1932

Abstract

Host-associated microbiomes contribute in many ways to the homeostasis of the metaorganism. The microbiome's contributions range from helping to provide nutrition and aiding growth, development, and behavior to protecting against pathogens and toxic compounds. Here we summarize the current knowledge of the diversity and importance of the microbiome to animals, using representative examples of wild and domesticated species. We demonstrate how the beneficial ecological roles of animal-associated microbiomes can be generally grouped into well-defined main categories and how microbe-based alternative treatments can be applied to mitigate problems for both economic and conservation purposes and to provide crucial knowledge about host–microbiota symbiotic interactions. We suggest a Customized Combination of Microbial-Based Therapies to promote animal health and contribute to the practice of sustainable husbandry. We also discuss the ecological connections and threats associated with animal biodiversity loss, microorganism extinction, and emerging diseases, such as the COVID-19 pandemic.

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2021-02-15
2024-10-04
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Literature Cited

  1. 1. 
    Qu A, Brulc JM, Wilson MK, Law BF, Theoret JR et al. 2008. Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome. PLOS ONE 3:8e2945
    [Google Scholar]
  2. 2. 
    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]
  3. 3. 
    Tamburini S, Shen N, Wu HC, Clemente JC 2016. The microbiome in early life: implications for health outcomes. Nat. Med. 22:7713–22
    [Google Scholar]
  4. 4. 
    Lewis Z, Lizé A. 2015. Insect behaviour and the microbiome. Curr. Opin. Insect Sci. 9:86–90
    [Google Scholar]
  5. 5. 
    Zhu L, Wu Q, Dai J, Zhang S, Wei F 2011. Evidence of cellulose metabolism by the giant panda gut microbiome. PNAS 108:4317714–19
    [Google Scholar]
  6. 6. 
    Malacrinò A. 2018. Meta-omics tools in the world of insect-microorganism interactions. Biology 7:450
    [Google Scholar]
  7. 7. 
    Pope PB, Denman SE, Jones M, Tringe SG, Barry K et al. 2010. Adaptation to herbivory by the Tammar wallaby includes bacterial and glycoside hydrolase profiles different from other herbivores. PNAS 107:3314793–98
    [Google Scholar]
  8. 8. 
    Shiffman ME, Soo RM, Dennis PG, Morrison M, Tyson GW, Hugenholtz P 2017. Gene and genome-centric analyses of koala and wombat fecal microbiomes point to metabolic specialization for digestion. PeerJ 5:e4075
    [Google Scholar]
  9. 9. 
    Ezenwa VO, Gerardo NM, Inouye DW, Medina M, Xavier JB 2012. Animal behavior and the microbiome. Science 338:6104198–99
    [Google Scholar]
  10. 10. 
    Bosch TCG, McFall-Ngai MJ. 2011. Metaorganisms as the new frontier. Zoology 114:4185–90
    [Google Scholar]
  11. 11. 
    Woodhams DC, Bletz MC, Becker CG, Bender HA, Buitrago-Rosas D et al. 2020. Publisher correction: Host-associated microbiomes are predicted by immune system complexity and climate. Genome Biol 21:40
    [Google Scholar]
  12. 12. 
    Bang C, Dagan T, Deines P, Dubilier N, Duschl WJ et al. 2018. Metaorganisms in extreme environments: Do microbes play a role in organismal adaptation. Zoology 127:1–19
    [Google Scholar]
  13. 13. 
    Vega Thurber R, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA et al. 2009. Metagenomic analysis of stressed coral holobionts. Environ. Microbiol. 11:82148–63
    [Google Scholar]
  14. 14. 
    Vega Thurber RL, Barott KL, Hall D, Liu H, Rodriguez-Mueller B et al. 2008. Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa. PNAS 105:4718413–18
    [Google Scholar]
  15. 15. 
    Bourne D, Iida Y, Uthicke S, Smith-Keune C 2008. Changes in coral-associated microbial communities during a bleaching event. ISME J 2:4350–63
    [Google Scholar]
  16. 16. 
    Vuong HE, Yano JM, Fung TC, Hsiao EY 2017. The microbiome and host behavior. Annu. Rev. Neurosci. 40:21–49
    [Google Scholar]
  17. 17. 
    Moeller AH, Foerster S, Wilson ML, Pusey AE, Hahn BH, Ochman H 2016. Social behavior shapes the chimpanzee pan-microbiome. Sci. Adv. 2:1e1500997
    [Google Scholar]
  18. 18. 
    Boettcher KJ, Ruby EG, McFall-Ngai MJ 1996. Bioluminescence in the symbiotic squid Euprymna scolopes is controlled by a daily biological rhythm. J. Comp. Physiol. A 179:65–73
    [Google Scholar]
  19. 19. 
    Hosokawa T, Kikuchi Y, Shimada M, Fukatsu T 2008. Symbiont acquisition alters behaviour of stinkbug nymphs. Biol. Lett. 4:145–48
    [Google Scholar]
  20. 20. 
    Duarte GAS, Villela HDM, Deocleciano M, Silva D, Barno A et al. 2020. Heat waves are a major threat to turbid coral reefs in Brazil. Front. Mar. Sci. 7:179
    [Google Scholar]
  21. 21. 
    Hughes TP, Kerry JT, Baird AH, Connolly SR, Chase TJ et al. 2019. Global warming impairs stock–recruitment dynamics of corals. Nature 568:7752387–90
    [Google Scholar]
  22. 22. 
    North AC, Hodgson DJ, Price SJ, Griffiths AGF 2015. Anthropogenic and ecological drivers of amphibian disease (ranavirosis). PLOS ONE 10:6e0127037
    [Google Scholar]
  23. 23. 
    Sánchez-Bayo F, Wyckhuys KAG. 2019. Worldwide decline of the entomofauna: a review of its drivers. Biol. Conserv. 232:8–27
    [Google Scholar]
  24. 24. 
    O'Shea TJ, Cryan PM, Hayman DTS, Plowright RK, Streicker DG 2016. Multiple mortality events in bats: a global review. Mammal. Rev. 46:3175–90
    [Google Scholar]
  25. 25. 
    Watkinson AR, Gill JA, Hulme M 2004. Flying in the face of climate change: a review of climate change, past, present and future. Ibis 146:Suppl. 14–10
    [Google Scholar]
  26. 26. 
    Peixoto RS, Rosado PM, Leite DCA, Rosado AS, Bourne DG 2017. Beneficial Microorganisms for Corals (BMC): proposed mechanisms for coral health and resilience. Front. Microbiol. 8:341
    [Google Scholar]
  27. 27. 
    Wilkins LGE, Leray M, O'Dea A, Yuen B, Peixoto RS et al. 2019. Host-associated microbiomes drive structure and function of marine ecosystems. PLOS Biol 17:11e3000533
    [Google Scholar]
  28. 28. 
    Egan S, Gardiner M. 2016. Microbial dysbiosis: rethinking disease in marine ecosystems. Front. Microbiol. 7:991
    [Google Scholar]
  29. 29. 
    Jiménez RR, Sommer S. 2017. The amphibian microbiome: natural range of variation, pathogenic dysbiosis, and role in conservation. Biodivers. Conserv. 26:4763–86
    [Google Scholar]
  30. 30. 
    Sweet MJ, Bulling MT. 2017. On the importance of the microbiome and pathobiome in coral health and disease. Front. Mar. Sci. 4:2261
    [Google Scholar]
  31. 31. 
    Huws SA, Creevey CJ, Oyama LB, Mizrahi I, Denman SE et al. 2018. Addressing global ruminant agricultural challenges through understanding the rumen microbiome: past, present, and future. Front. Microbiol. 9:2161
    [Google Scholar]
  32. 32. 
    MacHugh DE, Bradley DG. 2001. Livestock genetic origins: Goats buck the trend. PNAS 98:105382–84
    [Google Scholar]
  33. 33. 
    Lewis IM, Samatar SS. 1999 (1961). A Pastoral Democracy: A Study of Pastoralism and Politics Among the Northern Somali of the Horn of Africa Classics Afr. Anthropol. Münster, Ger. LIT Verlag:
    [Google Scholar]
  34. 34. 
    Sun H-Z, Zhou M, Wang O, Chen Y, Liu J-X, Guan LL 2020. Multi-omics reveals functional genomic and metabolic mechanisms of milk production and quality in dairy cows. Bioinformatics 36:82530–37
    [Google Scholar]
  35. 35. 
    de Freitas AS, de David DB, Takagaki BM, Roesch LFW 2020. Microbial patterns in rumen are associated with gain of weight in beef cattle. Antonie Van Leeuwenhoek 113:91299–312
    [Google Scholar]
  36. 36. 
    Alipour MJ, Jalanka J, Pessa-Morikawa T, Kokkonen T, Satokari R et al. 2018. The composition of the perinatal intestinal microbiota in cattle. Sci. Rep. 8:110437
    [Google Scholar]
  37. 37. 
    Han X, Yang Y, Yan H, Wang X, Qu L, Chen Y 2015. Rumen bacterial diversity of 80 to 110-day-old goats using 16S rRNA sequencing. PLOS ONE 10:2e0117811
    [Google Scholar]
  38. 38. 
    Wang L, Xu Q, Kong F, Yang Y, Wu D et al. 2016. Exploring the goat rumen microbiome from seven days to two years. PLOS ONE 11:5e0154354
    [Google Scholar]
  39. 39. 
    Koch RM, Swiger LA, Chambers D, Gregory KE 1963. Efficiency of feed use in beef cattle. J. Anim. Sci. 22:2486–94
    [Google Scholar]
  40. 40. 
    Li F, Guan LL. 2017. Metatranscriptomic profiling reveals linkages between the active rumen microbiome and feed efficiency in beef cattle. Appl. Environ. Microbiol. 83:9e00061–17
    [Google Scholar]
  41. 41. 
    Lima J, Auffret MD, Stewart RD, Dewhurst RJ, Duthie C-A et al. 2019. Identification of rumen microbial genes involved in pathways linked to appetite, growth, and feed conversion efficiency in cattle. Front. Genet. 10:701
    [Google Scholar]
  42. 42. 
    Patil RD, Ellison MJ, Wolff SM, Shearer C, Wright AM et al. 2018. Poor feed efficiency in sheep is associated with several structural abnormalities in the community metabolic network of their ruminal microbes. J. Anim. Sci. 96:62113–24
    [Google Scholar]
  43. 43. 
    Metzler-Zebeli BU, Lawlor PG, Magowan E, Zebeli Q 2018. Interactions between metabolically active bacteria and host gene expression at the cecal mucosa in pigs of diverging feed efficiency. J. Anim. Sci. 96:62249–64
    [Google Scholar]
  44. 44. 
    Attwood GT, Wakelin SA, Leahy SC, Rowe S, Clarke S et al. 2019. Applications of the soil, plant and rumen microbiomes in pastoral agriculture. Front Nutr 6:107
    [Google Scholar]
  45. 45. 
    Wallace RJ, Snelling TJ, McCartney CA, Tapio I, Strozzi F 2017. Application of meta-omics techniques to understand greenhouse gas emissions originating from ruminal metabolism. Genet. Sel. Evol. 49:9
    [Google Scholar]
  46. 46. 
    Seshadri R, Leahy SC, Attwood GT, Teh KH, Lambie SC et al. 2018. Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection. Nat. Biotechnol. 36:4359–67
    [Google Scholar]
  47. 47. 
    Wallace RJ, Sasson G, Garnsworthy PC, Tapio I, Gregson E et al. 2019. A heritable subset of the core rumen microbiome dictates dairy cow productivity and emissions. Sci. Adv. 5:7eaav8391
    [Google Scholar]
  48. 48. 
    Andersen TO, Kunath BJ, Hagen LH, Arntzen , Pope PB 2020. Rumen metaproteomics: closer to linking rumen microbial function to animal productivity traits. Methods In press
    [Google Scholar]
  49. 49. 
    Denman SE, Morgavi DP, McSweeney CS 2018. Review: the application of omics to rumen microbiota function. Animal 12:Suppl. 2s233–45
    [Google Scholar]
  50. 50. 
    Wang X, Tsai T, Deng F, Wei X, Chai J et al. 2019. Longitudinal investigation of the swine gut microbiome from birth to market reveals stage and growth performance associated bacteria. Microbiome 7:109
    [Google Scholar]
  51. 51. 
    Xiao L, Estellé J, Kiilerich P, Ramayo-Caldas Y, Xia Z et al. 2016. A reference gene catalogue of the pig gut microbiome. Nat. Microbiol. 1:16161
    [Google Scholar]
  52. 52. 
    Maltecca C, Bergamaschi M, Tiezzi F 2020. The interaction between microbiome and pig efficiency: a review. J. Anim. Breed. Genet. 137:14–13
    [Google Scholar]
  53. 53. 
    Quan J, Wu Z, Ye Y, Peng L, Wu J et al. 2020. Metagenomic characterization of intestinal regions in pigs with contrasting feed efficiency. Front. Microbiol. 11:32
    [Google Scholar]
  54. 54. 
    Wang W, Hu H, Zijlstra RT, Zheng J, Gänzle MG 2019. Metagenomic reconstructions of gut microbial metabolism in weanling pigs. Microbiome 7:48
    [Google Scholar]
  55. 55. 
    Guevarra RB, Lee JH, Lee SH, Seok M-J, Kim DW et al. 2019. Piglet gut microbial shifts early in life: causes and effects. J. Anim. Sci. Biotechnol. 10:1
    [Google Scholar]
  56. 56. 
    Joyce A, McCarthy CGP, Murphy S, Walsh F 2019. Antibiotic resistomes of healthy pig faecal metagenomes. Microb. Genom. 5:5e000272
    [Google Scholar]
  57. 57. 
    Wang C, Li P, Yan Q, Chen L, Li T et al. 2019. Characterization of the pig gut microbiome and antibiotic resistome in industrialized feedlots in China. mSystems 4:e00206–19
    [Google Scholar]
  58. 58. 
    Xiao Y, Xiang Y, Zhou W, Chen J, Li K, Yang H 2017. Microbial community mapping in intestinal tract of broiler chicken. Poult. Sci. 96:51387–93
    [Google Scholar]
  59. 59. 
    Wei S, Morrison M, Yu Z 2013. Bacterial census of poultry intestinal microbiome. Poult. Sci. 92:3671–83
    [Google Scholar]
  60. 60. 
    Clavijo V, Flórez MJV. 2018. The gastrointestinal microbiome and its association with the control of pathogens in broiler chicken production: a review. Poult. Sci. 97:31006–21
    [Google Scholar]
  61. 61. 
    Oakley BB, Lillehoj HS, Kogut MH, Kim WK, Maurer JJ et al. 2014. The chicken gastrointestinal microbiome. FEMS Microbiol. Lett. 360:2100–12
    [Google Scholar]
  62. 62. 
    Wilkinson TJ, Cowan AA, Vallin HE, Onime LA, Oyama LB et al. 2017. Characterization of the microbiome along the gastrointestinal tract of growing turkeys. Front. Microbiol. 8:1089
    [Google Scholar]
  63. 63. 
    Taylor KJM, Ngunjiri JM, Abundo MC, Jang H, Elaish M et al. 2020. Respiratory and gut microbiota in commercial turkey flocks with disparate weight gain trajectories display differential compositional dynamics. Appl. Environ. Microbiol. 86:12e00431–20
    [Google Scholar]
  64. 64. 
    Elokil AA, Abouelezz KFM, Ahmad HI, Pan Y, Li S 2020. Investigation of the impacts of antibiotic exposure on the diversity of the gut microbiota in chicks. Animals 10:5896
    [Google Scholar]
  65. 65. 
    Zilhão J, Angelucci DE, Igreja MA, Arnold LJ, Badal E et al. 2020. Last interglacial Iberian Neandertals as fisher-hunter-gatherers. Science 367:6485eaaz7943
    [Google Scholar]
  66. 66. 
    O'Connor S, Ono R, Clarkson C 2011. Pelagic fishing at 42,000 years before the present and the maritime skills of modern humans. Science 334:60591117–21
    [Google Scholar]
  67. 67. 
    Smith A, McNiven IJ, Rose D, Brown S, Johnston C, Crocker S 2019. Indigenous knowledge and resource management as world heritage values: Budj Bim Cultural Landscape, Australia. Archaeologies 15:2285–313
    [Google Scholar]
  68. 68. 
    Wettenhall G. 2010. The People of Budj Bim: Engineers of Aquaculture, Builders of Stone House Settlements and Warriors Defending Country Mollongghip, Aust.: em Press
    [Google Scholar]
  69. 69. 
    de Bruijn I, Liu Y, Wiegertjes GF, Raaijmakers JM 2018. Exploring fish microbial communities to mitigate emerging diseases in aquaculture. FEMS Microbiol. Ecol. 94:1fix161
    [Google Scholar]
  70. 70. 
    Talwar C, Nagar S, Lal R, Negi RK 2018. Fish gut microbiome: current approaches and future perspectives. Indian J. Microbiol. 58:4397–414
    [Google Scholar]
  71. 71. 
    Baker-Austin C, Oliver JD. 2018. Vibrio vulnificus: new insights into a deadly opportunistic pathogen. Environ. Microbiol. 20:2423–30
    [Google Scholar]
  72. 72. 
    Yeh H, Skubel SA, Patel H, Shi DC, Bushek D, Chikindas ML 2020. From farm to fingers: an exploration of probiotics for oysters, from production to human consumption. Probiotics Antimicrob. Proteins 12:2351–64
    [Google Scholar]
  73. 73. 
    Dubé CE, Ky C-L, Planes S 2019. Microbiome of the black-lipped pearl oyster, a multi-tissue description with functional profiling. Front. Microbiol. 10:1548
    [Google Scholar]
  74. 74. 
    Coelho LP, Kultima JR, Costea PI, Fournier C, Pan Y et al. 2018. Similarity of the dog and human gut microbiomes in gene content and response to diet. Microbiome 6:72
    [Google Scholar]
  75. 75. 
    Swanson KS, Dowd SE, Suchodolski JS, Middelbos IS, Vester BM et al. 2011. Phylogenetic and gene-centric metagenomics of the canine intestinal microbiome reveals similarities with humans and mice. ISME J 5:4639–49
    [Google Scholar]
  76. 76. 
    Wallis C, Marshall M, Colyer A, O'Flynn C, Deusch O, Harris S 2015. A longitudinal assessment of changes in bacterial community composition associated with the development of periodontal disease in dogs. Vet. Microbiol. 181:3–4271–82
    [Google Scholar]
  77. 77. 
    Ruparell A, Inui T, Staunton R, Wallis C, Deusch O, Holcombe LJ 2020. The canine oral microbiome: variation in bacterial populations across different niches. BMC Microbiol 20:42
    [Google Scholar]
  78. 78. 
    Tun HM, Brar MS, Khin N, Jun L, Hui RK-H et al. 2012. Gene-centric metagenomics analysis of feline intestinal microbiome using 454 junior pyrosequencing. J. Microbiol. Methods 88:3369–76
    [Google Scholar]
  79. 79. 
    Lyu Y, Su C, Verbrugghe A, Van de Wiele T, Martos Martinez-Caja A, Hesta M 2020. Past, present, and future of gastrointestinal microbiota research in cats. Front. Microbiol. 11:1661
    [Google Scholar]
  80. 80. 
    Equine Stud. 2019. Breaking down the $122 billion economic impact of the United States equine industry. Post University Blog Sept. 27. https://post.edu/blog/breaking-down-the-122-billion-economic-impact-of-the-united-states-equine-industry-2/
    [Google Scholar]
  81. 81. 
    Husso A, Jalanka J, Alipour MJ, Huhti P, Kareskoski M et al. 2020. The composition of the perinatal intestinal microbiota in horse. Sci. Rep. 10:441
    [Google Scholar]
  82. 82. 
    Jiménez E, Marín ML, Martín R, Odriozola JM, Olivares M et al. 2008. Is meconium from healthy newborns actually sterile. Res. Microbiol. 159:3187–93
    [Google Scholar]
  83. 83. 
    Collado MC, Rautava S, Aakko J, Isolauri E, Salminen S 2016. Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Sci. Rep. 6:23129
    [Google Scholar]
  84. 84. 
    Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J 2014. The placenta harbors a unique microbiome. Sci. Transl. Med. 6:237ra65
    [Google Scholar]
  85. 85. 
    Gao H, Chi X, Qin W, Wang L, Song P et al. 2019. Comparison of the gut microbiota composition between the wild and captive Tibetan wild ass (Equus kiang). J. Appl. Microbiol. 126:61869–78
    [Google Scholar]
  86. 86. 
    Williams CL, Caraballo-Rodríguez AM, Allaband C, Zarrinpar A, Knight R, Gauglitz JM 2018. Wildlife-microbiome interactions and disease: exploring opportunities for disease mitigation across ecological scales. Drug Discov. Today 28:105–15
    [Google Scholar]
  87. 87. 
    Trevelline BK, Fontaine SS, Hartup BK, Kohl KD 2019. Conservation biology needs a microbial renaissance: a call for the consideration of host-associated microbiota in wildlife management practices. Proc. Biol. Sci. 286:189520182448
    [Google Scholar]
  88. 88. 
    Fisher MC, Garner TWJ. 2020. Chytrid fungi and global amphibian declines. Nat. Rev. Microbiol. 18:6332–43
    [Google Scholar]
  89. 89. 
    Schmeller DS, Courchamp F, Killeen G 2020. Biodiversity loss, emerging pathogens and human health risks. Biodivers. Conserv. 29:3095–102
    [Google Scholar]
  90. 90. 
    Cardinale BJ, Emmett Duffy J, Gonzalez A, Hooper DU, Perrings C et al. 2012. Correction: corrigendum: biodiversity loss and its impact on humanity. Nature 489:326
    [Google Scholar]
  91. 91. 
    Woolhouse MEJ. 2002. Population biology of emerging and re-emerging pathogens. Trends Microbiol 10:10S3–7
    [Google Scholar]
  92. 92. 
    Delwart E. 2012. Animal virus discovery: improving animal health, understanding zoonoses, and opportunities for vaccine development. Curr. Opin. Virol. 2:3344–52
    [Google Scholar]
  93. 93. 
    Hasle G. 2013. Transport of ixodid ticks and tick-borne pathogens by migratory birds. Front. Cell. Infect. Microbiol. 3:48
    [Google Scholar]
  94. 94. 
    Di Marco M, Baker ML, Daszak P, De Barro P, Eskew EA et al. 2020. Opinion: Sustainable development must account for pandemic risk. PNAS 117:83888–92
    [Google Scholar]
  95. 95. 
    Grogan LF, Berger L, Rose K, Grillo V, Cashins SD, Skerratt LF 2014. Surveillance for emerging biodiversity diseases of wildlife. PLOS Pathog 10:5e1004015
    [Google Scholar]
  96. 96. 
    Lutz HL, Jackson EW, Webala PW, Babyesiza WS, Kerbis Peterhans JC et al. 2019. Ecology and host identity outweigh evolutionary history in shaping the bat microbiome. mSystems 4:6e00511–19
    [Google Scholar]
  97. 97. 
    Song SJ, Sanders JG, Delsuc F, Metcalf J, Amato K et al. 2020. Comparative analyses of vertebrate gut microbiomes reveal convergence between birds and bats. mBio 11:1e02901–19
    [Google Scholar]
  98. 98. 
    Roberts CM, McClean CJ, Veron JEN, Hawkins JP, Allen GR et al. 2002. Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295:55581280–84
    [Google Scholar]
  99. 99. 
    Sebens KP. 1994. Biodiversity of coral reefs: What are we losing and why?. Am. Zool. 34:1115–33
    [Google Scholar]
  100. 100. 
    Reaka-Kudla ML. 2001. Crustaceans. Encyclopedia of Biodiversity SA Levin 915–43 Cambridge, MA: Academic
    [Google Scholar]
  101. 101. 
    O'Neil JM, Capone DG. 2008. Nitrogen cycling in coral reef environments. Nitrogen in the Marine Environment DG Capone, DA Bronk, MR Mulholland, EJ Carpenter 949–89 Cambridge, MA: Academic 2nd ed.
    [Google Scholar]
  102. 102. 
    Hatcher PE. 1990. Seasonal and age-related variation in the needle quality of five conifer species. Oecologia 85:2200–12
    [Google Scholar]
  103. 103. 
    Raina J-B, Tapiolas D, Willis BL, Bourne DG 2009. Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl. Environ. Microbiol. 75:113492–501
    [Google Scholar]
  104. 104. 
    Moberg F, Folke C. 1999. Ecological goods and services of coral reef ecosystems. Ecol. Econ. 29:2215–33
    [Google Scholar]
  105. 105. 
    Haas AF, Fairoz MFM, Kelly LW, Nelson CE, Dinsdale EA et al. 2016. Global microbialization of coral reefs. Nat. Microbiol. 1:616042
    [Google Scholar]
  106. 106. 
    Santos HF, Carmo FL, Duarte G, Dini-Andreote F, Castro CB et al. 2014. Climate change affects key nitrogen-fixing bacterial populations on coral reefs. ISME J 8:112272–79
    [Google Scholar]
  107. 107. 
    Ainsworth TD, Krause L, Bridge T, Torda G, Raina J-B et al. 2015. The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J 9:2261–74
    [Google Scholar]
  108. 108. 
    Santos HF, Duarte GAS, da Costa Rachid CTC, Chaloub RM, Calderon EN et al. 2015. Impact of oil spills on coral reefs can be reduced by bioremediation using probiotic microbiota. Sci. Rep. 5:18268
    [Google Scholar]
  109. 109. 
    Glasl B, Webster NS, Bourne DG 2017. Microbial indicators as a diagnostic tool for assessing water quality and climate stress in coral reef ecosystems. Mar. Biol. 164:91
    [Google Scholar]
  110. 110. 
    Ahmed HI, Herrera M, Liew YJ, Aranda M 2019. Long-term temperature stress in the coral model Aiptasia supports the “Anna Karenina principle” for bacterial microbiomes. Front. Microbiol. 10:1709975
    [Google Scholar]
  111. 111. 
    van Oppen MJH, Blackall LL 2019. Coral microbiome dynamics, functions and design in a changing world. Nat. Rev. Microbiol. 17:9557–67
    [Google Scholar]
  112. 112. 
    Whale Dolphin Conserv 2018. Whale and dolphin species guide Guide, Whale Dolphin Conserv. Plymouth, MA: https://us.whales.org/whales-dolphins/species-guide/
    [Google Scholar]
  113. 113. 
    Van Bonn WG. 2014. Fowler's Zoo and Wild Animal Medicine 8 St. Louis, MO: Elsevier Suanders eBook ed.
    [Google Scholar]
  114. 114. 
    Bik EM, Costello EK, Switzer AD, Callahan BJ, Holmes SP et al. 2016. Marine mammals harbor unique microbiotas shaped by and yet distinct from the sea. Nat. Commun. 7:10516
    [Google Scholar]
  115. 115. 
    Loudon AH, Kurtz A, Esposito E, Umile TP, Minbiole KPC et al. 2020. Columbia spotted frogs (Rana luteiventris) have characteristic skin microbiota that may be shaped by cutaneous skin peptides and the environment. FEMS Microbiol. Ecol. 96:10fiaa168
    [Google Scholar]
  116. 116. 
    Kruger A. 2020. Frog skin microbiota vary with host species and environment but not chytrid infection. Front. Microbiol. 11:1330
    [Google Scholar]
  117. 117. 
    Jiménez RR, Alvarado G, Estrella J, Sommer S 2019. Moving beyond the host: unraveling the skin microbiome of endangered Costa Rican amphibians. Front. Microbiol. 10:2060
    [Google Scholar]
  118. 118. 
    Douglas AJ, Hug LA, Katzenback BA 2020. Composition of the North American wood frog (Rana sylvatica) bacterial skin microbiome and seasonal variation in community structure. Microb. Ecol. http://dx.doi.org/10.1007/s00248-020-01550-5
    [Crossref] [Google Scholar]
  119. 119. 
    Walke JB, Belden LK. 2016. Harnessing the microbiome to prevent fungal infections: lessons from amphibians. PLOS Pathog 12:9e1005796
    [Google Scholar]
  120. 120. 
    Amato KR, Yeoman CJ, Cerda G, Schmitt CA, Cramer JD et al. 2015. Variable responses of human and non-human primate gut microbiomes to a Western diet. Microbiome 3:53
    [Google Scholar]
  121. 121. 
    Grieneisen L, Muehlbauer AL, Blekhman R 2020. Microbial control of host gene regulation and the evolution of host-microbiome interactions in primates. Philos. Trans. R. Soc. Lond. B 375:180820190598
    [Google Scholar]
  122. 122. 
    Hicks AL, Lee KJ, Couto-Rodriguez M, Patel J, Sinha R et al. 2018. Gut microbiomes of wild great apes fluctuate seasonally in response to diet. Nat. Commun. 9:1786
    [Google Scholar]
  123. 123. 
    Ren T, Grieneisen LE, Alberts SC, Archie EA, Wu M 2016. Development, diet and dynamism: longitudinal and cross-sectional predictors of gut microbial communities in wild baboons. Environ. Microbiol. 18:51312–25
    [Google Scholar]
  124. 124. 
    Moeller AH, Peeters M, Ndjango J-B, Li Y, Hahn BH, Ochman H 2013. Sympatric chimpanzees and gorillas harbor convergent gut microbial communities. Genome Res 23:101715–20
    [Google Scholar]
  125. 125. 
    Ochman H, Worobey M, Kuo C-H, Ndjango J-BN, Peeters M et al. 2010. Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLOS Biol 8:11e1000546
    [Google Scholar]
  126. 126. 
    Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E 2006. The coral probiotic hypothesis. Environ. Microbiol. 8:122068–73
    [Google Scholar]
  127. 127. 
    Teplitski M, Ritchie K. 2009. How feasible is the biological control of coral diseases?. Trends Ecol. Evol. 24:7378–85
    [Google Scholar]
  128. 128. 
    Voolstra CR, Ziegler M. 2020. Adapting with microbial help: Microbiome flexibility facilitates rapid responses to environmental change. Bioessays 42:7e2000004
    [Google Scholar]
  129. 129. 
    Brodnicke OB, Bourne DG, Heron SF, Pears RJ, Stella JS et al. 2019. Unravelling the links between heat stress, bleaching and disease: fate of tabular corals following a combined disease and bleaching event. Coral Reefs 38:4591–603
    [Google Scholar]
  130. 130. 
    Nielsen DA, Petrou K, Gates RD 2018. Coral bleaching from a single cell perspective. ISME J 12:61558–67
    [Google Scholar]
  131. 131. 
    Hughes TP, Kerry JT, Baird AH, Connolly SR, Dietzel A et al. 2018. Global warming transforms coral reef assemblages. Nature 556:7702492–96
    [Google Scholar]
  132. 132. 
    Ben-Haim Y, Zicherman-Keren M, Rosenberg E 2003. Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl. Environ. Microbiol 69:74236–42
    [Google Scholar]
  133. 133. 
    Rosales SM, Clark AS, Huebner LK, Ruzicka RR, Muller EM 2020. Rhodobacterales and Rhizobiales are associated with stony coral tissue loss disease and its suspected sources of transmission. Front. Microbiol. 11:681
    [Google Scholar]
  134. 134. 
    Aeby GS, Ushijima B, Campbell JE, Jones S, Williams GJ et al. 2019. Pathogenesis of a tissue loss disease affecting multiple species of corals along the Florida Reef Tract. Front. Mar. Sci. 6:189
    [Google Scholar]
  135. 135. 
    Skerratt LF, Berger L, Speare R, Cashins S, McDonald KR et al. 2007. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4:125
    [Google Scholar]
  136. 136. 
    Schmidt BR, Bozzuto C, Lötters S, Steinfartz S 2017. Dynamics of host populations affected by the emerging fungal pathogen. R. Soc. Open Sci. 4:3160801
    [Google Scholar]
  137. 137. 
    Franklinos LHV, Lorch JM, Bohuski E, Rodriguez-Ramos Fernandez J, Wright ON et al. 2017. Emerging fungal pathogen Ophidiomyces ophiodiicola in wild European snakes. Sci. Rep. 7:3844
    [Google Scholar]
  138. 138. 
    Drees KP, Lorch JM, Puechmaille SJ, Parise KL, Wibbelt G et al. 2017. Phylogenetics of a fungal invasion: origins and widespread dispersal of white-nose syndrome. mBio 8:6e01941–17
    [Google Scholar]
  139. 139. 
    Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM et al. 2009. Bat white-nose syndrome: An emerging fungal pathogen. Science 323:5911227
    [Google Scholar]
  140. 140. 
    Frick WF, Puechmaille SJ, Hoyt JR, Nickel BA, Langwig KE et al. 2015. Disease alters macroecological patterns of North American bats. Glob. Ecol. Biogeogr. 24:7741–49
    [Google Scholar]
  141. 141. 
    McKenzie VJ, Song SJ, Delsuc F, Prest TL, Oliverio AM et al. 2017. The effects of captivity on the mammalian gut microbiome. Integr. Comp. Biol. 57:4690–704
    [Google Scholar]
  142. 142. 
    Dennis P, Ellis S, Mellen J, Lee P, Olea-Popelka F et al. 2012. IOD in rhinos—epidemiology group report: report from the Epidemiology Working Group of the International Workshop on Iron Overload Disorder in Browsing Rhinoceros (February 2011). J. Zoo Wildl. Med. 43:Suppl.v3S114–16
    [Google Scholar]
  143. 143. 
    Roth TL, Switzer A, Watanabe-Chailland M, Bik EM, Relman DA et al. 2019. Reduced gut microbiome diversity and metabolome differences in rhinoceros species at risk for iron overload disorder. Front. Microbiol. 10:2291
    [Google Scholar]
  144. 144. 
    Leite DCA, Leão P, Garrido AG, Lins U, Santos HF et al. 2017. Broadcast spawning coral can vertically transfer its associated bacterial core. Front. Microbiol. 8:176
    [Google Scholar]
  145. 145. 
    Zheng H, Steele MI, Leonard SP, Motta EVS, Moran NA 2018. Honey bees as models for gut microbiota research. Lab. Anim. 47:11317–25
    [Google Scholar]
  146. 146. 
    Rosado PM, Leite DCA, Duarte GAS, Chaloub RM, Jospin G et al. 2019. Marine probiotics: increasing coral resistance to bleaching through microbiome manipulation. ISME J 13:4921–36
    [Google Scholar]
  147. 147. 
    Hoyt JR, Langwig KE, White JP, Kaarakka HM, Redell JA et al. 2019. Field trial of a probiotic bacteria to protect bats from white-nose syndrome. Sci. Rep. 9:9158
    [Google Scholar]
  148. 148. 
    Mimee M, Citorik RJ, Lu TK 2016. Microbiome therapeutics—advances and challenges. Adv. Drug Deliv. Rev. 105:44–54
    [Google Scholar]
  149. 149. 
    Banerjee G, Ray AK. 2017. The advancement of probiotics research and its application in fish farming industries. Res. Vet. Sci. 115:66–77
    [Google Scholar]
  150. 150. 
    Holden WM, Hanlon SM, Woodhams DC, Chappell TM, Wells HL et al. 2015. Skin bacteria provide early protection for newly metamorphosed southern leopard frogs (Rana sphenocephala) against the frog-killing fungus. Batrachochytrium dendrobatidis. Biol. Conserv. 187:91–102
    [Google Scholar]
  151. 151. 
    Peixoto RS, Sweet M, Bourne DG 2019. Customized medicine for corals. Front. Mar. Sci. 6:686
    [Google Scholar]
  152. 152. 
    Zmora N, Zilberman-Schapira G, Suez J, Mor U, Dori-Bachash M et al. 2018. Personalized gut mucosal colonization resistance to empiric probiotics is associated with unique host and microbiome features. Cell 174:61388–1405.e21
    [Google Scholar]
  153. 153. 
    Kashyap PC, Chia N, Nelson H, Segal E, Elinav E 2017. Microbiome at the frontier of personalized medicine. Mayo Clin. Proc. 92:121855–64
    [Google Scholar]
  154. 154. 
    Gilbert JA, Stephens B. 2018. Microbiology of the built environment. Nat. Rev. Microbiol. 16:11661–70
    [Google Scholar]
  155. 155. 
    Peters RD, Sturz AV, Carter MR, Sanderson JB 2003. Developing disease-suppressive soils through crop rotation and tillage management practices. Soil Tillage Res 72:2181–92
    [Google Scholar]
  156. 156. 
    Hong S, Jv H, Lu M, Wang B, Zhao Y, Ruan Y 2020. Significant decline in banana Fusarium wilt disease is associated with soil microbiome reconstruction under chilli pepper-banana rotation. Eur. J. Soil Biol. 97:103154
    [Google Scholar]
  157. 157. 
    van Elsas JD, Garbeva P, Salles J 2002. Effects of agronomical measures on the microbial diversity of soils as related to the suppression of soil-borne plant pathogens. Biodegradation 13:29–40
    [Google Scholar]
  158. 158. 
    Berg G, Köberl M, Rybakova D, Müller H, Grosch R, Smalla K 2017. Plant microbial diversity is suggested as the key to future biocontrol and health trends. FEMS Microbiol. Ecol. 93:5 https://doi.org/10.1093/femsec/fix050
    [Crossref] [Google Scholar]
  159. 159. 
    Yang Y, Ashworth AJ, DeBruyn JM, Willett C, Durso LM et al. 2019. Soil bacterial biodiversity is driven by long-term pasture management, poultry litter, and cattle manure inputs. PeerJ 7:e7839
    [Google Scholar]
  160. 160. 
    de Faccio Carvalho PC, Anghinoni I, de Moraes A, de Souza ED, Sulc RM et al. 2010. Managing grazing animals to achieve nutrient cycling and soil improvement in no-till integrated systems. Nutr. Cycl. Agroecosyst. 88:2259–73
    [Google Scholar]
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