Fluorescence in situ hybridization probing of protozoal Entodinium spp. and their methanogenic colonizers in the rumen of cattle fed alfalfa hay or triticale straw

Journal of Applied Microbiology

Volumn 116, Issue 1, 2014, Pages 14-22

  Xia, Y ^a,b   Kong, Y H ^b   Seviour, R ^c   Forster, R J ^a   Kisidayova, S ^d   Mcallister, T A ^a  

^a LETHBRIDGE RESEARCH CENTRE   (Canada)

^b KUNMING UNIVERSITY   (China)

^c LA TROBE UNIVERSITY   (Australia)

^d INSTITUTE OF ANIMAL PHYSIOLOGY   (Slovakia)

Author keywords

Entodinium; Fluorescence in situ hybridization; Methanogens; Rumen ecology; Symbiosis

Indexed keywords

FLUORESCENCE; FLUORESCENCE MICROSCOPY; METHANOGENS; PROBES; PROTOZOA;

CATTLE FEED; EFFECTIVE APPROACHES; ENTODINIA; FLUORESCENCE IN SITU HYBRIDIZATION; HYBRIDIZATION PROBE; RELATIVE ABUNDANCE; RUMEN ECOLOGY; SYMBIOSIS; SYMBIOTIC RELATIONSHIP; TRITICALE STRAWS;

FISH;

ABUNDANCE; ALFALFA; CATTLE; COLONIZATION; FLUORESCENCE; FORAGE; HYBRIDIZATION; PHYLOGENETICS; PROTOZOAN;

ALFALFA; ARTICLE; CATTLE; CONTROLLED STUDY; ENTODINIUM; ENTODINIUM CAUDAUM; ENTODINIUM FURCA; ENTODINIUM SIMPLEX; FLUORESCENCE IN SITU HYBRIDIZATION; FORAGE; METHANOBREVIBACTER; METHANOBREVIBACTER MILLERAE; METHANOBREVIBACTER SMITHII; METHANOBREVIBACTER THAUERI; METHANOGEN; METHANOSPHAERA; MICROBIAL COLONIZATION; MOLECULAR PROBE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTOZOAL COLONIZATION; PROTOZOON; RUMINANT STOMACH; STRAW; TRITICALE; ANIMAL; BOVINE; EURYARCHAEOTA; PARASITOLOGY; RUMEN;

ANIMALIA; ARCHAEA; BOS; ENTODINIUM; ENTODINIUM FURCA; ENTODINIUM SIMPLEX; MEDICAGO SATIVA; METHANOBREVIBACTER; METHANOBREVIBACTER SMITHII; METHANOBREVIBACTER THAUERI; METHANOMICROBIUM; METHANOSPHAERA; PROTOZOA; TRITICOSECALE;

RNA 16S;

ANIMALS; CATTLE; EURYARCHAEOTA; IN SITU HYBRIDIZATION, FLUORESCENCE; MEDICAGO SATIVA; RNA, RIBOSOMAL, 16S; RUMEN; TRITICALE;

EID: 84890428906     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12356     Document Type: Article

References (39)

1. Abramoff, M.D., Magalhaes, P.J. and Ram, S.J. (2004) Image processing with imageJ. Biophotonics Int 11, 36-41.
2. Amann, R.I. (1995) In situ hybridization of micro-organisms by whole cell hybridization with rRNA-targeted nucleic acid probes. In Molecular Microbial Ecological Manual ed. Akkermans, A.D.L., van Elsas, J.D. and de Bruijn, F.J. part 3.3.6. pp. 1-15. London: Kluwer Academic Publications.
3. Amann, R.I., Ludwig, W. and Schleifer, K.H. (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59, 143-169.
4. Baker, B.J., Hugenholtz, P., Dawson, S.C. and Banfield, J.F. (2003) Extremely acidophilic protists from acid mine drainage host Rickettsiales-lineage endosymbionts that have intervening sequences in their 16S rRNA genes. Appl Environ Microbiol 69, 5512-5518.
5. Chagan, I., Tokura, M., Jouany, J.P. and Ushida, K. (1999) Detection of methanogenic archaea associated with rumen ciliate protozoa. J Gen Appl Microbiol 45, 305-308.
6. Coleman, G.S. (1978) Rumen entodiniomorphid protozoa. In Methods of Cultivating Parasites In Vitro ed. Taylor, A.E.R. and Baker, J.R. pp. 39-54. London: Academic Press.
7. Coleman, G.S. (1992) The rate of uptake and metabolism of starch grains and cellulose particles by Entodinium species, Eudiplodinium maggii, some other entodiniomorphid protozoa and natural protozoal populations taken from the ovine rumen. J Appl Bacteriol 73, 507-513.
8. Finlay, B.J. and Fenchel, T. (1990) Hydrogenosomes in some anaerobic protozoa resemble mitochondria. FEMS Microbiol Lett 65, 311-314.
9. Fried, J., Ludwig, W., Psenner, R. and Schleifer, K.H. (2002) Improvement of ciliate identification and quantification: a new protocol for fluorescence in situ hybridization (FISH) in combination with silver stain techniques. Syst Appl Microbiol 25, 555-571.
10. Hugenholtz, P., Tyson, G.W. and Blackall, L.L. (2001) Design and evaluation of 16S rRNA-targeted oligonucleotide probes for fluorescence in situ hybridization. In Methods of Molecular Biology ed. Aquino de Muro, M. and Rapley, R. vol. 17. pp. 29-42. Totowa: Humana Press.
11. Irbis, C. and Ushida, K. (2004) Detection of methanogens and proteobacteria from a single cell of rumen ciliate protozoa. J Gen Appl Microbiol 50, 203-212.
12. Janssen, P.H. and Kirs, M. (2008) Structure of the archaeal community of the rumen. Appl Environ Microbiol 74, 3619-3625.
13. Jouany, J.P. (1991) Defaunation of the rumen. In Rumen Microbial Metabolism and Ruminant Digestion ed. Jouany, J.P. pp. 239-261. Paris: INRA.
14. Kamra, D.N., Sawal, R.K., Pathak, N.N., Kewalramani, N. and Agarwal, N. (1991) Diurnal variation in ciliate protozoa in the rumen of black buck (Antilope cervicapra) fed green forage. Lett Appl Microbiol 13, 165-167.
15. Kišidayová, S., Váradyová, Z., Michalowski, T. and Newbold, C.J. (2005) Regeneration of cryoresistance of in vitro rumen ciliate cultures. Cryobiology 51, 76-84.
16. Kong, Y.H., He, M., McAllister, T.A., Seviour, R. and Forster, R.J. (2010a) Quantitative fluorescence in situ hybridization of microbial communities in the rumens of cattle fed different diets. Appl Environ Microbiol 76, 6933-6938.
17. Kong, Y.H., Teather, R.M. and Forster, R.J. (2010b) Composition, spatial distribution, and diversity of the bacterial communities in the rumen of cows fed different forages. FEMS Microbiol Ecol 74, 612-622.
18. Kong, Y.H., Xia, Y., Seviour, R., Forster, R.J. and McAllister, T.A. (2013) Biodiversity and composition of methanogenic populations in the rumen of cows fed alfalfa hay or triticale straw. FEMS Microbiol Ecol 84, 302-315.
19. Lloyd, D., Williams, A.G., Amann, R., Hayes, A.J., Durrant, L. and Ralphs, J.R. (1996) Intracellular prokaryotes in rumen ciliate protozoa: detection by confocal laser scanning microscopy after in situ hybridization with fluorescent 16S rRNA probes. Eur J Protistol 32, 523-531.
20. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, A., Buchner, A., Lai, T. et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32, 1363-1371.
21. Moss, A.R., Jouany, J.P. and Newbold, J. (2000) Methane production by ruminants: its contribution to global warming. Animal Res 49, 231-253.
22. Ohene-Adjei, S., Teather, R.M., Ivan, M. and Forster, R.J. (2007) Postinoculation protozoan establishment and association patterns of methanogenic archaea in the ovine rumen. Appl Environ Microbiol 73, 4609-4618.
23. Paul, K., Nonoh, J.O., Mikulski, L. and Brune, A. (2012) "Methanoplasmatales", Thermoplasmatales-related archaea in termite guts and other environments are the seventh order of methanogens. Appl Environ Microbiol 78, 8245-8253.
24. Pei, C.X., Mao, S.Y., Cheng, Y.F. and Zhu, W.Y. (2010) Diversity, abundance and novel 16S rRNA gene sequences of methanogens in rumen liquid, solid and epithelium fractions of Jinnan cattle. Animal 4, 20-29.
25. Pruesse, E., Quast, C., Knittel, K., Fuchs, B.M., Ludwig, W., Peplies, J. and Glöckner, F.O. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35, 7188-7196.
26. Ranilla, M.J., Jouany, J.P. and Morgavi, D.P. (2007) Methane production and substrate degradation by rumen microbial communities containing single protozoal species in vitro. Lett Appl Microbiol 45, 675-680.
27. Regensbogenova, M., McEwan, N.R., Javorsky, P., Kisidayova, S., Michalowski, T., Newbold, C.J., Hackstein, J.H.P. and Pristas, P. (2004) A re-appraisal of the diversity of the methanogens associated with the rumen ciliates. FEMS Microbiol Lett 238, 307-313.
28. Schmidt, S.L., Bernhard, D., Schlegel, M. and Fried, J. (2006) Fluorescence in situ hybridization with specific oligonucleotide rRNA probes distinguishes the sibling species Stylonychia lemnae and Stylonychia mytilus (Ciliophora, Spirotrichea). Protist 157, 21-30.
29. Schramm, A., Fuchs, B.M., Nielsen, J.L., Tonolla, M. and Stahl, D.A. (2002) Fluorescence in situ hybridization of 16S rRNA gene clones (Clone-FISH) for probe validation and screening of clone libraries. Environ Microbiol 4, 713-720.
30. Sharp, R., Ziemer, C.J., Stern, M.D. and Stahl, D.A. (1998) Taxon-specific associations between protozoal and methanogen populations in the rumen and a model rumen system. FEMS Microbiol Ecol 26, 71-78.
31. Shin, E.C., Choi, B.R., Lim, W.J., Hong, S.Y., An, C.L., Cho, K.M., Kim, Y.K., An, J.M. et al. (2004) Phylogenetic analysis of archaea in three fractions of cow rumen based on the 16S rDNA sequence. Anaerobe 10, 313-319.
32. Tokura, M., Ushida, K., Miyazaki, K. and Kojima, Y. (1997) Methanogens associated with rumen ciliates. FEMS Microbiol Ecol 22, 137-143.
33. Tymensen, L.D. and McAllister, T.A. (2012) Community structure analysis of methanogens associated with rumen protozoa reveals bias in universal archaeal primers. Appl Environ Microbiol 78, 4051-4056.
34. Tymensen, L.D., Barkley, C. and McAllister, T.A. (2012a) Relative diversity and community structure analysis of rumen protozoa according to T-RFLP and microscopic methods. J Microbiol Methods 88, 1-6.
35. Tymensen, L.D., Beauchemin, K.A. and McAllister, T.A. (2012b) Structures of free-living and protozoa-associated methanogen communities in the bovine rumen differ according to comparative analysis of 16S rRNA and mcrA genes. Microbiology 158, 1808-1817.
36. Ushida, K., Jouany, J.P. and Demeyer, D.I. (1991) Effects of presence or absence of rumen protozoa on the efficiency of utilization of concentrate and fibrous feeds. In Physiological Aspects of Digestion and Metabolism in Ruminants ed. Tsuda, T., Sasaki, Y. and Kawashima, R. pp. 625-654. Tokyo: Academic Press.
37. Whitford, M.F., Teather, R.M. and Forster, R.J. (2001) Phylogenetic analysis of methanogens from the bovine rumen. BMC Microbiol 1, 5.
38. Xia, Y., Kong, Y.H. and Nielsen, P.H. (2007) In situ detection of protein-hydrolysing microorganisms in activated sludge. FEMS Microbiol Ecol 60, 156-165.
39. Xia, Y., Massé, D.I., McAllister, T.A., Beaulieu, C., Talbot, G., Kong, Y.H. and Seviour, R. (2011) In situ identification of keratin-hydrolyzing organisms in swine manure inoculated anaerobic digesters. FEMS Microbiol Ecol 78, 451-462.