The players may change but the game remains: Network analyses of ruminal microbiomes suggest taxonomic differences mask functional similarity

Nucleic Acids Research

Volumn 43, Issue 20, 2015, Pages 9600-9612

  Taxis, Tasia M ^a   Wolff, Sara ^a   Gregg, Sarah J ^a   Minton, Nicholas O ^a   Zhang, Chiqian ^b   Dai, Jingjing ^b   Schnabel, Robert D ^a   Taylor, Jeremy F ^a   Kerley, Monty S ^a   Pires, J Chris ^a   Lamberson, William R ^a   Conant, Gavin C ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; DNA 16S; FATTY ACID; MICROBIAL ENZYME; ENZYME; RIBOSOME DNA; RNA 16S; VOLATILE FATTY ACID;

AMINO ACID SEQUENCE; ARTICLE; BODY WEIGHT; BOVINE; BULLOCK; FATTY ACID METABOLISM; FOOD INTAKE; GENE DOSAGE; GENE IDENTIFICATION; GENE MAPPING; GENETIC VARIABILITY; HOST PATHOGEN INTERACTION; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIAL METABOLISM; NONHUMAN; PRIORITY JOURNAL; RUMEN FLUID; RUMEN MICROORGANISM; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; TAXONOMY; ANIMAL; CHEMISTRY; GENETICS; MALE; METABOLISM; METAGENOME; MICROBIOLOGY; MICROFLORA; PHYLOGENY; RUMEN;

ANIMALS; CATTLE; DNA, RIBOSOMAL; ENZYMES; FATTY ACIDS, VOLATILE; MALE; METABOLIC NETWORKS AND PATHWAYS; METAGENOME; METAGENOMICS; MICROBIOTA; PHYLOGENY; RNA, RIBOSOMAL, 16S; RUMEN;

EID: 84951815312     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv973     Document Type: Article

References (64)

1. Ley, R.E., Peterson, D.A. and Gordon, J.I. (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell, 124, 837-848.
2. Stevens, C.E. and Hume, I.D. (1998) Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol. Rev., 78, 393-427.
3. Ley, R.E., Lozupone, C.A., Hamady, M., Knight, R. and Gordon, J.I. (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat. Rev. Microbiol., 6, 776-788.
4. Mackie, R.I. (2002) Mutualistic fermentative digestion in the gastrointestinal tract: diversity and evolution. Integr. Comp. Biol., 42, 319-326.
5. Russell, J.B. and Rychlik, J.L. (2001) Factors that alter rumen microbial ecology. Science, 292, 1119-1122.
6. Hooper, L.V., Midtvedt, T. and Gordon, J.I. (2002) How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu. Rev. Nutr., 22, 283-307.
7. Kim, M., Morrison, M. and Yu, Z. (2011) Status of the phylogenetic diversity census of ruminal microbiomes. FEMS Microbiol. Ecol., 76, 49-63.
8. Guan, L.L., Nkrumah, J.D., Basarab, J.A. and Moore, S.S. (2008) Linkage of microbial ecology to phenotype: correlation of rumen microbial ecology to cattles feed efficiency. FEMS Microbiol. Lett., 288, 85-91.
9. Kobayashi, Y. (2006) Inclusion of novel bacteria in rumen microbiology: need for basic and applied science. Anim. Sci. J., 77, 375-385.
10. Hess, M., Sczyrba, A., Egan, R., Kim, T.W., Chokhawala, H., Schroth, G., Luo, S., Clark, D.S., Chen, F., Zhang, T. et al. (2011) Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science, 331, 463-467.
11. Eckburg, P.B., Bik, E.M., Bernstein, C.N., Purdom, E., Dethlefsen, L., Sargent, M., Gill, S.R., Nelson, K.E. and Relman, D.A. (2005) Diversity of the human intestinal microbial flora. Science, 308, 1635-1638.
12. Venter, J.C., Remington, K., Heidelberg, J.F., Halpern, A.L., Rusch, D., Eisen, J.A., Wu, D., Paulsen, I., Nelson, K.E., Nelson, W. et al. (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science, 304, 66-74.
13. Beja, O., Suzuki, M.T., Heidelberg, J.F., Nelson, W.C., Preston, C.M., Hamada, T., Eisen, J.A., Fraser, C.M. and DeLong, E.F. (2002) Unsuspected diversity among marine aerobic anoxygenic phototrophs. Nature, 415, 630-633.
14. Ley, R.E., Backhed, F., Turnbaugh, P., Lozupone, C.A., Knight, R.D. and Gordon, J.I. (2005) Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. U.S.A., 102, 11070-11075.
15. Turnbaugh, P.J., Ley, R.E., Mahowald, M.A., Magrini, V., Mardis, E.R. and Gordon, J.I. (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature, 444, 1027-1031.
16. Greenblum, S., Chiu, H.-C., Levy, R., Carr, R. and Borenstein, E. (2013) Towards a predictive systems-level model of the human microbiome: progress, challenges, and opportunities. Curr. Opin. Biotechnol., 24, 810-820.
17. Tringe, S.G., von Mering, C., Kobayashi, A., Salamov, A.A., Chen, K., Chang, H.W., Podar, M., Short, J.M., Mathur, E.J., Detter, J.C. et al. (2005) Comparative metagenomics of microbial communities. Science, 308, 554-557.
18. Gill, S.R., Pop, M., Deboy, R.T., Eckburg, P.B., Turnbaugh, P.J., Samuel, B.S., Gordon, J.I., Relman, D.A., Fraser-Liggett, C.M. and Nelson, K.E. (2006) Metagenomic analysis of the human distal gut microbiome. Science, 312, 1355-1359.
19. Greenblum, S., Turnbaugh, P.J. and Borenstein, E. (2012) Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease. Proc. Natl. Acad. Sci., 109, 594-599.
20. Abubucker, S., Segata, N., Goll, J., Schubert, A.M., Izard, J., Cantarel, B.L., Rodriguez-Mueller, B., Zucker, J., Thiagarajan, M. and Henrissat, B. (2012) Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comput. Biol., 8, e1002358.
21. Turnbaugh, P.J., Hamady, M., Yatsunenko, T., Cantarel, B.L., Duncan, A., Ley, R.E., Sogin, M.L., Jones, W.J., Roe, B.A. and Affourtit, J.P. (2009) A core gut microbiome in obese and lean twins. Nature, 457, 480-484.
22. Human Microbiome Project Consortium. (2012) Structure, function and diversity of the healthy human microbiome. Nature, 486, 207-214.
23. Franzosa, E.A., Morgan, X.C., Segata, N., Waldron, L., Reyes, J., Earl, A.M., Giannoukos, G., Boylan, M.R., Ciulla, D. and Gevers, D. (2014) Relating the metatranscriptome and metagenome of the human gut. Proc. Natl. Acad. Sci., 111, E2329-E2338.
24. Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K.S., Manichanh, C., Nielsen, T., Pons, N., Levenez, F. and Yamada, T. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature, 464, 59-65.
25. Jeraldo, P., Sipos, M., Chia, N., Brulc, J.M., Dhillon, A.S., Konkel, M.E., Larson, C.L., Nelson, K.E., Qu, A. and Schook, L.B. (2012) Quantification of the relative roles of niche and neutral processes in structuring gastrointestinal microbiomes. Proc. Natl. Acad. Sci., 109, 9692-9698.
26. Levy, R. and Borenstein, E. (2013) Metabolic modeling of species interaction in the human microbiome elucidates community-level assembly rules. Proc. Natl. Acad. Sci., 110, 12804-12809.
27. Raes, J. and Bork, P. (2008) Molecular eco-systems biology: towards an understanding of community function. Nat. Rev. Microbiol., 6, 693-699.
28. Woyke, T., Teeling, H., Ivanova, N.N., Huntemann, M., Richter, M., Gloeckner, F.O., Boffelli, D., Anderson, I.J., Barry, K.W., Shapiro, H.J. et al. (2006) Symbiosis insights through metagenomic analysis of a microbial consortium. Nature, 443, 950-955.
29. Wu, D., Daugherty, S.C., Van Aken, S.E., Pai, G.H., Watkins, K.L., Khouri, H., Tallon, L.J., Zaborsky, J.M., Dunbar, H.E., Tran, P.L. et al. (2006) Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol., 4, e188.
30. Qin, J., Li, Y., Cai, Z., Li, S., Zhu, J., Zhang, F., Liang, S., Zhang, W., Guan, Y. and Shen, D. (2012) A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature, 490, 55-60.
31. Brulc, J.M., Antonopoulos, D.A., Miller, M.E., Wilson, M.K., Yannarell, A.C., Dinsdale, E.A., Edwards, R.E., Frank, E.D., Emerson, J.B., Wacklin, P. et al. (2009) Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc. Natl. Acad. Sci. U.S.A., 106, 1948-1953.
32. Zhu, X., Gerstein, M. and Snyder, M. (2007) Getting connected: analysis and principles of biological networks. Genes Dev., 21, 1010-1024.
33. Wang, Z., Nkrumah, J., Li, C., Basarab, J., Goonewardene, L., Okine, E., Crews, D. and Moore, S. (2006) Test duration for growth, feed intake, and feed efficiency in beef cattle using the GrowSafe System. J. Anim. Sci., 84, 2289-2298.
34. Ewing, B. and Green, P. (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res., 8, 186-194.
35. Cole, J.R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R.J., Kulam-Syed-Mohideen, A.S., McGarrell, D.M., Marsh, T., Garrity, G.M. et al. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res., 37, D141-D145.
36. Benson, D.A., Cavanaugh, M., Clark, K., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J. and Sayers, E.W. (2013) GenBank. Nucleic Acids Res., 41, D36-D42.
37. Ellison, M.J., Conant, G.C., Cockrum, R.R., Austin, K.J., Truong, H., Becchi, M., Lamberson, W.R. and Cammack, K.M. (2014) Diet alters both the structure and taxonomy of the ovine gut microbial ecosystem. DNA Res., 21, 115-125.
38. Miller, C.S., Baker, B.J., Thomas, B.C., Singer, S.W. and Banfield, J.F. (2011) EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data. Genome Biol., 12, R44.
39. Needleman, S.B. and Wunsch, C.D. (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J. Mol. Biol., 48, 443-453.
40. Truong, H., Li, D., Sajjapongse, K., Conant, G. and Becchi, M. (2014) Large-scale pairwise alignments on GPU clusters: exploring the implementation space. J. Signal Process. Syst., 1-19.
41. Langmead, B., Trapnell, C., Pop, M. and Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, R25.
42. Caspi, R., Altman, T., Billington, R., Dreher, K., Foerster, H., Fulcher, C.A., Holland, T.A., Keseler, I.M., Kothari, A., Kubo, A. et al. (2014) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases. Nucleic Acids Res., 42, D459-D471.
43. Bekaert, M. and Conant, G.C. (2011) Copy number alterations among mammalian enyzmes cluster in the metabolic network. Mol. Biol. Evol., 28, 1111-1121.
44. Conant, G.C. (2009) Neutral evolution on mammalian protein surfaces. Trends Genet., 25, 377-381.
45. Flicek, P., Ahmed, I., Amode, M.R., Barrell, D., Beal, K., Brent, S., Carvalho-Silva, D., Clapham, P., Coates, G., Fairley, S. et al. (2013) Ensembl 2013. Nucleic Acids Res., 41, D48-D55.
46. Hudson, C.M. and Conant, G.C. (2011) Expression level, cellular compartment and metabolic network position all influence the average selective constraint on mammalian enzymes. BMC Evol. Biol., 11, 89.
47. Pérez-Bercoff, Å., McLysaght, A. and Conant, G.C. (2011) Patterns of indirect protein interactions suggest a spatial organization to metabolism. Mol. Biosyst., 7, 3056-3064.
48. Bergman, E. (1990) Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol. Rev., 70, 567-590.
49. Duarte, N.C., Becker, S.A., Jamshidi, N., Thiele, I., Mo, M.L., Vo, T.D., Srivas, R. and Palsson, B.Ø. (2007) Global reconstruction of the human metabolic network based on genomic and bibliomic data. Proc. Natl. Acad. Sci. U.S.A., 104, 1777-1782.
50. Yoon, J., Blumer, A. and Lee, K. (2006) An algorithm for modularity analysis of directed and weighted biological networks based on edge-betweenness centrality. Bioinformatics, 22, 3106-3108.
51. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J.H., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped Blast and Psi-Blast : a new-generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402.
52. Doring, A., Weese, D., Rausch, T. and Reinert, K. (2008) SeqAn an efficient, generic C++ library for sequence analysis. BMC Bioinformatics, 9, 11.
53. Smith, T.F. and Waterman, M.S. (1981) Identification of common molecular subsequences. J. Mol. Biol., 147, 195-197.
54. R Development Core Team. (2008) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
55. Strickland, M.S., Lauber, C., Fierer, N. and Bradford, M.A. (2009) Testing the functional significance of microbial community composition. Ecology, 90, 441-451.
56. Matias Rodrigues, J.F. and Wagner, A. (2009) Evolutionary plasticity and innovations in complex metabolic reaction networks. PLoS Comput. Biol., 5, e1000613.
57. Janga, S.C. and Babu, M.M. (2008) Network-based approaches for linking metabolism with environment. Genome Biol., 9, 239.
58. Stolyar, S., Van Dien, S., Hillesland, K.L., Pinel, N., Lie, T.J., Leigh, J.A. and Stahl, D.A. (2007) Metabolic modeling of a mutualistic microbial community. Mol. Syst. Biol., 3, 92.
59. Ross, E.M., Moate, P.J., Bath, C.R., Davidson, S.E., Sawbridge, T.I., Guthridge, K.M., Cocks, B.G. and Hayes, B.J. (2012) High throughput whole rumen metagenome profiling using untargeted massively parallel sequencing. BMC Genet., 13, 53.
60. Weimer, P., Stevenson, D., Mantovani, H. and Man, S. (2010) Host specificity of the ruminal bacterial community in the dairy cow following near-total exchange of ruminal contents. J. Dairy Sci., 93, 5902-5912.
61. Hubbell, S.P. (2006) Neutral theory and the evolution of ecological equivalence. Ecology, 87, 1387-1398.
62. Wagner, A. (2005) Robustness and Evolvability in Living Systems. Princeton University Press, Princeton, NJ.
63. Duarte, N.C., Herrgård, M.J. and Palsson, B.Ø. (2004) Reconstruction and validation of Saccharomyces cerevisiae iND750, a fully compartmentalized genome-scale metabolic model. Genome Res., 14, 1298-1309.
64. Chave, J. (2004) Neutral theory and community ecology. Ecol. Lett., 7, 241-253.