1932

Abstract

The longstanding interactions between mammals and their symbionts enable thousands of mammal species to consume herbivorous diets. The microbial communities in mammals degrade both plant fiber and toxins. Microbial toxin degradation has been repeatedly documented in domestic ruminants, but similar work in wild mammals is more limited due to constraints on sampling and manipulating the microbial communities in these species. In this review, we briefly describe the toxins commonly encountered in mammalian diets, major classes of biotransformation enzymes in microbes and mammals, and the gut chambers that house symbiotic microbes. We next examine evidence for microbial detoxification in domestic ruminants before providing case studies on microbial toxin degradation in both foregut- and hindgut-fermenting wild mammals. We end by discussing species that may be promising for future investigations, and the advantages and limitations of approaches currently available for studying degradation of toxins by mammalian gut microbes.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-111121-085333
2022-09-08
2024-06-02
Loading full text...

Full text loading...

/deliver/fulltext/micro/76/1/annurev-micro-111121-085333.html?itemId=/content/journals/10.1146/annurev-micro-111121-085333&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Aagnes TH, Sørmo W, Mathiesen SD. 1995. Ruminal microbial digestion in free-living, in captive lichen-fed, and in starved reindeer (Rangifer tarandus tarandus) in winter. Appl. Environ. Microbiol. 61:2583–91
    [Google Scholar]
  2. 2.
    Agrawal AA, Petschenka G, Bingham RA, Weber MG, Rasmann S. 2012. Toxic cardenolides: chemical ecology and coevolution of specialized plant-herbivore interactions. New Phytol 194:128–45
    [Google Scholar]
  3. 3.
    Allen AR, Booker L, Rockwood GA 2016. Acute cyanide toxicity. Toxicology of Cyanides and Cyanogens AH Hall, GE Isom, GA Rockwood 1–20 Chichester, UK: John Wiley
    [Google Scholar]
  4. 4.
    Allison MJ, Hammond AC, Jones RJ. 1990. Detection of ruminal bacteria that degrade toxic dihydroxypyridine compounds produced from mimosine. Appl. Environ. Microbiol. 56:3590–94
    [Google Scholar]
  5. 5.
    Allison MJ, Mayberry WR, Mcsweeney CS, Stahl DA. 1992. Synergistes jonesii, gen. nov., sp.nov.: a rumen bacterium that degrades toxic pyridinediols. Syst. Appl. Microbiol. 15:4522–29
    [Google Scholar]
  6. 6.
    Aung A. 2019. Leucaena feeding systems in Myanmar. Trop. Grassl. Forrajes Trop. 7:4423–27
    [Google Scholar]
  7. 7.
    Barba FJ, Nikmaram N, Roohinejad S, Khelfa A, Zhu Z, Koubaa M. 2016. Bioavailability of glucosinolates and their breakdown products: impact of processing. Front. Nutr 3:24
    [Google Scholar]
  8. 8.
    Barker CJ, Gillett A, Polkinghorne A, Timms P. 2013. Investigation of the koala (Phascolarctos cinereus) hindgut microbiome via 16S pyrosequencing. Vet. Microbiol. 167:3–4554–64
    [Google Scholar]
  9. 9.
    Bezard P, Brilland S, Kumpula J. 2015. Composition of late summer diet by semi-domesticated reindeer in different grazing conditions in northernmost Finland. Rangifer 35:139–52
    [Google Scholar]
  10. 10.
    Bjørkvoll E, Pedersen B, Hytteborn H, Jónsdóttir IS, Langvatn R. 2009. Seasonal and interannual dietary variation during winter in female Svalbard reindeer (Rangifer tarandus platyrhynchus). Arct. Antarct. Alp. Res. 41:188–96
    [Google Scholar]
  11. 11.
    Blyton MDJ, Soo RM, Hugenholtz P, Moore BD. 2022. Characterization of the juvenile koala gut microbiome across wild populations. Environ. Microbiol. In press. https://doi.org/10.1111/1462-2920.15884
    [Crossref] [Google Scholar]
  12. 12.
    Blyton MDJ, Soo RM, Hugenholtz P, Moore BD. 2022. Maternal inheritance of the koala gut microbiome and its compositional and functional maturation during juvenile development. Environ. Microbiol. 24:1475–93
    [Google Scholar]
  13. 13.
    Brodie ED. 1977. Hedgehogs use toad venom in their own defence. Nature 268:5621627–28
    [Google Scholar]
  14. 14.
    Browne HP, Forster SC, Anonye BO, Kumar N, Neville BA et al. 2016. Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation. Nature 533:7604543–46
    [Google Scholar]
  15. 15.
    Cambiom EKA, Almeida AP, Tadra-Sfeir MZ, Junior FG, Andrade PP et al. 2012. Isolation and identification of sodium fluoroacetate degrading bacteria from caprine rumen in Brazil. Sci. World J. 2012:178254
    [Google Scholar]
  16. 16.
    Carman RJ, Waynforth HB. 1984. Chronic fistulation and cannulation of the rabbit caecum. Lab. Anim. 18:3258–60
    [Google Scholar]
  17. 17.
    Carmody RN, Turnbaugh PJ. 2014. Host-microbial interactions in the metabolism of therapeutic and diet-derived xenobiotics. J. Clin. Investig. 124:104173–81
    [Google Scholar]
  18. 18.
    Castillo C, Hernández J. 2021. Ruminal fistulation and cannulation: a necessary procedure for the advancement of biotechnological research in ruminants. Animals 11:71870
    [Google Scholar]
  19. 19.
    Chau R, Kalaitzis JA, Neilan BA. 2011. On the origins and biosynthesis of tetrodotoxin. Aquat. Toxicol. 104:1–261–72
    [Google Scholar]
  20. 20.
    Chen L, Qiu Q, Jiang Y, Wang K, Lin Z et al. 2019. Large-scale ruminant genome sequencing provides insights into their evolution and distinct traits. Science 364:6446eaav6202
    [Google Scholar]
  21. 21.
    Cipollone R, Frangipani E, Tiburzi F, Imperi F, Ascenzi P, Visca P. 2007. Involvement of Pseudomonas aeruginosa rhodanese in protection from cyanide toxicity. Appl. Environ. Microbiol. 73:2390–98
    [Google Scholar]
  22. 22.
    Clarke G, Sandhu KV, Griffin BT, Dinan TG, Cryan JF, Hyland NP. 2019. Gut reactions: breaking down xenobiotic-microbiome interactions. Pharmacol. Rev. 71:2198–224
    [Google Scholar]
  23. 23.
    Cocchietto M, Skert N, Nimis P, Sava G. 2002. A review on usnic acid, an interesting natural compound. Naturwissenschaften 89:4137–46
    [Google Scholar]
  24. 24.
    Cork SJ, Hume ID, Dawson TJ. 1983. Digestion and metabolism of a natural foliar diet (Eucalyptus punctata) by an arboreal marsupial, the koala (Phascolarctos cinereus). J. Comp. Physiol. B 153:2181–90
    [Google Scholar]
  25. 25.
    Cork SJ, Warner ACI. 1983. The passage of digesta markers through the gut of a folivorous marsupial, the koala Phascolarctos cinereus. J. Comp. Physiol. B 152:143–51
    [Google Scholar]
  26. 26.
    Couet CE, Hopley J, Hanley AB. 1996. Metabolic activation of pyrrolizidine alkaloids by human, rat and avocado microsomes. Toxicon 34:91058–61
    [Google Scholar]
  27. 27.
    Cressey P, Reeve J. 2019. Metabolism of cyanogenic glycosides: a review. Food Chem. Toxicol. 125:225–32
    [Google Scholar]
  28. 28.
    Culvenor CCJ, Dann AT, Dick AT. 1962. Alkylation as the mechanism by which the hepatotoxic pyrrolizidine alkaloids act on cell nuclei. Nature 195:4841570–73
    [Google Scholar]
  29. 29.
    Dahlhausen KE, Jospin G, Coil DA, Eisen JA, Wilkins LGE. 2020. Isolation and sequence-based characterization of a koala symbiont: Lonepinella koalarum. PeerJ 8:e10177
    [Google Scholar]
  30. 30.
    Dailey RN, Montgomery DL, Ingram JT, Siemion R, Vasquez M, Raisbeck MF. 2008. Toxicity of the lichen secondary metabolite (+)-usnic acid in domestic sheep. Vet. Pathol. 45:119–25
    [Google Scholar]
  31. 31.
    David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE et al. 2014. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:7484559–63
    [Google Scholar]
  32. 32.
    Davis CK, Webb RI, Sly LI, Denman SE, McSweeney CS. 2012. Isolation and survey of novel fluoroacetate-degrading bacteria belonging to the phylum Synergistetes. FEMS Microbiol. Ecol. 80:3671–84
    [Google Scholar]
  33. 33.
    Davis DD. 1964. The Giant Panda: A Morphological Study of Evolutionary Mechanisms Chicago: Chic. Nat. Hist. Mus.
  34. 34.
    Dawson KA, Allison MJ, Hartman PA. 1980. Isolation and some characteristics of anaerobic oxalate-degrading bacteria from the rumen. Appl. Environ. Microbiol. 40:4833–39
    [Google Scholar]
  35. 35.
    Dearing MD, Foley WJ, McLean S. 2005. The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Annu. Rev. Ecol. Evol. Syst. 36:169–89
    [Google Scholar]
  36. 36.
    Demment MW, Van Soest PJ. 1985. A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores. Am. Nat. 125:5641–72
    [Google Scholar]
  37. 37.
    Derakhshani H, Corley SW, Al Jassim R. 2016. Isolation and characterization of mimosine, 3, 4 DHP and 2, 3 DHP degrading bacteria from a commercial rumen inoculum: isolation of mimosine degrading bacteria. J. Basic Microbiol. 56:5580–85
    [Google Scholar]
  38. 38.
    Dierenfeld ES, Hintz HF, Robertson JB, Van Soest PJ, Oftedal OT. 1982. Utilization of bamboo by the giant panda. J. Nutr. 112:4636–41
    [Google Scholar]
  39. 39.
    Dominguez-Bello MG, Stewart CS 1990. Degradation of mimosine, 2,3-dihydroxy pyridine and 3-hydroxy-4(1H)-pyridine by bacteria from the rumen of sheep in Venezuela. FEMS Microbiol. Lett. 73:4283–89
    [Google Scholar]
  40. 40.
    Duarte ALL, Medeiros RMT, Carvalho FKL, Lee ST, Cook D et al. 2014. Induction and transfer of resistance to poisoning by Amorimia (Mascagnia) septentrionalis in goats. J. Appl. Toxicol. 34:2220–23
    [Google Scholar]
  41. 41.
    Duncan AJ, Milne JA. 1992. Rumen microbial degradation of allyl cyanide as a possible explanation for the tolerance of sheep to brassica-derived glucosinolates. J. Sci. Food Agric. 58:115–19
    [Google Scholar]
  42. 42.
    El-Nezami H, Kankaanpaa P, Salminen S, Ahokas J. 1998. Ability of dairy strains of lactic acid bacteria to bind a common food carcinogen, aflatoxin B1. Food Chem. Toxicol. 36:4321–26
    [Google Scholar]
  43. 43.
    Erb M, Kliebenstein DJ. 2020. Plant secondary metabolites as defenses, regulators, and primary metabolites: the blurred functional trichotomy. Plant Physiol 184:139–52
    [Google Scholar]
  44. 44.
    Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H et al. 2013. The long-term stability of the human gut microbiota. Science 341:61411237439
    [Google Scholar]
  45. 45.
    Ferretti P, Pasolli E, Tett A, Asnicar F, Gorfer V et al. 2018. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host Microbe 24:1133–45.e5
    [Google Scholar]
  46. 46.
    Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. 2012. Microbial degradation of complex carbohydrates in the gut. Gut Microbes 3:4289–306
    [Google Scholar]
  47. 47.
    Freeland WJ, Janzen DH. 1974. Strategies in herbivory by mammals: the role of plant secondary compounds. Am. Nat. 108:961269–89
    [Google Scholar]
  48. 48.
    Glad T, Barboza P, Mackie RI, Wright A-DG, Brusetti L et al. 2014. Dietary supplementation of usnic acid, an antimicrobial compound in lichens, does not affect rumen bacterial diversity or density in reindeer. Curr. Microbiol. 68:6724–28
    [Google Scholar]
  49. 49.
    Glendinning JI, Mejia AA, Brower LP. 1988. Behavioral and ecological interactions of foraging mice (Peromyscus melanotis) with overwintering monarch butterflies (Danaus plexippus) in Mexico. Oecologia 75:2222–27
    [Google Scholar]
  50. 50.
    Goel G, Puniya AK, Singh K. 2007. Phenotypic characterization of tannin-protein complex degrading bacteria from faeces of goat. Small Rumin. Res. 69:1–3217–20
    [Google Scholar]
  51. 51.
    Gołębiewski M, Tretyn A. 2020. Generating amplicon reads for microbial community assessment with next-generation sequencing. J. Appl. Microbiol. 128:2330–54
    [Google Scholar]
  52. 52.
    Goncharov NV, Jenkins RO, Radilov AS. 2006. Toxicology of fluoroacetate: a review, with possible directions for therapy research. J. Appl. Toxicol. 26:2148–61
    [Google Scholar]
  53. 53.
    Gu S, Chen D, Zhang J-N, Lv X, Wang K et al. 2013. Bacterial community mapping of the mouse gastrointestinal tract. PLOS ONE 8:10e74957
    [Google Scholar]
  54. 54.
    Gustine DL, Moyer BG, Wangsness PJ, Shenk JS. 1977. Ruminal metabolism of 3-nitropropanoyl-d-glucopyranoses from crownvetch. J. Anim. Sci. 44:61107–11
    [Google Scholar]
  55. 55.
    Haiser HJ, Seim KL, Balskus EP, Turnbaugh PJ. 2014. Mechanistic insight into digoxin inactivation by Eggerthella lenta augments our understanding of its pharmacokinetics. Gut Microbes 5:2233–38
    [Google Scholar]
  56. 56.
    Halliday MJ, Pakereng C, Edison RG, Ara P, Dida PR et al. 2019. Effectiveness of inoculation with rumen fluid containing Synergistes jonesii to control DHP toxicity in ruminants in eastern Indonesia. Trop. Grassl. Forrajes Trop. 7:3252–57
    [Google Scholar]
  57. 57.
    Halliday MJ, Padmanabha J, McSweeney CS et al. 2013. Leucaena toxicity: a new perspective on the most widely used forage tree legume. Trop. Grassl. Forrajes Trop. 1:11
    [Google Scholar]
  58. 58.
    Halliday MJ, Giles HE, Dalzell SA, McSweeney CS, Shelton HM 2014. The efficacy of in vitro Synergistes jonesii inoculum in preventing DHP toxicity in steers fed leucaena-grass diets. Trop. Grassl. Forrajes Trop. 2:168
    [Google Scholar]
  59. 59.
    Hammer TJ, Bowers MD. 2015. Gut microbes may facilitate insect herbivory of chemically defended plants. Oecologia 179:11–14
    [Google Scholar]
  60. 60.
    Hartmann T. 2007. From waste products to ecochemicals: fifty years research of plant secondary metabolism. Phytochemistry 68:22–242831–46
    [Google Scholar]
  61. 61.
    He P, Young LG, Forsberg C. 1992. Microbial transformation of deoxynivalenol (vomitoxin). Appl. Environ. Microbiol. 58:123857–63
    [Google Scholar]
  62. 62.
    Hornicke H, Bjornhag G. 1980. Coprophagy and related strategies for digesta utilization. Digestive Physiology and Metabolism in Ruminants: Proceedings of the 5th International Symposium on Ruminant Physiology, Clermont—Ferrand, 3rd–7th September, 1979 Y Ruckebusch, P Thivend 707–30 Dordrecht, Neth.: Springer
    [Google Scholar]
  63. 63.
    Huang H, Yie S, Liu Y, Wang C, Cai Z et al. 2016. Dietary resources shape the adaptive changes of cyanide detoxification function in giant panda (Ailuropoda melanoleuca). Sci. Rep. 6:134700
    [Google Scholar]
  64. 64.
    Hult K, Teiling A, Gatenbeck S. 1976. Degradation of ochratoxin A by a ruminant. Appl. Environ. Microbiol. 32:3443–44
    [Google Scholar]
  65. 65.
    Ichinohe T, Orden EA, Del Barrio AN, Lapitan RM, Fujihara T et al. 2004. Comparison of voluntary feed intake, rumen passage and degradation kinetics between crossbred Brahmam cattle (Bos indicus) and swamp buffaloes (Bubalus bubalis) fed a fattening diet based on corn silage. Anim. Sci. J. 75:6533–40
    [Google Scholar]
  66. 66.
    Janis C. 1976. The evolutionary strategy of the equidae and the origins of rumen and cecal digestion. Evolution 30:4757–74
    [Google Scholar]
  67. 67.
    Jones RJ, Megarrity RG. 1983. Comparative toxicity responses of goats fed on Leucaena leucocephala in Australia and Hawaii. Aust. J. Agric. Res. 34:678190
    [Google Scholar]
  68. 68.
    Jones RJ, Megarrity RG. 1986. Successful transfer of DHP-degrading bacteria from Hawaiian goats to Australian ruminants to overcome the toxicity of Leucaena. Aust. Vet. J. 63:8259–62
    [Google Scholar]
  69. 69.
    Kang S, Khan S, Webb R, Denman S, McSweeney C. 2020. Characterization and survey in cattle of a rumen Pyrimadobacter sp. which degrades the plant toxin fluoroacetate. FEMS Microbiol. Ecol. 96:7fiaa077
    [Google Scholar]
  70. 70.
    Karasov WH, Douglas AE. 2013. Comparative digestive physiology. Compr. Physiol. 3:2741–83
    [Google Scholar]
  71. 71.
    Kiessling KH, Pettersson H, Sandholm K, Olsen M. 1984. Metabolism of aflatoxin, ochratoxin, zearalenone, and three trichothecenes by intact rumen fluid, rumen protozoa, and rumen bacteria. Appl. Environ. Microbiol. 47:51070–73
    [Google Scholar]
  72. 72.
    Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T. 2012. Symbiont-mediated insecticide resistance. PNAS 109:228618–22
    [Google Scholar]
  73. 73.
    Klaassen CD 2019. Casarett and Doull's Toxicology: The Basic Science of Poisons New York: McGraw-Hill
  74. 74.
    Klein DR. 1982. Fire, lichens, and caribou. J. Range Manag. 35:339095
    [Google Scholar]
  75. 75.
    Klieve AV, Ouwerkerk D, Turner A, Roberton R. 2002. The production and storage of a fermentor-grown bacterial culture containing Synergistes jonesii, for protecting cattle against mimosine and 3-hydroxy-4(1H)-pyridone toxicity from feeding on Leucaena leucocephala. Aust. J. Agric. Res. 53:115
    [Google Scholar]
  76. 76.
    Kohl K, Dearing MD. 2012. Experience matters: Prior exposure to plant toxins enhances diversity of cut microbes in herbivores. Ecol. Lett.151008–15
    [Google Scholar]
  77. 77.
    Kohl KD. 2020. Ecological and evolutionary mechanisms underlying patterns of phylosymbiosis in host-associated microbial communities. Philos. Trans. R. Soc. B 375:179820190251
    [Google Scholar]
  78. 78.
    Kohl KD, Connelly JW, Dearing MD, Forbey JS. 2016. Microbial detoxification in the gut of a specialist avian herbivore, the Greater Sage-Grouse. FEMS Microbiol. Lett. 363:14fnw144
    [Google Scholar]
  79. 79.
    Kohl KD, Dearing MD. 2016. The woodrat gut microbiota as an experimental system for understanding microbial metabolism of dietary toxins. Front. Microbiol. 7:1165
    [Google Scholar]
  80. 80.
    Kohl KD, Miller AW, Marvin JE, Mackie R, Dearing MD. 2014. Herbivorous rodents (Neotoma spp.) harbour abundant and active foregut microbiota: foregut microbes in herbivorous woodrats. Environ. Microbiol. 16:92869–78
    [Google Scholar]
  81. 81.
    Kohl KD, Stengel A, Dearing MD. 2016. Inoculation of tannin-degrading bacteria into novel hosts increases performance on tannin-rich diets: Tannin-degrading bacteria aid hosts consuming tannins. Environ. Microbiol. 18:61720–29
    [Google Scholar]
  82. 82.
    Kohl KD, Stengel A, Samuni-Blank M, Dearing MD. 2013. Effects of anatomy and diet on gastrointestinal pH in rodents: anatomy, diet, and gut pH in rodents. J. Exp. Zool. 319:4225–29
    [Google Scholar]
  83. 83.
    Kohl KD, Weiss RB, Cox J, Dale C, Dearing MD. 2014. Gut microbes of mammalian herbivores facilitate intake of plant toxins. Ecol. Lett. 17:101238–46
    [Google Scholar]
  84. 84.
    Koppel N, Maini Rekdal V, Balskus EP 2017. Chemical transformation of xenobiotics by the human gut microbiota. Science 356:6344eaag2770
    [Google Scholar]
  85. 85.
    Krockenberger AK, Hume ID. 2007. A flexible digestive strategy accommodates the nutritional demands of reproduction in a free-living folivore, the Koala (Phascolarctos cinereus). Funct. Ecol. 21:4748–56
    [Google Scholar]
  86. 86.
    Lanigan GW. 1976. Peptococcus heliotrinreducans, sp.nov., a cytochrome-producing anaerobe which metabolizes pyrrolizidine alkaloids. J. Gen. Microbiol. 94:11–10
    [Google Scholar]
  87. 87.
    Lattanzio V. 2013. Phenolic compounds: introduction. Natural Products, ed. KG Ramawat, J-M Mérillon1543–80 Berlin: Springer
    [Google Scholar]
  88. 88.
    Lehtonen P, Helander M, Wink M, Sporer F, Saikkonen K. 2005. Transfer of endophyte-origin defensive alkaloids from a grass to a hemiparasitic plant. Ecol. Lett. 8:121256–63
    [Google Scholar]
  89. 89.
    Leung JM, Graham AL, Knowles SCL. 2018. Parasite-microbiota interactions with the vertebrate gut: synthesis through an ecological lens. Front. Microbiol. 9:843
    [Google Scholar]
  90. 90.
    Levin D, Raab N, Pinto Y, Rothschild D, Zanir G et al. 2021. Diversity and functional landscapes in the microbiota of animals in the wild. Science 372:6539eabb5352
    [Google Scholar]
  91. 91.
    Levin DA. 1976. Alkaloid-bearing plants: an ecogeographic perspective. Am. Nat. 110:972261–84
    [Google Scholar]
  92. 92.
    Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR et al. 2008. Evolution of mammals and their gut microbes. Science 320:58831647–51
    [Google Scholar]
  93. 93.
    Lichman BR. 2021. The scaffold-forming steps of plant alkaloid biosynthesis. Nat. Prod. Rep. 38:1103–29
    [Google Scholar]
  94. 94.
    Ligabue-Braun R, Carlini CR 2015. Poisonous birds: a timely review. Toxicon 99:102–8
    [Google Scholar]
  95. 95.
    Lodge-Ivey SL, Rappe MS, Johnston WH, Bohlken RE, Craig AM. 2005. Molecular analysis of a consortium of ruminal microbes that detoxify pyrrolizidine alkaloids. Can. J. Microbiol. 51:6455–65
    [Google Scholar]
  96. 96.
    Loh ZH, Ouwerkerk D, Klieve AV, Hungerford NL, Fletcher MT. 2020. Toxin degradation by rumen microorganisms: a review. Toxins 12:10664
    [Google Scholar]
  97. 97.
    Mackie RI 1997. Gut environment and evolution of mutualistic fermentative digestion. Gastrointestinal Microbiology RI Mackie, BA White 13–35 Boston, MA: Springer
    [Google Scholar]
  98. 98.
    Mao S, Zhang M, Liu J, Zhu W. 2015. Characterising the bacterial microbiota across the gastrointestinal tracts of dairy cattle: membership and potential function. Sci. Rep. 5:116116
    [Google Scholar]
  99. 99.
    McKie MR, Brown DL, Melesse A, Odenyo AA. 2004. Rumen microbes from African ruminants can degrade Acacia angustissima diamino acids. Anim. Feed Sci. Technol. 117:3–4179–95
    [Google Scholar]
  100. 100.
    McSweeney CS, Blackall LL, Collins E, Conlan LL, Webb RI et al. 2005. Enrichment, isolation and characterisation of ruminal bacteria that degrade non-protein amino acids from the tropical legume Acacia angustissima. Anim. Feed Sci. Technol. 121:1–2191–204
    [Google Scholar]
  101. 101.
    McSweeney CS, Odenyo A, Krause DO. 2002. Rumen microbial responses to antinutritive factors in fodder trees and shrub legumes. J. Appl. Anim. Res. 21:2181–205
    [Google Scholar]
  102. 102.
    McSweeney CS, Padmanabha J, Halliday MJ, Hubbard B, Dierens L et al. 2019. Detection of Synergistes jonesii and genetic variants in ruminants from different geographical locations. Trop. Grassl. Forrajes Trop. 7:2154–63
    [Google Scholar]
  103. 103.
    Miller AW, Oakeson KF, Dale C, Dearing MD. 2016. Microbial community transplant results in increased and long-term oxalate degradation. Microb. Ecol. 72:2470–78
    [Google Scholar]
  104. 104.
    Moeller AH, Sanders JG. 2020. Roles of the gut microbiota in the adaptive evolution of mammalian species. Philos. Trans. R. Soc. B 375:180820190597
    [Google Scholar]
  105. 105.
    Molyneux RJ, Johnson AE, Stuart LD. 1988. Delayed manifestation of Senecio-induced pyrrolizidine alkaloidosis in cattle: case reports. Vet. Hum. Toxicol. 30:3201–5
    [Google Scholar]
  106. 106.
    Moore BD, Foley WJ. 2000. A review of feeding and diet selection in koalas (Phascolarctos cinereus). Aust. J. Zool. 48:331733
    [Google Scholar]
  107. 107.
    Nelson KE, Thonney ML, Woolston TK, Zinder SH, Pell AN. 1998. Phenotypic and phylogenetic characterization of ruminal tannin-tolerant bacteria. Appl. Environ. Microbiol. 64:103824–30
    [Google Scholar]
  108. 108.
    Nunn PB, Bell EA, Watson AA, Nash RJ. 2010. Toxicity of non-protein amino acids to humans and domestic animals. Nat. Prod. Commun. 5:31934578X1000500
    [Google Scholar]
  109. 109.
    Odenyo AA, McSweeney CS, Palmer B, Negassa D, Osuji PO. 1999. In vitro screening of rumen fluid samples from indigenous African ruminants provides evidence for rumen fluid with superior capacities to digest tannin-rich fodders. Aust. J. Agric. Res. 50:7114757
    [Google Scholar]
  110. 110.
    Osawa R. 1990. Formation of a clear zone on tannin-treated brain heart infusion agar by a Streptococcus sp. isolated from feces of koalas. Appl. Environ. Microbiol. 56:3829–31
    [Google Scholar]
  111. 111.
    Osawa R, Bird P, Harbrow D, Ogimoto K, Seymour G. 1993. Microbiological studies of the intestinal microflora of the koala, Phascolarctos-cinereus1. Colonization of the cecal wall by tannin-protein-complex-degrading Enterobacteria. Aust. J. Zool. 41:6599609
    [Google Scholar]
  112. 112.
    Osawa R, Carrick F. 1990. Use of a dietary supplement in koalas during systemic antibiotic treatment of chlamydial infection. Aust. Vet. J. 67:8305–7
    [Google Scholar]
  113. 113.
    Osawa R, Rainey F, Fujisawa T, Lang E, Busse HJ et al. 1995. Lonepinella koalarum gen. nov., sp. nov., a new tannin-protein complex degrading bacterium. Syst. Appl. Microbiol. 18:3368–73
    [Google Scholar]
  114. 114.
    Osawa R, Sly LI. 1992. Occurrence of tannin-protein complex degrading Streptococcus sp. in feces of various animals. Syst. Appl. Microbiol. 15:1144–47
    [Google Scholar]
  115. 115.
    Osawa R, Walsh TP, Cork SJ. 1993. Metabolism of tannin-protein complex by facultatively anaerobic bacteria isolated from koala feces. Biodegradation 4:291–99
    [Google Scholar]
  116. 116.
    Petschenka G, Agrawal AA. 2016. How herbivores coopt plant defenses: natural selection, specialization, and sequestration. Curr. Opin. Insect Sci. 14:17–24
    [Google Scholar]
  117. 117.
    Pichersky E, Lewinsohn E. 2011. Convergent evolution in plant specialized metabolism. Annu. Rev. Plant Biol. 62:549–66
    [Google Scholar]
  118. 118.
    Pichersky E, Raguso RA. 2018. Why do plants produce so many terpenoid compounds?. New Phytol 220:3692–702
    [Google Scholar]
  119. 119.
    Pimm SL, Joppa LN. 2015. How many plant species are there, where are they, and at what rate are they going extinct?. Ann. Mo. Bot. Gard. 100:3170–76
    [Google Scholar]
  120. 120.
    Polkinghorne A, Hanger J, Timms P. 2013. Recent advances in understanding the biology, epidemiology and control of chlamydial infections in koalas. Vet. Microbiol. 165:3–4214–23
    [Google Scholar]
  121. 121.
    Qin J, Li R, Raes J, Arumugam M, Burgdorf KS et al. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:728559–65
    [Google Scholar]
  122. 122.
    Quartinello F, Kremser K, Schoen H, Tesei D, Ploszczanski L et al. 2021. Together is better: the rumen microbial community as biological toolbox for degradation of synthetic polyesters. Front. Bioeng. Biotechnol. 9:684459
    [Google Scholar]
  123. 123.
    Rahman MM, Abdullah RB, Wan Khadijah WE 2013. A review of oxalate poisoning in domestic animals: tolerance and performance aspects. J. Anim. Physiol. Anim. Nutr. 97:4605–14
    [Google Scholar]
  124. 124.
    Ralphs MH, Creamer R, Baucom D, Gardner DR, Welsh SL et al. 2008. Relationship between the endophyte Embellisia spp. and the toxic alkaloid swainsonine in major locoweed species (Astragalus and Oxytropis). J. Chem. Ecol. 34:132–38
    [Google Scholar]
  125. 125.
    Reynolds JE, Rommel SA. 1996. Structure and function of the gastrointestinal tract of the Florida manatee, Trichechus manatus latirostris. Anat. Rec. 245:3539–58
    [Google Scholar]
  126. 126.
    Russell G, Smith R. 1968. Reduction of heliotrine by a rumen microorganism. Aust. J. Biol. Sci. 21:6127790
    [Google Scholar]
  127. 127.
    Salgado-Flores A, Hagen LH, Ishaq SL, Zamanzadeh M, Wright A-DG et al. 2016. Rumen and cecum microbiomes in reindeer (Rangifer tarandus tarandus) are changed in response to a lichen diet and may affect enteric methane emissions. PLOS ONE 11:5e0155213
    [Google Scholar]
  128. 128.
    Savitzky AH, Mori A, Hutchinson DA, Saporito RA, Burghardt GM et al. 2012. Sequestered defensive toxins in tetrapod vertebrates: principles, patterns, and prospects for future studies. Chemoecology 22:3141–58
    [Google Scholar]
  129. 129.
    Schaller GB 1985. The Giant Pandas of Wolong Chicago: Univ. Chicago Press
  130. 130.
    Shelton HM, Kerven G, Dalzell SA. 2019. An update on leucaena toxicity: Is inoculation with Synergistes jonesii necessary?. Trop. Grassl. Forrajes Trop. 7:2146–53
    [Google Scholar]
  131. 131.
    Skopec MM, Hagerman AE, Karasov WH. 2004. Do salivary proline-rich proteins counteract dietary hydrolyzable tannin in laboratory rats?. J. Chem. Ecol. 30:91679–92
    [Google Scholar]
  132. 132.
    Smith GS. 1992. Toxification and detoxification of plant compounds by ruminants: an overview. J. Range Manag. 45:12530
    [Google Scholar]
  133. 133.
    Sorensen JS, McLister JD, Dearing MD. 2005. Novel plant secondary metabolites impact dietary specialists more than generalists (Neotoma spp.). Ecology 86:1140–54
    [Google Scholar]
  134. 134.
    Spanogiannopoulos P, Bess EN, Carmody RN, Turnbaugh PJ. 2016. The microbial pharmacists within us: a metagenomic view of xenobiotic metabolism. Nat. Rev. Microbiol. 14:5273–87
    [Google Scholar]
  135. 135.
    Spribille T, Tuovinen V, Resl P, Vanderpool D, Wolinski H et al. 2016. Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353:6298488–92
    [Google Scholar]
  136. 136.
    Stevens CE, Hume ID. 1998. Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol. Rev. 78:2393–427
    [Google Scholar]
  137. 137.
    Stevens CE, Hume ID. 2004. Comparative Physiology of the Vertebrate Digestive System Cambridge, UK: Cambridge Univ. Press
  138. 138.
    Stewart C-B, Schilling JW, Wilson AC. 1987. Adaptive evolution in the stomach lysozymes of foregut fermenters. Nature 330:6146401–4
    [Google Scholar]
  139. 139.
    Sundset MA, Barboza PS, Green TK, Folkow LP, Blix AS, Mathiesen SD. 2010. Microbial degradation of usnic acid in the reindeer rumen. Naturwissenschaften 97:3273–78
    [Google Scholar]
  140. 140.
    Sundset MA, Kohn A, Mathiesen SD, Præsteng KE. 2008. Eubacterium rangiferina, a novel usnic acid-resistant bacterium from the reindeer rumen. Naturwissenschaften 95:8741–49
    [Google Scholar]
  141. 141.
    Sundset MA, Salgado-Flores A, Wright A-DG, Pope PB. 2013. The reindeer rumen microbiome. Encyclopedia of Metagenomics KE Nelson 1–12 New York: Springer
    [Google Scholar]
  142. 142.
    Tan ETT, Al Jassim R, D'Arcy BR, Fletcher MT 2017. In vitro biodegradation of hepatotoxic indospicine in Indigofera spicata and its degradation derivatives by camel foregut and cattle rumen fluids. J. Agric. Food Chem. 65:347528–34
    [Google Scholar]
  143. 143.
    Theriot CM, Koenigsknecht MJ, Carlson PE, Hatton GE, Nelson AM et al. 2014. Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Nat. Commun. 5:13114
    [Google Scholar]
  144. 144.
    Ujvari B, Casewell NR, Sunagar K, Arbuckle K, Wüster W et al. 2015. Widespread convergence in toxin resistance by predictable molecular evolution. PNAS 112:3811911–16
    [Google Scholar]
  145. 145.
    Van Soest PJ. 1994. Nutritional Ecology of the Ruminant Ithaca, NY: Comstock
  146. 146.
    Węgrzyn MH, Wietrzyk-Pełka P, Galanty A, Cykowska-Marzencka B, Sundset MA. 2019. Incomplete degradation of lichen usnic acid and atranorin in Svalbard reindeer (Rangifer tarandus platyrhynchus). Polar Res 38: https://doi.org/10.33265/polar.v38.3375
    [Crossref] [Google Scholar]
  147. 147.
    Weinstein SB, Malanga KN, Agwanda B, Maldonado JE, Dearing MD. 2020. The secret social lives of African crested rats, Lophiomys imhausi. J. Mammal. 101:61680–91
    [Google Scholar]
  148. 148.
    Weinstein SB, Martínez-Mota R, Stapleton TE, Klure DM, Greenhalgh R et al. 2021. Microbiome stability and structure is governed by host phylogeny over diet and geography in woodrats (Neotoma spp.). PNAS 118:47e2108787118
    [Google Scholar]
  149. 149.
    Wink M. 2008. Plant secondary metabolism: diversity, function and its evolution. Nat. Prod. Commun. 3:81934578X0800300
    [Google Scholar]
  150. 150.
    Wood R. 2016. Acute animal and human poisonings from cyanotoxin exposure—a review of the literature. Environ. Int. 91:276–82
    [Google Scholar]
  151. 151.
    Youngblut ND, Reischer GH, Walters W, Schuster N, Walzer C et al. 2019. Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nat. Commun. 10:12200
    [Google Scholar]
  152. 152.
    Zhu L, Yang Z, Yao R, Xu L, Chen H et al. 2018. Potential mechanism of detoxification of cyanide compounds by gut microbiomes of bamboo-eating pandas. mSphere 3:3e00229–18
    [Google Scholar]
/content/journals/10.1146/annurev-micro-111121-085333
Loading
/content/journals/10.1146/annurev-micro-111121-085333
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error