Pathogenic eukaryotes in gut microbiota of western lowland gorillas as revealed by molecular survey

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Hamad, Ibrahim ^a   Keita, Mamadou B ^a   Peeters, Martine ^b   Delaporte, Eric ^b   Raoult, Didier ^a   Bittar, Fadi ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; PRIMER DNA; RNA 18S;

ANIMAL; CHEMISTRY; EUKARYOTE; FECES; GASTROINTESTINAL TRACT; GENETICS; GORILLA; HUMAN; METABOLISM; MICROBIOLOGY; MICROFLORA; MOLECULAR GENETICS; PATHOGENICITY; PHYLOGENY; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; BIOMARKERS; DNA PRIMERS; EUKARYOTA; FECES; GASTROINTESTINAL TRACT; GORILLA GORILLA; HUMANS; MICROBIOTA; MOLECULAR SEQUENCE DATA; PHYLOGENY; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 18S;

EID: 84923307053     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep06417     Document Type: Article

References (58)

1. Hooper, L. V. & Gordon, J. I. Commensal host-bacterial relationships in the gut. Science 292, 1115-1118 (2001).
2. Round, J. L. & Mazmanian, S. K. The gut microbiota shapes intestinal immune responses during health and disease. Nat.Rev.Immunol. 9, 313-323 (2009).
3. Dale, C. & Moran, N. A. Molecular interactions between bacterial symbionts and their hosts. Cell 126, 453-465 (2006).
4. Parfrey, L. W., Walters, W. A. & Knight, R. Microbial eukaryotes in the human microbiome: ecology, evolution, and future directions. Front Microbiol. 2, 153 (2011).
5. Raoult, D. The apes as reservoir of human pathogens. Clin. Microbiol. Infect. 18, 513 (2012).
6. Peeters, M. & Delaporte, E. Simian retroviruses in African apes. Clin. Microbiol. Infect. 18, 514-520 (2012).
7. Chapman, C. A., Gillespie, T. R. & Goldberg, T. L. Primates and the Ecology of their Infectious Diseases: How will Anthropogenic Change Affect Host-Parasite Interactions? Evol. Anthr. 14, 134-144 (2005).
8. The Mountain Gorilla Veterinary, P. Risk of Disease Transmission between Conservation Personnel and the Mountain Gorillas: Results from an Employee Health Program in Rwanda. EcoHealth 1, 351-361 (2004).
9. Ashford, R.W., Lawson, H., Butynski, T. M. & Reid, G. D. F. Patterns of intestinal parasitism in the mountain gorilla Gorilla gorilla in the Bwindi-Impenetrable Forest, Uganda. J.Zool. 239, 507-514 (1996).
10. Sleeman, J. M., Meader, L. L., Mudakikwa, A. B., Foster, J. W. & Patton, S. Gastrointestinal parasites of mountain gorillas (Gorilla gorilla beringei) in the Parc National des Volcans, Rwanda. J.Zoo.Wildl.Med. 31, 322-328 (2000).
11. Landsoud-Soukate, J., Tutin, C. E. & Fernandez, M. Intestinal parasites of sympatric gorillas and chimpanzees in the Lopé Reserve, Gabon. Ann.Trop.Med.Parasitol. 89, 73-79 (1995).
12. Lilly, A. A., Mehlman, P. T. & Doran, D. Intestinal Parasites in Gorillas, Chimpanzees, and Humans at Mondika Research Site, Dzanga-Ndoki National Park, Central African Republic. International Journal of Primatol. 23, 555-573 (2002).
13. Freeman, A. S., Kinsella, J. M., Cipolletta, C., Deem, S. L. & Karesh, W. B. Endoparasites of western lowland gorillas (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic. J.Wildl.Dis. 40, 775-781 (2004).
14. Hamad, I., Delaporte, E., Raoult, D. & Bittar, F. Detection of termites and other insects consumed by African great apes using molecular fecal analysis. Scientific reports 4, 4478 (2014).
15. Scanlan, P. D.&Marchesi, J. R. Micro-eukaryotic diversity of the human distal gut microbiota: qualitative assessment using culture-dependent and-independent analysis of faeces. ISME.J. 2, 1183-1193 (2008).
16. Hamad, I., Sokhna, C., Raoult, D. & Bittar, F. Molecular detection of eukaryotes in a single human stool sample from Senegal. PloS One 7, e40888 (2012).
17. Scupham, A. J. et al. Abundant and diverse fungal microbiota in the murine intestine. Appl.Environ.Microbiol. 72, 793-801 (2006).
18. Nam, Y. D. et al. Bacterial, archaeal, and eukaryal diversity in the intestines of Korean people. J.Microbiol. 46, 491-501 (2008).
19. Chen, Y. et al. Correlation between gastrointestinal fungi and varying degrees of chronic hepatitis B virus infection. Diagn.Microbiol.Infect.Dis. 70, 492-498 (2010).
20. Li, Q. et al. Use of 18S ribosomal DNA polymerase chain reaction-denaturing gradient gel electrophoresis to study composition of fungal community in 2 patients with intestinal transplants. Hum.Pathol. 43, 1273-1281 (2012).
21. Bills, G. & Polishoot, J. Abundance and diversi ty of microfungi in leaf litter of a lowland rain forest in Costa Rica. Mycologia 86, 187-198 (1994).
22. Suh, S. O., Blackwell, M., Kurtzman, C. P. & Lachance, M. A. Phylogenetics of Saccharomycetales, the ascomycete yeasts. Mycologia 98, 1006-1017 (2006).
23. Chanchaichaovivat, A., Ruenwongsa, P. & Panijpan, B. Screening and identification of yeast strains from fruits and vegetables: Potential for biological control of postharvest chilli anthracnose (Colletotrichum capsici). Biol. Control 42, 326-335 (2007).
24. Lages, F., Silva-Graca, M. & Lucas, C. Active glycerol uptake is a mechanism underlying halotolerance in yeasts: a study of 42 species. Microbiol. 145 (Pt 9), 2577-2585 (1999).
25. Kurtzman, C.&Wickerham, L. Saccharomycopsis crataegensis, a new heterothallic yeast. Antonie van Leeuwenhoek 39, 81-87 (1973).
26. Phaff, H. J. & Starmer, W. T. Yeasts associated with plants, insects and soil. In: (Rose, A.H. and Harrison, J.S. eds) The yeast Vol. 1 2nd (eds Rose, A. H. & Harrison, J. S.) 123-179 (Academic Press London, 1987).
27. Sláviková, E., adkertiov, R. & Vránová, D. Yeasts colonizing the leaves of fruit trees. Ann. Microbiol. 59, 419-424 (2009).
28. Toivola, A., Yarrow, D., van den Bosch, E., van Dijken, J. P. & Scheffers, W. A. Alcoholic Fermentation of d-Xylose by Yeasts. Appl.Environ.Microbiol. 47, 1221-1223 (1984).
29. Visagie, C. M., Roets, F. & Jacobs, K. A new species of Penicillium, P. ramulosum sp. nov., from the natural environment. Mycologia 101, 888-895 (2009).
30. Jia-Rong, G. U., Yu-Ming, J. U. & Huan-Ju, H. Bionectriaceous fungi collected from forests in Taiwan. Bot.Stud. 51, 61-74 (2010).
31. Poinar, G. O., Jr. Xylaria antiqua sp. nov. (Ascomycota: Xylariaceae) in Dominican amber. J. Bot. Res. Inst. Texas 8, 145-149 (2014).
32. Kruys, A., Eriksson,O. E.&Wedin,M. Phylogenetic relationships of coprophilous Pleosporales (Dothideomycetes, Ascomycota), and the classification of some bitunicate taxa of unknown position. Mycol.Res. 110, 527-536 (2006).
33. Tavanti, A., Davidson, A. D., Gow, N. A., Maiden, M. C. & Odds, F. C. Candida orthopsilosis and Candida metapsilosis spp. nov. to replace Candida parapsilosis groups II and III. J. Clin.Microbiol. 43, 284-292 (2005).
34. Lee, Y. W. et al. Distribution of Malassezia species on the scalp in korean seborrheic dermatitis patients. Ann.Dermatol. 23, 156-161 (2011).
35. Wolf, D. G. et al. Multidrug-resistant Trichosporon asahii infection of nongranulocytopenic patients in three intensive care units. J.Clin.Microbiol. 39, 4420-4425 (2001).
36. Sawhasan, P., Worapong, J., Flegel, T. & Vinijsanun, T. Fungal partnerships stimulate growth of Termitomyces clypeatus stalk mycelium in vitro. World J. Microb. Biot. 28, 1-2311 (2012).
37. Deblauwe, I. & Janssens, G. P. New insights in insect prey choice by chimpanzees and gorillas in southeast Cameroon: the role of nutritional value. Am.J Phys.Anthropol. 135, 42-55 (2008).
38. Modry, D. et al. The occurrence and ape-to-ape transmission of the entodiniomorphid ciliate Troglodytella abrassarti in captive gorillas. J.Eukaryot.Microbiol. 56, 83-87 (2009).
39. Tokiwa, T., Petrzelkova, K., Modry, D., Ito, A. & Imai, S. Morphological observations of Troglodytella abrassarti (Entodiniomorphida, Troglodytellidae) from the lowland gorilla (Gorilla gorilla gorilla). Jpn. J. Protozool. 41 (2008).
40. Profousov, I. et al. The ciliate, Troglodytella abrassarti, contributes to polysaccharide hydrolytic activities in the chimpanzee colon. Folia Microbiol.(Praha) 56, 339-343 (2011).
41. Yakoob, J. et al. Blastocystis hominis andDientamoeba fragilis in patients fulfilling irritable bowel syndrome criteria. Parasitol.Res. 107, 679-684 (2010).
42. Alfellani, M. A. et al. Diversity and distribution of Blastocystis sp. subtypes in nonhuman primates. Parasitol. 140, 966-971 (2013).
43. Smejkalov, P., Petrzelkov, K. J., Pomajbkov, K.,Modry, D.& Cepicka, I. Extensive diversity of intestinal trichomonads of non-human primates. Parasitol. 139, 92-102 (2012).
44. Castella, J., Munoz, E., Ferrer, D. & Gutierrez, J. F. Isolation of the trichomonad Tetratrichomonas buttreyi (Hibler et al., 1960) Honigberg, 1963 in bovine diarrhoeic faeces. Vet.Parasitol. 70, 41-45 (1997).
45. Polderman, A. M. & Blotkamp, J. Oesophagostomum infections in humans. Parasitol.Today 11, 451-456 (1995).
46. Krepel, H. P., Baeta, S. & Polderman, A. M. Human Oesophagostomum infection in northern Togo and Ghana: epidemiological aspects. Ann.Trop.Med.Parasitol. 86, 289-300 (1992).
47. de Silva, N. R. et al. Soil-transmitted helminth infections: updating the global picture. Trends Parasitol. 19, 547-551 (2003).
48. Kalema, G. Epidemiology of the intestinal parasite burden of mountain gorillas, Gorilla gorilla beringei, in Bwindi Impenetrable National Park, South West Uganda. B.V.Z.S. 14, 18-34. (1995).
49. Hasegawa, H. et al. Humans and great apes cohabiting the forest ecosystem in central african republic harbour the same hookworms. PLoS Negl. Trop. Dis. 8, e2715 (2014).
50. Ederli, N. B. & Oliveira, F. C. Differential localization of Libyostrongylus douglassii (Cobbold, 1882) Lane, 1923 and L. dentatus Hoberg, Lloyd, and Omar, 1995 (Nematoda: Trichostrongylidae) in ostrich (Struthio camelus Linnaeus, 1758) proventriculi. J. Parasitol. 95, 757-759 (2009).
51. Calvert, J. Food selection by western gorillas (G.g.Gorilla) in relaetion to food chemistry. Oecologia 65, 236-246 (1985).
52. Rogers, M.,Maisels, E., Fernandez, M. & Tutin, E. Gorilla diet in the Lopé Reserve Gabon: a nutritional analysis. Oecologia 84, 326-339 (1990).
53. Goldsmith, M. L. Ecological Constraints on the Foraging Effort of Western Gorillas (Gorilla gorilla gorilla) at Bai Hoköu, Central African Republic. Int. J. Primatol. 20, 1-23 (1999).
54. Yamagiwa, J. Socioecological factors influencing population structure of gorillas and chimpanzees. Primates 40, 87-104 (1999).
55. Bradley, B. J. et al. Plant DNA sequences from feces: potential means for assessing diets of wild primates. Am. J. Primatol. 69, 699-705 (2007).
56. Neel, C. et al. Molecular epidemiology of simian immunodeficiency virus infection in wild-living gorillas. J. Virol. 84, 1464-1476 (2010).
57. Tamura, K. et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739 (2011).
58. Rozen, S. &Skaletsky, H. Primer3 on theWWWfor general users and for biologist programmers. Methods Mol Biol. 132, 365-386 (2000).