PeerJ 2, e321, doi: 10.7717/peerj.321 (2014).
19. Phillips, C. D. et al. Microbiome analysis among bats describes influences of host phylogeny, life history, physiology and geography. Mol Ecol 21, 2617-2627, doi: 10.1111/j.1365-294X.2012.05568.x (2012).
20. Linnenbrink, M. et al. The role of biogeography in shaping diversity of the intestinal microbiota in house mice. Mol Ecol 22, 1904-1916, doi: 10.1111/mec.12206 (2013).
21. Amato, K. R. et al. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J 7, 1344-1353, doi: 10.1038/ismej.2013.16 (2013).
22. McCord, A. I. et al. Fecal microbiomes of non-human primates in Western Uganda reveal species-specific communities largely resistant to habitat perturbation. Am J Primatol 76, 347-354, doi: 10.1002/ajp.22238 (2014).
23. Struhsaker, T. T. et al. Demographic Variation Among Udzungwa Red Colobus in Relation to Gross Ecological and Sociological Parameters. Int J Primatol 25, 615-658, doi: 10.1023/B:IJOP.0000023578.08343.4e (2004).
24. Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A., Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853-858, doi: 10.1038/35002501 (2000).
25. Mittermeier, R. A. et al. Hotspots Revisited: Earth's Biologically Richest and Most Endangered Terrestrial Ecoregions (Conservation International, 2005).
26. Rovero, F. et al. Targeted vertebrate surveys enhance the faunal importance and improve explanatory models within the Eastern Arc Mountains of Kenya and Tanzania. Diversity Distrib. 20, 1438-1449, doi: 10.1111/ddi.12246 (2014).
27. Marshall, A. R. Ecological report on Magombera forest (2008).
28. Rovero, F., Mtui, A. S., Kitegile, A. S., Nielsen, M. R. Hunting or habitat degradation? Decline of primate populations in Udzungwa Mountains, Tanzania: An analysis of threats. Biological Conservation 146, 89-96, doi: 10.1016/j.biocon.2011.09.017 (2012).
29. Marshall, A. R. Disturbance in the Udzungwas: responses of monkeys and trees to forest degradation, University of York (2007).
30. Steel, R. I. The Effects of Habitat Parameters on the Behavior, Ecology, and Conservation of the Udzungwa Red Colobus Monkey (Procolobus gordonorum). Ph.D. Thesis, Duke University, USA (2012).
31. Yildirim, S. et al. Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities. PLoS One 5, e13963, doi: 10.1371/journal.pone.0013963 (2010).
32. Engel, P., Moran, N. A. The gut microbiota of insects-diversity in structure and function. FEMS Microbiol Rev 37, 699-735, doi: 10.1111/1574-6976.12025 (2013).
33. Biddle, A., Stewart, L., Blanchard, J., Leschine, S. Untangling the Genetic Basis of Fibrolytic Specialization by Lachnospiraceae and Ruminococcaceae in Diverse Gut Communities. Diversity 5, 627-640, doi: 10.3390/d5030627 (2013).
34. Brulc, J. M. et al. Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc Natl Acad Sci USA 106, 1948-1953, doi: 10.1073/pnas.0806191105 (2009).
35. Ding, S. Y. et al. Cellulosomal scaffoldin-like proteins from Ruminococcus flavefaciens. J Bacteriol 183, 1945-1953, doi: 10.1128/jb.183.6.1945-1953.2001 (2001).
36. Albanese, D., De Filippo, C., Cavalieri, D., Donati, C. Explaining diversity in metagenomic datasets by phylogenetic-based feature weighting. PLoS Comput Biol 11, e1004186, doi: 10.1371/journal.pcbi.1004186 (2015).
37. Warnecke, F. et al. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450, 560-565, doi: 10.1038/nature06269 (2007).
38. Obregon-Tito, A. J. et al. Subsistence strategies in traditional societies distinguish gut microbiomes. Nat Commun 6, 6505, doi: 10.1038/ncomms7505 (2015).
39. Schnorr, S. L. et al. Gut microbiome of the Hadza hunter-gatherers. Nat Commun 5, 3654, doi: 10.1038/ncomms4654 (2014).
40. Lozupone, C., Lladser, M. E., Knights, D., Stombaugh, J., Knight, R. UniFrac: an effective distance metric for microbial community comparison. ISME J 5, 169-172, doi: 10.1038/ismej.2010.133 (2011).
41. Tung, J. et al. Social networks predict gut microbiome composition in wild baboons. Elife 4, doi: 10.7554/eLife.05224 (2015).
42. Martinez, I. et al. The gut microbiota of rural papua new guineans: composition, diversity patterns, and ecological processes. Cell Rep 11, 527-538, doi: 10.1016/j.celrep.2015.03.049 (2015).
43. Barelli, C. et al. Modeling Primate Abundance in Complex Landscapes: A Case Study From the Udzungwa Mountains of Tanzania. Int J Primatol. 1-18, doi: 10.1007/s10764-015-9815-7 (2015).
44. Hamaker, B. R., Tuncil, Y. E. A perspective on the complexity of dietary fiber structures and their potential effect on the gut microbiota. J Mol Biol 426, 3838-3850, doi: 10.1016/j.jmb.2014.07.028 (2014).
45. Goldsmith, J. R., Sartor, R. B. The role of diet on intestinal microbiota metabolism: downstream impacts on host immune function and health, and therapeutic implications. J Gastroenterol 49, 785-798, doi: 10.1007/s00535-014-0953-z (2014).
46. Kanehisa, M. et al. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 42, D199-205, doi: 10.1093/nar/gkt1076 (2014).
47. Langille, M. G. et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31, 814-821, doi: 10.1038/nbt.2676 (2013).
48. Koropatkin, N. M., Cameron, E. A., Martens, E. C. How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 10, 323-335, doi: 10.1038/nrmicro2746 (2012).
49. Flint, H. J., Bayer, E. A. Plant cell wall breakdown by anaerobic microorganisms from the Mammalian digestive tract. Ann N Y Acad Sci 1125, 280-288, doi: 10.1196/annals.1419.022 (2008).
50. Struhsaker, T. T. The Red Colobus Monkeys: Variation in Demography, Behavior, and Ecology of Endangered Species (Oxford University Press, 2010).
51. Vlckova, K., Mrazek, J., Kopecny, J., Petrzelkova, K. J. Evaluation of different storage methods to characterize the fecal bacterial communities of captive western lowland gorillas (Gorilla gorilla gorilla). J Microbiol Methods 91, 45-51, doi: 10.1016/j. mimet.2012.07.015 (2012).
52. Larsen, A. M., Mohammed, H. H., Arias, C. R. Comparison of DNA extraction protocols for the analysis of gut microbiota in fishes. FEMS Microbiol Lett 362, doi: 10.1093/femsle/fnu031 (2015).
53. Schumann, P. E. Stackebrandt & M. Goodfellow (Editors), Nucleic Acid Techniques in Bacterial Systematics (Modern Microbiological Methods). XXIX + 329 S., 46 Abb., 28 Tab. Chichester-New York-Brisbane-Toronto-Singapore 1991. John Wiley & Sons. ISBN: 0-471-92906-9.
54. J. Basic Microbiol. 31, 479-480, doi: 10.1002/jobm.3620310616 (1991).
55. Weisburg, W. G., Barns, S. M., Pelletier, D. A., Lane, D. J. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173, 697-703 (1991).
56. Albanese, D., Fontana, P., De Filippo, C., Cavalieri, D., Donati, C. MICCA: a complete and accurate software for taxonomic profiling of metagenomic data. Scientific Reports. doi: 10.1038/srep09743 (2015).
57. Wang, Q., Garrity, G. M., Tiedje, J. M., Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73, 5261-5267, doi: 10.1128/aem.00062-07 (2007).
58. Caporaso, J. G. et al. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266-267, doi: 10.1093/bioinformatics/btp636 (2010).
59. DeSantis, T. Z. et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72, 5069-5072, doi: 10.1128/aem.03006-05 (2006).
60. Price, M. N., Dehal, P. S., Arkin, A. P. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One 5, e9490, doi: 10.1371/journal.pone.0009490 (2010).
61. McMurdie, P. J., Holmes, S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8, e61217, doi: 10.1371/journal.pone.0061217 (2013).
62. Westfall, P. H. Resampling-Based Multiple Testing: Examples and Methods for P-Value Adjustment (John Wiley & Sons, 1993).