Gut microbes of mammalian herbivores facilitate intake of plant toxins

Ecology Letters

Volumn 17, Issue 10, 2014, Pages 1238-1246

  Kohl, Kevin D ^a   Weiss, Robert B ^b   Cox, James ^b   Dale, Colin ^a   Dearing, M Denise ^a  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Detoxification; Herbivory; Host microbe interactions; Mammalian herbivore; Microbiome; Plant secondary compounds; Plant herbivore interactions; Symbiosis

Indexed keywords

MAMMALIA;

TOXIN;

ANIMAL; CHEMISTRY; DIET; GASTROINTESTINAL TRACT; HERBIVORY; LARREA; METABOLISM; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY; SIGMODONTINAE; VETERINARY;

ANIMALS; DIET; GASTROINTESTINAL TRACT; HERBIVORY; LARREA; MICROBIOTA; SIGMODONTINAE; TOXINS, BIOLOGICAL;

EID: 84908278472     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/ele.12329     Document Type: Article

References (44)

1. Betancourt, J.L., Van Devender, T.R. & Martin, P.S. (1990). Packrat Middens: The Last 40,000 years of Biotic Change. University of Arizona Press, Tucson, AZ.
2. Bjöorkholm, B., Bok, C.M., Lundin, A., Rafter, J., Hibberd, M.L. & Pettersson, S. (2009). Intestinal microbiota regulate xenobiotic metabolism in the liver. PLoS ONE, 4, e6958.
3. Blum, U. & Shafer, S.R. (1988). Microbial populations and phenolic acids in soil. Soil Biol. Biochem., 20, 793-800.
4. Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Huntley, J., Fierer, N. et al. (2012). Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J., 6, 1621-1624.
5. Dearing, M.D. (2013). Temperature-dependent toxicity in mammals with implications for herbivores: a review. J. Comp. Physiol. B., 183, 43-50.
6. Dearing, M.D., Mangione, A.M. & Karasov, W.H. (2000). Diet breadth of mammalian herbivores: nutrient versus detoxification constraints. Oecologia, 123, 397-405.
7. Dearing, M.D., Foley, W.J. & McLean, S. (2005). The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Ann. Rev. Ecol. Evol. Syst., 36, 169-185.
8. Foley, W.J., McLean, S. & Cork, S.J. (1995). Consequences of biotransformation of plant secondary metabolites on acid-base metabolism in mammals - a final common pathway? J. Chem. Ecol., 21, 721-743.
9. Freeland, W.J. & Janzen, D.H. (1974). Strategies in herbivory by mammals: the role of plant secondary compounds. Amer. Nat., 108, 269-287.
10. Goodman, T., Grice, H.C., Becking, G.C. & Salem, F.A. (1970). A cystic nephropathy induced by nordihydroguaiaretic acid in the rat: light and electron microscopic investigations. Lab. Invest., 23, 93-107.
11. Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol., 59, 307-321.
12. Jones, R.J. & Megarrity, R.G. (1986). Successful transfer of DHPdegrading bacteria from Hawaiian goats to Australian ruminants to overcome the toxicity of Leucaena. Aust. Vet. J., 63, 259.
13. Karasov, W.H. (1989). Nutritional bottleneck in a herbivore, the desert woodrat (Neotoma lepida). Physiol. Zool., 62, 1351-1382.
14. Kenagy, G.J. & Hoyt, D.F. (1980). Reingestion of feces in rodents and its daily rhythmicity. Oecologia, 44, 403-409.
15. Kohl, K.D. & Dearing, M.D. (2012). Experience matters: prior exposure to plant toxins enhances diversity of gut microbes in herbivores. Ecol. Lett., 15, 1008-1015.
16. Kohl, K.D. & Dearing, M.D. (2014). Wild-caught rodents retain a majority of their natural gut microbiota upon entrance into captivity. Environ. Microbiol. Rep., 6, 191-195.
17. Kohl, K.D., Weiss, R.B., Dale, C. & Dearing, M.D. (2011). Diversity and novelty of the gut microbial community of an herbivorous rodent (Neotoma bryanti). Symbiosis, 54, 47-54.
18. Krehbiel, C.R., Rust, S.R., Zhang, G. & Gilliland, S.E. (2003). Bacterial direct-fed microbials in ruminant diets: performance response and mode of action. J. Anim. Sci., 81, E120-E132.
19. Krishnamani, R. & Mahaney, W.C. (2000). Geophagy among primates: adaptive significance and ecological consequences. Anim. Behav., 59, 899-915.
20. Lambert, J.D., Zhao, D., Meyers, R.O., Kuester, R.K., Timmermann, B.N. & Dorr, R.T. (2002). Nordihydroguaiaretic acid: hepatotoxicity and detoxification in the mouse. Toxicon, 40, 1701-1708.
21. Mabry, T.J., DiFeo, D.R.J., Sakakibara, M., Bohnstedt, C.F.J. & Seigler, D. (1977). Tha natural products chemistry of Larrea. In: Creosote bush: Biology and Chemistry of Larrea in New World Deserts (eds Mabry, T.J., Hunziker, J.H. & DiFeo, D.R.J.). Hutchinson and Ross, Stroudsberg, pp. 115-134.
22. Magnanou, E., Malenke, J.R. & Dearing, M.D. (2009). Expression of biotransformation genes in woodrat (Neotoma) herbivores on novel and ancestral diets: identification of candidate genes responsible for dietary shifts. Mol. Ecol., 18, 2401-2414.
23. Mangione, A.M., Dearing, M.D. & Karasov, W.H. (2000). Interpopulation differences in tolerance to creosote bush resin in desert woodrats (Neotoma lepida). Ecology, 81, 2067-2076.
24. Mangione, A.M., Dearing, M.D. & Karasov, W.H. (2001). Detoxification in relation to toxin tolerance in desert woodrats eating creosote bush. J. Chem. Ecol., 27, 2559-2578.
25. Manichanh, C., Reeder, J., Gilbert, P., Varela, E., Llopis, M., Antolin, M. et al. (2010). Reshaping the gut microbiome with bacterial transplantation and antibiotic intake. Genome Res., 20, 1411-1419.
26. Markle, J.G.M., Frank, D.N., Mortin-Toth, S., Robertson, C.E., Feazel, L.M., Rolle-Kampczyk, U. et al. (2013). Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science, 339, 1084-1088.
27. Martin, T.E. & Maron, J.L. (2012). Climate impacts on birds and plant communities from altered animal-plant interactions. Nat. Clim. Change, 2, 195-200.
28. Maurice, C.F., Haiser, H.J. & Turnbaugh, P.J. (2013). Xenobiotics shape the physiology and gene expression of the active human gut microbiome. Cell, 152, 39-50.
29. Meyer, F., Paarmann, D., D'Souza, M., Olson, R., Glass, E.M., Kubal, M. et al. (2008). The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics, 9, 386.
30. Moore, B.D. & Foley, W.J. (2005). Tree use by koalas in a chemically complex landscape. Nature, 435, 488-490.
31. Muheim, A., Waldner, R., Sanglard, D., Reiser, J., Schoemaker, H.E. & Leisola, M.S.A. (1991). Purification and properties of an aryl-alcohol dehydrogenase from the white-rot fungus Phanerochaete chrysosporium. Eur. J. Biochem., 195, 369-375.
32. Overbeek, R., Begley, T., Butler, R.M., Choudhuri, J.V., Chuang, H.-Y., Cohoon, M. et al. (2005). The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res., 33, 5691-5702.
33. Peng, Y., Leung, H.C., Yiu, S.M. & Chin, F.Y. (2012). IDBA-UD: a de novo assembler for single cell and metagenomic sequencing data with highly uneven depth. Bioinformatics, 28, 1420-1428.
34. Price, S.A., Hopkins, S.S.B., Smith, K.K. & Roth, V.L. (2012). Tempo of trophic evolution and its impact on mammalian diversification. Proc. Natl Acad. Sci., 109, 7008-7012.
35. Quintero, I. & Wiens, J.J. (2013). Rates of projected climate change dramatically exceed past rates of climate niche evolution among vertebrate species. Ecol. Lett., 16, 1095-1103.
36. Rios, J.M., Mangione, A.M. & Gianello, J.C. (2008). Effects of natural phenolic compounds from a desert dominant shrub Larrea divaricata Cav. on toxicity and survival in mice. Rev. Chil. Hist. Nat., 81, 293-302.
37. Sorensen, J.S., McLister, J.D. & Dearing, M.D. (2005). Plant secondary metabolites compromise the energy budgets of specialist and generalist mammalian herbivores. Ecology, 86, 125-139.
38. Sundset, M.A., Barboza, P.S., Green, T.K., Folkow, L.P., Blix, A.S. & Mathiesen, S.D. (2010). Microbial degradation of usnic acid in the reindeer rumen. Naturwissenschaften, 97, 273-278.
39. Van Devender, T.R. & Spaulding, W.G. (1979). Development of vegetation and climate in the southwestern United States. Science, 204, 701-710.
40. Verástegui, M.A., Sánchez, C.A., Heredia, N.L. & García-Alvarado, J.S. (1996). Antimicrobial activity of extracts of three major plants from the Chihuahuan desert. J. Ethnopharmacol., 52, 175-177.
41. Verhoeven, K.J.F., Biere, A., Harvey, J.A. & Van Der Putten, W.H. (2009). Plant invaders and their novel natural enemies: who is na€i{dotless}ve? Ecol. Lett., 12, 107-117.
42. Vijay-Kumar, M., Aitken, J.D., Carvalho, F.A., Cullender, T.C., Mwangi, S., Srinivasan, S. et al. (2010). Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science, 328, 228-231.
43. Vorhies, C.T. & Taylor, W.P. (1940). Life history and ecology of the white-throated wood rat, Neotoma albigula albigula Hartley, in relation to grazing in Arizona. Univ. Arizona Agric. Tech. Bull., 86, 453-529.
44. Whelan, S. & Goldman, N. (2001). A general empirical model of protein evolution derived from multiple protein families using a maximumlikelihood approach. Mol. Biol. Evol., 18, 691-699.