Analysis of the hydrogenotrophic microbiota of wild and captive black howler monkeys (Alouatta pigra) in palenque national park, Mexico

American Journal of Primatology

Volumn 73, Issue 9, 2011, Pages 909-919

  Nakamura, Noriko ^a   Amato, Katherine R ^a   Garber, Paul ^a   Estrada, Alejandro ^b   Mackie, Roderick I ^a   Gaskins, H Rex ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Alouatta pigra; DGGE; Intestinal hydrogenotrophs; Quantitative PCR

Indexed keywords

ARCHAEAL DNA; RNA 16S;

ABUNDANCE; BIOENERGETICS; CAPTIVE POPULATION; CARBOHYDRATE; DIET; ELECTROKINESIS; FECES; FERMENTATION; HYDROGEN; LEAF; METHANOGENESIS; METHANOGENIC BACTERIUM; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; POLYMERASE CHAIN REACTION; PRIMATE; SPECIES DIVERSITY; WILD POPULATION;

ALOUATTA; ANIMAL; ANIMAL DISEASE; ARTICLE; CHEMISTRY; FECES; FEMALE; GENETIC VARIABILITY; GENETICS; GRAM NEGATIVE ANAEROBIC BACTERIA; MALE; METAGENOME; METHANOBACTERIUM; MEXICO; MICROBIOLOGY; POLYMERASE CHAIN REACTION; PRINCIPAL COMPONENT ANALYSIS; PULSED FIELD GEL ELECTROPHORESIS; WILD ANIMAL; ZOO ANIMAL;

ALOUATTA; ANIMALS; ANIMALS, WILD; ANIMALS, ZOO; DNA, ARCHAEAL; ELECTROPHORESIS, GEL, PULSED-FIELD; FECES; FEMALE; GENETIC VARIATION; MALE; METAGENOME; METHANOBACTERIUM; MEXICO; POLYMERASE CHAIN REACTION; PRINCIPAL COMPONENT ANALYSIS; RNA, RIBOSOMAL, 16S; SULFUR-REDUCING BACTERIA;

CHIAPAS; MEXICO [NORTH AMERICA]; PALENQUE NATIONAL PARK;

ALOUATTA; ALOUATTA CARAYA; ALOUATTA PIGRA; ANIMALIA; BACTERIA (MICROORGANISMS); DESULFOVIBRIONALES; HAPLORHINI; PRIMATES;

EID: 79960555172     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.20961     Document Type: Article

References (41)

1. Amann RI, Ludwig W, Schleifer KH. 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiology Reviews 59:143-169.
2. Benno Y, Itoh K, Miyao Y, Mitsuoka T. 1987. Comparison of fecal microflora between wild Japanese monkeys in a snowy area and laboratory-reared Japanese monkeys. Nippon Juigaku Zasshi 49:1059-1064.
3. 2 by methane- and non-methane-producing human colonic bacterial communities. FEMS Microbiology Ecology 19:193-202.
4. Bond JHJ, Engel RR, Levitt MD. 1971. Factors influencing pulmonary methane excretion in man. An indirect method of studying the in situ metabolism of the methane-producing colonic bacteria. Journal of Experimental Medicine 133:572-588.
5. Cornick NA, Jensen NS, Stahl DA, Hartman PA, Allison MJ. 1994. Lachnospira pectinoschiza sp. nov., an anaerobic pectinophile from the pig intestine. International Journal of Systematic Bacteriology 44:87-93.
6. Cotta M, Forster R. 2006. The family Lachnospiraceae, including the genera Butyrivibrio, Lachnospira and Roseburia. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E, editors. The Prokaryotes, 3rd ed. New York: Springer. p 1002-1021.
7. Crissey SD, Pribyl LS. 1997. Utilizing wild foraging ecology information to provide captive primates with an appropriate diet. Proceedings of the Nutrition Society 56:1083-1094.
8. Daly K, Sharp RJ, McCarthy AJ. 2000. Development of oligonucleotide probes and PCR primers for detecting phylogenetic subgroups of sulfate-reducing bacteria. Microbiology 146:1693-1705.
9. Dar SA, Kuenen JG, Muyzer G. 2005. Nested PCR-denaturing gradient gel electrophoresis approach to determine the diversity of sulfate-reducing bacteria in complex microbial communities. Applied and Environmental Microbiology 71:2325-2330.
10. Denman SE, Tomkins NW, McSweeney CS. 2007. Quantitation and diversity analysis of ruminal methanogenic populations in response to the antimethanogenic compound bromochloromethane. FEMS Microbiology Ecology 62:313-322.
11. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology 72:5069-5072.
12. Dethlefsen L, Huse S, Sogin ML, Relman DA. 2008. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biology 6:e280.
13. Duncan SH, Barcenilla A, Stewart CS, Pryde SE, Flint HJ. 2002a. Acetate utilization and butyryl coenzyme A (CoA): acetate-CoA transferase in butyrate-producing bacteria from the human large intestine. Applied and Environmental Microbiology 68:5186-5190.
14. Duncan SH, Hold GL, Barcenilla A, Stewart CS, Flint HJ. 2002b. Roseburia intestinalis sp. nov., a novel saccharolytic, butyrate-producing bacterium from human faeces. International Journal of Systematic and Evolutionary Microbiology 52:1615-1620.
15. Eisenberg JF, Muckenhirn NA, Rundran R. 1972. The relation between ecology and social structure in primates. Science 176:863-874.
16. Falony G, Vlachou A, Verbrugghe K, De Vuyst L. 2006. Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose. Applied and Environmental Microbiology 72:7835-7841.
17. Florin TH, Zhu G, Kirk KM, Martin NG. 2000. Shared and unique environmental factors determine the ecology of methanogens in humans and rats. American Journal of Gastroenterology 95:2872-2879.
18. Fricke WF, Seedorf H, Henne A, Kruer M, Liesegang H, Hedderich R, Gottschalk G, Thauer RK. 2006. The genome sequence of Methanosphaera stadtmanae reveals why this human intestinal archaeon is restricted to methanol and H2 for methane formation and ATP synthesis. Journal of Bacteriology 188:642-658.
19. Fujita S, Kageyama T. 2007. Polymerase chain reaction detection of Clostridium perfringens in feces from captive and wild chimpanzees, Pan troglodytes. Journal of Medical Primatology 36:25-32.
20. Hackstein JH, Van Alen TA, Op Den Camp H, Smits A, Mariman E. 1995. Intestinal methanogenesis in primates-a genetic and evolutionary approach. Dtsch Tierarztl Wochenschr 102:152-154.
21. Janse I, Bok J, Zwart G. 2004. A simple remedy against artifactual double bands in denaturing gradient gel electrophoresis. Journal of Microbiological Methods 57:279-281.
22. Kondo R, Nedwell DB, Purdy KJ, de Queiroz Silva S. 2004. Detection and enumeration of sulphate-reducing bacteria in estuarine sediments by competitive PCR. Geomicrobiology Journal 21:145-157.
23. Lepp PW, Brinig MM, Ouverney CC, Palm K, Armitage GC, Relman DA. 2004. Methanogenic Archaea and human periodontal disease. Proceedings of the National Academy of Science of the United States of America 101:6176-6181.
24. Levitt MD, Furne JK, Kuskowski M, Ruddy J. 2006. Stability of human methanogenic flora over 35 years and a review of insights obtained from breath methane measurements. Clinical Gastroenterology and Hepatology 4:123-129.
25. Miller TL, Wolin MJ. 1985. Methanosphaera stadtmaniae gen. nov., sp. nov.: a species that forms methane by reducing methanol with hydrogen. Archives of Microbiology 141:116-122.
26. Milton K, McBee RH. 1983. Rates of fermentative digestion in the howler monkey, Alouatta palliata (primates: ceboidea). Comparative Biochemistry and Physiology-Part A: Comparative Physiology 74:29-31.
27. Milton K, Soest PJV, Robertson JB. 1980. Digestive efficiencies of wild howler monkeys. Physiology and Zoology 53:402-409.
28. Muyzer G, de Waal EC, Uitterlinden AG. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Applied and Environmental Microbiology 59:695-700.
29. Nakamura N, Lin HC, McSweeney CS, Mackie RI, Gaskins HR. 2010. Mechanisms of microbial hydrogen disposal in the human colon and implications for health and disease. Annual Review of Food Science and Technology 1:363-395.
30. Raskin L, Stromley JM, Rittmann BE, Stahl DA. 1994. Group-specific 16S rRNA hybridization probes to describe natural communities of methanogens. Applied and Environmental Microbiology 60:1232-1240.
31. 2-utilizing species Eubacterium limosum and pectin-fermenting Lachnospira multiparus during growth in a pectin medium. Applied and Environmental Microbiology 42:20-22.
32. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4:406-425.
33. Samuel BS, Gordon JI. 2006. A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proceedings of the National Academy of Science of the United States of America 103:10011-10016.
34. Serio-Silva JC, Hernández-Salazar LT, Rico-Gray V. 1999. Nutritional composition of the diet of Alouatta palliata mexicana females in different reproductive states. Zoo Biology 18:507-513.
35. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24:1596-1599.
36. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027-1031.
37. Uenishi G, Fujita S, Ohashi G, Kato A, Yamauchi S, Matsuzawa T, Ushida K. 2007. Molecular analyses of the intestinal microbiota of chimpanzees in the wild and in captivity. American Journal of Primatology 69:367-376.
38. Ufnar JA, Wang SY, Ufnar DF, Ellender RD. 2007. Methanobrevibacter ruminantium as an indicator of domesticated-ruminant fecal pollution in surface waters. Applied and Environmental Microbiology 73:7118-7121.
39. Wright AD, Williams AJ, Winder B, Christophersen CT, Rodgers SL, Smith KD. 2004. Molecular diversity of rumen methanogens from sheep in Western Australia. Applied and Environmental Microbiology 70:1263-1270.
40. Wright AD, Auckland CH, Lynn DH. 2007. Molecular diversity of methanogens in feedlot cattle from Ontario and Prince Edward Island, Canada. Applied and Environmental Microbiology 73:4206-4210.
41. Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, Parameswaran P, Crowell MD, Wing R, Rittmann BE, Krajmalnik-Brown R. 2009. Human gut microbiota in obesity and after gastric bypass. Proceedings of the National Academy of Science of the United States of America 106:2365-2370.