Diet–microbiome–disease: Investigating diet’s influence on infectious disease resistance through alteration of the gut microbiome

English version

Autoři: Erica V. Harris ^aff001; Jacobus C. de Roode ^aff001; Nicole M. Gerardo ^aff001
Působiště autorů: Department of Biology, O. Wayne Rollins Research Center, Emory University, Atlanta, Georgia, United States of America ^aff001
Vyšlo v časopise: Diet–microbiome–disease: Investigating diet’s influence on infectious disease resistance through alteration of the gut microbiome. PLoS Pathog 15(10): e32767. doi:10.1371/journal.ppat.1007891
Kategorie: Review
doi: https://doi.org/10.1371/journal.ppat.1007891

Souhrn

Abiotic and biotic factors can affect host resistance to parasites. Host diet and host gut microbiomes are two increasingly recognized factors influencing disease resistance. In particular, recent studies demonstrate that (1) particular diets can reduce parasitism; (2) diets can alter the gut microbiome; and (3) the gut microbiome can decrease parasitism. These three separate relationships suggest the existence of indirect links through which diets reduce parasitism through an alteration of the gut microbiome. However, such links are rarely considered and even more rarely experimentally validated. This is surprising because there is increasing discussion of the therapeutic potential of diets and gut microbiomes to control infectious disease. To elucidate these potential indirect links, we review and examine studies on a wide range of animal systems commonly used in diet, microbiome, and disease research. We also examine the relative benefits and disadvantages of particular systems for the study of these indirect links and conclude that mice and insects are currently the best animal systems to test for the effect of diet-altered protective gut microbiomes on infectious disease. Focusing on these systems, we provide experimental guidelines and highlight challenges that must be overcome. Although previous studies have recommended these systems for microbiome research, here we specifically recommend these systems because of their proven relationships between diet and parasitism, between diet and the microbiome, and between the microbiome and parasite resistance. Thus, they provide a sound foundation to explore the three-way interaction between diet, the microbiome, and infectious disease.

Klíčová slova:

Bees – Diet – Infectious diseases – Microbiome – Parasitic diseases – Parasitism – Protozoan infections – Trypanosoma

Zdroje

1. Lambrechts L, Fellous S, Koella JC. Coevolutionary interactions between host and parasite genotypes. Trends Parasitol. 2006;22: 12–6. doi: 10.1016/j.pt.2005.11.008 16310412

2. Lafferty KD, Dobson AP, Kuris AM. Parasites dominate food web links. Proc Natl Acad Sci U S A. 2006;103: 11211–6. doi: 10.1073/pnas.0604755103 16844774

3. Wolinska J, King KC. Environment can alter selection in host-parasite interactions. 2009;25: 236–244. doi: 10.1016/j.pt.2009.02.004 19356982

4. Lazzaro BP, Little TJ. Immunity in a variable world. Philos Trans R Soc B Biol Sci. 2009;364: 15–26. doi: 10.1098/rstb.2008.0141 18926975

5. van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368: 407–15. doi: 10.1056/NEJMoa1205037 23323867

6. Dong Y, Manfredini F, Dimopoulos G. Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog. 2009;5: e1000423. doi: 10.1371/journal.ppat.1000423 19424427

7. Villarino NF, LeCleir GR, Denny JE, Dearth SP, Harding CL, Sloan SS, et al. Composition of the gut microbiota modulates the severity of malaria. Proc Natl Acad Sci. 2016;113: 2235–2240. doi: 10.1073/pnas.1504887113 26858424

8. Linenberg I, Christophides GK, Gendrin M. Larval diet affects mosquito development and permissiveness to Plasmodium infection. Sci Rep. 2016;6: 38230. doi: 10.1038/srep38230 27910908

9. Maes PW, Rodrigues PAP, Oliver R, Mott BM, Anderson KE. Diet-related gut bacterial dysbiosis correlates with impaired development, increased mortality and Nosema disease in the honeybee (Apis mellifera). Mol Ecol. 2016;25: 5439–5450. doi: 10.1111/mec.13862 27717118

10. Sansone CL, Cohen J, Yasunaga A, Xu J, Osborn G, Subramanian H, et al. Microbiota-dependent priming of antiviral intestinal immunity in Drosophila. Cell Host Microbe. 2015;18: 571–581. doi: 10.1016/j.chom.2015.10.010 26567510

11. Emery O, Schmidt K, Engel P. Immune system stimulation by the gut symbiont Frischella perrara in the honey bee (Apis mellifera). Mol Ecol. 2017;26: 2576–2590. doi: 10.1111/mec.14058 28207182

12. Derrien M, Veiga P. Rethinking diet to aid human–microbe symbiosis. Trends Microbiol. 2017;25: 100–112. doi: 10.1016/j.tim.2016.09.011 27916707

13. Huffman MA, Gotoh S, Turner LA, Hamai M, Yoshida K. Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates. 1997;38: 111–125. doi: 10.1007/BF02382002

14. Page JE, Huffman MA, Smith V, Towers GHN. Chemical basis for Aspilia leaf-swallowing by chimpanzees: a reanalysis. J Chem Ecol. 1997;23: 2211–2226. doi: 10.1023/B:JOEC.0000006440.57230.a9

15. Singer MS, Mace KC, Bernays EA. Self-medication as adaptive plasticity: increased ingestion of plant toxins by parasitized caterpillars. PLoS ONE. 2009;4: e4796. doi: 10.1371/journal.pone.0004796 19274098

16. Sternberg ED, Lefèvre T, Li J, de Castillejo CLF, Li H, Hunter MD, et al. Food plant derived disease tolerance and resistance in a natural butterfly-plant-parasite interactions. Evolution. 2012;66: 3367–76. doi: 10.1111/j.1558-5646.2012.01693.x 23106703

17. Tao L, Hoang KM, Hunter MD, de Roode JC. Fitness costs of animal medication: antiparasitic plant chemicals reduce fitness of monarch butterfly hosts. J Anim Ecol. 2016;85: 1246–1254. doi: 10.1111/1365-2656.12558 27286503

18. Gowler CD, Leon KE, Hunter MD, de Roode JC. Secondary defense chemicals in milkweed reduce parasite infection in monarch butterflies, Danaus plexippus. J Chem Ecol. 2015;41: 520–523. doi: 10.1007/s10886-015-0586-6 25953502

19. de Roode JC, Pedersen AB, Hunter MD, Altizer S. Host plant species affects virulence in monarch butterfly parasites. J Anim Ecol. 2008;77: 120–126. doi: 10.1111/j.1365-2656.2007.01305.x 18177332

20. Kelly CA, Bowers MD. Host plant iridoid glycosides mediate herbivore interactions with natural enemies. Oecologia. 2018;188: 491–500. doi: 10.1007/s00442-018-4224-1 30003369

21. Richardson LL, Adler LS, Leonard AS, Andicoechea J, Regan KH, Anthony WE, et al. Secondary metabolites in floral nectar reduce parasite infections in bumblebees. Proc Biol Sci. 2015;282: 20142471-. doi: 10.1098/rspb.2014.2471 25694627

22. Anthony WE, Palmer-Young EC, Leonard AS, Irwin RE, Adler LS. Testing dose-dependent effects of the nectar alkaloid anabasine on trypanosome parasite loads in adult bumble bees. PLoS ONE. 2015;10: e0142496. doi: 10.1371/journal.pone.0142496 26545106

23. Alaux C, Ducloz F, Crauser D, Le Conte Y. Diet effects on honeybee immunocompetence. Biol Lett. 2010;6: 562–565. doi: 10.1098/rsbl.2009.0986 20089536

24. Foley K, Fazio G, Jensen AB, Hughes WOH. Nutritional limitation and resistance to opportunistic Aspergillus parasites in honey bee larvae. J Invertebr Pathol. 2012;111: 68–73. doi: 10.1016/j.jip.2012.06.006 22750047

25. Howick VM, Lazzaro BP. Genotype and diet shape resistance and tolerance across distinct phases of bacterial infection. BMC Evol Biol. 2014;14: 56. doi: 10.1186/1471-2148-14-56 24655914

26. Nagajyothi F, Weiss LM, Zhao D, Koba W, Jelicks LA, Cui M-H, et al. High fat diet modulates Trypanosoma cruzi infection associated myocarditis. PLoS Negl Trop Dis. 2014;8: e3118. doi: 10.1371/journal.pntd.0003118 25275627

27. Shankar AH, Genton B, Semba RD, Baisor M, Paino J, Tamja S, et al. Effect of vitamin A supplementation on morbidity due to Plasmodium falciparum in young children in Papua New Guinea: a randomised trial. Lancet. 1999;354: 203–9. doi: 10.1016/S0140-6736(98)08293-2 10421302

28. Meadows DN, Bahous RH, Best AF, Rozen R. High dietary folate in mice alters immune response and reduces survival after malarial infection. PLoS ONE. 2015;10: e0143738. doi: 10.1371/journal.pone.0143738 26599510

29. Kangassalo K, Valtonen TM, Roff D, Pölkki M, Dubovskiy IM, Sorvari J, et al. Intra- and trans-generational effects of larval diet on susceptibility to an entomopathogenic fungus, Beauveria bassiana, in the greater wax moth, Galleria mellonella. J Evol Biol. 2015;28: 1453–1464. doi: 10.1111/jeb.12666 26052853

30. Waldor MK, Tyson G, Borenstein E, Ochman H, Moeller A, Finlay BB, et al. Where next for microbiome research? PLoS Biol. 2015;13: e1002050. doi: 10.1371/journal.pbio.1002050 25602283

31. Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat Rev Genet. 2012; doi: 10.1038/nrg3182 22411464

32. Moeller AH, Li Y, Mpoudi Ngole E, Ahuka-Mundeke S, Lonsdorf EV, Pusey AE, et al. Rapid changes in the gut microbiome during human evolution. Proc Natl Acad Sci. 2014;111: 16431–16435. doi: 10.1073/pnas.1419136111 25368157

33. Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, Moran N. A simple and distinctive microbiota associated with honey bees and bumble bees. Mol Ecol. 2011;20: 619–628. doi: 10.1111/j.1365-294X.2010.04959.x 21175905

34. Colman DR, Toolson EC, Takacs-Vesbach CD. Do diet and taxonomy influence insect gut bacterial communities? Mol Ecol. 2012;21: 5124–5137. doi: 10.1111/j.1365-294X.2012.05752.x 22978555

35. Warnecke F, Luginbühl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT, et al. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature. 2007;450: 560–5. doi: 10.1038/nature06269 18033299

36. Mikaelyan A, Dietrich C, Köhler T, Poulsen M, Sillam-Dussès D, Brune A. Diet is the primary determinant of bacterial community structure in the guts of higher termites. Mol Ecol. 2015;24: 5284–95. doi: 10.1111/mec.13376 26348261

37. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen Y-Y, Keilbaugh SA, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334: 105–8. doi: 10.1126/science.1208344 21885731

38. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505: 559–63. doi: 10.1038/nature12820 24336217

39. Tarayre C, Bauwens J, Mattéotti C, Brasseur C, Millet C, Massart S, et al. Multiple analyses of microbial communities applied to the gut of the wood-feeding termite Reticulitermes flavipes fed on artificial diets. Symbiosis. 2015;65: 143–155. doi: 10.1007/s13199-015-0328-0

40. David LA, Materna AC, Friedman J, Campos-Baptista MI, Blackburn MC, Perrotta A, et al. Host lifestyle affects human microbiota on daily timescales. Genome Biol. 2014;15: R89. doi: 10.1186/gb-2014-15-7-r89 25146375

41. Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H, Goodman AL, et al. The long-term stability of the human gut microbiota. Science. 2013;341: 1237439. doi: 10.1126/science.1237439 23828941

42. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, et al. Enterotypes of the human gut microbiome. Nature. 2011;473: 174–80. doi: 10.1038/nature09944 21508958

43. Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S, et al. Gut microbiota composition correlates with diet and health in the elderly. 2012; doi: 10.1038/nature11319 22797518

44. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med. 2009;1: 6ra14. doi: 10.1126/scitranslmed.3000322 20368178

45. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2010;107: 14691–14696. doi: 10.1073/pnas.1005963107 20679230

46. Miyake S, Ngugi DK, Stingl U. Diet strongly influences the gut microbiota of surgeonfishes. Mol Ecol. 2014; doi: 10.1111/mec.13050 25533191

47. Pinto-Tomás A, Sittenfeld A, Uribe-Lorío L, Chavarría F, Mora M, Janzen DH, et al. Comparison of midgut bacterial diversity in tropical caterpillars (Lepidoptera: Saturniidae) fed on different diets. Environ Entomol. 2011;40: 1111–1122. doi: 10.1603/EN11083 22251723

48. Kišidayová S, Váradyová Z, Pristaš P, Piknová M, Nigutová K, Petrželková KJ, et al. Effects of high- and low-fiber diets on fecal fermentation and fecal microbial populations of captive chimpanzees. Am J Primatol. 2009;71: 548–557. doi: 10.1002/ajp.20687 19367605

49. Wang Y, Gilbreath TM, Kukutla P, Yan G, Xu J. Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya. PLoS ONE. 2011;6: e24767. doi: 10.1371/journal.pone.0024767 21957459

50. Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr. 1995;125: 1401–1412. doi: 10.1093/jn/125.6.1401 7782892

51. Roberfroid M, Gibson GR, Hoyles L, McCartney AL, Rastall R, Rowland I, et al. Prebiotic effects: metabolic and health benefits. Br J Nutr. 2010;104: S1–S63. doi: 10.1017/S0007114510003363 20920376

52. Gibson GR. Dietary modulation of the human gut microflora using the prebiotics oligofructose and inulin. J Nutr. 1999;129: 1438S–1441S. doi: 10.1093/jn/129.7.1438S 10395616

53. Jovanovic-Malinovska R, Kuzmanova S, Winkelhausen E. Oligosaccharide profile in fruits and vegetables as sources of prebiotics and functional foods. Int J Food Prop. 2014;17: 949–965. doi: 10.1080/10942912.2012.680221

54. Kleessen B, Schwarz S, Boehm A, Fuhrmann H, Richter A, Henle T, et al. Jerusalem artichoke and chicory inulin in bakery products affect faecal microbiota of healthy volunteers. Br J Nutr. 2007;98: 540. doi: 10.1017/S0007114507730751 17445348

55. Tuohy KM, Kolida S, Lustenberger AM, Gibson GR. The prebiotic effects of biscuits containing partially hydrolysed guar gum and fructo-oligosaccharides–a human volunteer study. Br J Nutr. 2001;86: 341. doi: 10.1079/bjn2001394 11570986

56. Aly SM, Abdel-Galil Ahmed Y, Abdel-Aziz Ghareeb A, Mohamed MF. Studies on Bacillus subtilis and Lactobacillus acidophilus, as potential probiotics, on the immune response and resistance of Tilapia nilotica (Oreochromis niloticus) to challenge infections. Fish Shellfish Immunol. 2008;25: 128–136. doi: 10.1016/j.fsi.2008.03.013 18450477

57. Boger MCL, Lammerts van Bueren A, Dijkhuizen L. Cross-feeding among probiotic bacterial strains on prebiotic inulin involves the extracellular exo-inulinase of Lactobacillus paracasei Strain W20. Appl Environ Microbiol. 2018;84. doi: 10.1128/AEM.01539-18 30171006

58. Sazawal S, Hiremath G, Dhingra U, Malik P, Deb S, Black RE. Efficacy of probiotics in prevention of acute diarrhoea: a meta-analysis of masked, randomised, placebo-controlled trials. Lancet Infect Dis. 2006;6: 374–382. doi: 10.1016/S1473-3099(06)70495-9 16728323

59. Falagas ME, Betsi GI, Athanasiou S. Probiotics for the treatment of women with bacterial vaginosis. Clin Microbiol Infect. 2007;13: 657–664. doi: 10.1111/j.1469-0691.2007.01688.x 17633390

60. Li Y, Liu H, Dai X, Li J, Ding F. Effects of dietary inulin and mannan oligosaccharide on immune related genes expression and disease resistance of Pacific white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol. 2018;76: 78–92. doi: 10.1016/j.fsi.2018.02.034 29471061

61. El Khoury S, Rousseau A, Lecoeur A, Cheaib B, Bouslama S, Mercier P-L, et al. Deleterious interaction between honeybees (Apis mellifera) and its microsporidian intracellular parasite Nosema ceranae was mitigated by administrating either endogenous or allochthonous gut microbiota strains. Front Ecol Evol. 2018;6. doi: 10.3389/fevo.2018.00058

62. Piazzon MC, Calduch-Giner JA, Fouz B, Estensoro I, Simó-Mirabet P, Puyalto M, et al. Under control: how a dietary additive can restore the gut microbiome and proteomic profile, and improve disease resilience in a marine teleostean fish fed vegetable diets. Microbiome. 2017;5: 164. doi: 10.1186/s40168-017-0390-3 29282153

63. Sonnenburg JL, Bäckhed F. Diet–microbiota interactions as moderators of human metabolism. Nature. 2016;535: 56–64. doi: 10.1038/nature18846 27383980

64. Pernice M, Simpson SJ, Ponton F. Towards an integrated understanding of gut microbiota using insects as model systems. J Insect Physiol. 2014;69: 12–18. doi: 10.1016/j.jinsphys.2014.05.016 24862156

65. Engel P, Moran N. The gut microbiota of insects–diversity in structure and function. FEMS Microbiol Rev. 2013;37: 699–735. doi: 10.1111/1574-6976.12025 23692388

66. Dillon RJ, Dillon VM. The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol. 2004;49: 71–92. doi: 10.1146/annurev.ento.49.061802.123416 14651457

67. Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102: 11070–5. doi: 10.1073/pnas.0504978102 16033867

68. Hildebrandt MA, Hoffmann C, Sherrill-Mix SA, Keilbaugh SA, Hamady M, Chen Y-Y, et al. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology. 2009;137: 1716–24.e1–2. doi: 10.1053/j.gastro.2009.08.042 19706296

69. Chandler JA, Lang J, Bhatnagar S, Eisen JA, Kopp A. Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system. PLoS Genet. 2011;7. doi: 10.1371/journal.pgen.1002272 21966276

70. Vacchini V, Gonella E, Crotti E, Prosdocimi EM, Mazzetto F, Chouaia B, et al. Bacterial diversity shift determined by different diets in the gut of the spotted wing fly Drosophila suzukii is primarily reflected on acetic acid bacteria. Environ Microbiol Rep. 2017;9: 91–103. doi: 10.1111/1758-2229.12505 27886661

71. Broderick NA, Lemaitre B. Gut-associated microbes of Drosophila melanogaster. Gut Microbes. 2012;3: 307–321. doi: 10.4161/gmic.19896 22572876

72. Wong CNA, Ng P, Douglas AE. Low-diversity bacterial community in the gut of the fruitfly Drosophila melanogaster. Environ Microbiol. 2011;13: 1889–900. doi: 10.1111/j.1462-2920.2011.02511.x 21631690

73. Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci. 2010;107: 20051–20056. doi: 10.1073/pnas.1009906107 21041648

74. Fink C, Staubach F, Kuenzel S, Baines JF, Roeder T. Noninvasive analysis of microbiome dynamics in the fruit fly Drosophila melanogaster. Appl Environ Microbiol. 2013;79: 6984–6988. doi: 10.1128/AEM.01903-13 24014528

75. Billiet A, Meeus I, Van Nieuwerburgh F, Deforce D, Wäckers F, Smagghe G. Impact of sugar syrup and pollen diet on the bacterial diversity in the gut of indoor-reared bumblebees (Bombus terrestris). Apidologie. 2016;47: 548–560. doi: 10.1007/s13592-015-0399-1

76. Staudacher H, Kaltenpoth M, Breeuwer JAJ, Menken SBJ, Heckel DG, Groot AT. Variability of bacterial communities in the moth Heliothis virescens indicates transient association with the host. PLoS ONE. 2016;11: e0154514. doi: 10.1371/journal.pone.0154514 27139886

77. Belda E, Pedrola L, Peretó J, Martínez-Blanch JF, Montagud A, Navarro E, et al. Microbial diversity in the midguts of field and lab-reared populations of the European Corn Borer Ostrinia nubilalis. PLoS ONE. 2011;6. doi: 10.1371/journal.pone.0021751 21738787

78. Priya NG, Ojha A, Kajla MK, Raj A, Rajagopal R. Host plant induced variation in gut bacteria of Helicoverpa armigera. PLoS ONE. 2012;7: e30768. doi: 10.1371/journal.pone.0030768 22292034

79. Robinson CJ, Schloss P, Ramos Y, Raffa K, Handelsman J. Robustness of the bacterial community in the cabbage white butterfly larval midgut. Microb Ecol. 2010;59: 199–211. doi: 10.1007/s00248-009-9595-8 19924467

80. Broderick NA, Raffa KF, Goodman RM, Handelsman J. Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl Environ Microbiol. 2004;70: 293–300. doi: 10.1128/AEM.70.1.293-300.2004 14711655

81. Oliver KM, Russell JA, Moran NA, Hunter MS. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci U S A. 2003;100: 1803–7. doi: 10.1073/pnas.0335320100 12563031

82. Scarborough CL, Ferrari J, Godfray HCJ. Aphid protected from pathogen by endosymbiont. Science. 2005;310: 1781. doi: 10.1126/science.1120180 16357252

83. Kaltenpoth M, Göttler W, Herzner G, Strohm E. Symbiotic bacteria protect wasp larvae from fungal infestation. Curr Biol. 2005;15: 475–479. doi: 10.1016/j.cub.2004.12.084 15753044

84. Kroiss J, Kaltenpoth M, Schneider B, Schwinger M-G, Hertweck C, Maddula RK, et al. Symbiotic streptomycetes provide antibiotic combination prophylaxis for wasp offspring. Nat Chem Biol. 2010;6: 261–263. doi: 10.1038/nchembio.331 20190763

85. Brucker RM, Harris RN, Schwantes CR, Gallaher TN, Flaherty DC, Lam BA, et al. Amphibian chemical defense: antifungal metabolites of the microsymbiont Janthinobacterium lividum on the salamander Plethodon cinereus. J Chem Ecol. 2008;34: 1422–1429. doi: 10.1007/s10886-008-9555-7 18949519

86. Silverman MS, Davis I, Pillai DR. Success of self-administered home fecal transplantation for chronic Clostridium difficile infection. Clin Gastroenterol Hepatol. 2010;8: 471–3. doi: 10.1016/j.cgh.2010.01.007 20117243

87. Brandt LJ, Aroniadis OC, Mellow M, Kanatzar A, Kelly C, Park T, et al. Long-term follow-up of colonoscopic fecal microbiota transplant for recurrent Clostridium difficile infection. Am J Gastroenterol. 2012;107: 1079–1087. doi: 10.1038/ajg.2012.60 22450732

88. Youngster I, Sauk J, Pindar C, Wilson RG, Kaplan JL, Smith MB, et al. Fecal microbiota transplant for relapsing Clostridium difficile infection using a frozen inoculum from unrelated donors: a randomized, open-label, controlled pilot study. Clin Infect Dis. 2014;58: 1515–1522. doi: 10.1093/cid/ciu135 24762631

89. Hensley-McBain T, Zevin AS, Manuzak J, Smith E, Gile J, Miller C, et al. Effects of fecal microbial transplantation on microbiome and immunity in Simian Immunodeficiency Virus-infected macaques. J Virol. 2016;90: 4981–4989. doi: 10.1128/JVI.00099-16 26937040

90. Koch H, Schmid-Hempel P. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci U S A. 2011;108: 19288–92. doi: 10.1073/pnas.1110474108 22084077

91. Palmer-Young EC, Raffel TR, McFrederick QS. pH-mediated inhibition of a bumble bee parasite by an intestinal symbiont. Parasitology. 2019;146: 380–388. doi: 10.1017/S0031182018001555 30246672

92. Forsgren E, Olofsson TC, Vásquez A, Fries I. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie. 2009;41: 99–108. doi: 10.1051/apido/2009065

93. Evans JD, Armstrong TN. Inhibition of the American foulbrood bacterium, Paenibacillus larvae larvae, by bacteria isolated from honey bees. J Apic Res. 2005;44: 168–171. doi: 10.1080/00218839.2005.11101173

94. Yoshiyama M, Kimura K. Bacteria in the gut of Japanese honeybee, Apis cerana japonica, and their antagonistic effect against Paenibacillus larvae, the causal agent of American foulbrood. J Invertebr Pathol. 2009;102: 91–96. doi: 10.1016/j.jip.2009.07.005 19616552

95. Dillon RJ, Vennard CT, Buckling A, Charnley AK. Diversity of locust gut bacteria protects against pathogen invasion. Ecol Lett. 2005;8: 1291–1298. doi: 10.1111/j.1461-0248.2005.00828.x

96. Kešnerová L, Mars RAT, Ellegaard KM, Troilo M, Sauer U, Engel P. Disentangling metabolic functions of bacteria in the honey bee gut. PLoS Biol. 2017;15: e2003467. doi: 10.1371/journal.pbio.2003467 29232373

97. Heintz-Buschart A, Wilmes P. Human gut microbiome: function matters. Trends Microbiol. 2018;26: 563–574. doi: 10.1016/j.tim.2017.11.002 29173869

98. Carrara F, Giometto A, Seymour M, Rinaldo A, Altermatt F. Experimental evidence for strong stabilizing forces at high functional diversity of aquatic microbial communities. Ecology. 2015;96: 1340–1350. doi: 10.1890/14-1324.1 26236847

99. Moya A, Ferrer M. Functional redundancy-induced stability of gut microbiota subjected to disturbance. Trends Microbiol. 2016;24: 402–413. doi: 10.1016/j.tim.2016.02.002 26996765

100. van Hoek MJA, Merks RMH. Emergence of microbial diversity due to cross-feeding interactions in a spatial model of gut microbial metabolism. BMC Syst Biol. 2017;11: 56. doi: 10.1186/s12918-017-0430-4 28511646

101. Yooseph S, Kirkness EF, Tran TM, Harkins DM, Jones MB, Torralba MG, et al. Stool microbiota composition is associated with the prospective risk of Plasmodium falciparum infection. 2011; doi: 10.1186/s12864-015-1819-3 26296559

102. Morton ER, Lynch J, Froment A, Lafosse S, Heyer E, Przeworski M, et al. Variation in rural African gut microbiota is strongly correlated with colonization by Entamoeba and subsistence. PLoS Genet. 2015;11: e1005658. doi: 10.1371/journal.pgen.1005658 26619199

103. Boissière A, Tchioffo MT, Bachar D, Abate L, Marie A, Nsango SE, et al. Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with Plasmodium falciparum infection. PLoS Pathog. 2012;8: e1002742. doi: 10.1371/journal.ppat.1002742 22693451

104. Ramirez JL, Short SM, Bahia AC, Saraiva RG, Dong Y, Kang S, et al. Chromobacterium Csp_P reduces malaria and dengue infection in vector mosquitoes and has entomopathogenic and in vitro anti-pathogen activities. PLoS Pathog. 2014;10: e1004398. doi: 10.1371/journal.ppat.1004398 25340821

105. Yilmaz B, Portugal S, Tran TM, Gozzelino R, Ramos S, Gomes J, et al. Gut microbiota elicits a protective immune response against malaria transmission. Cell. 2014;159: 1277–1289. doi: 10.1016/j.cell.2014.10.053 25480293

106. Fanning S, Hall LJ, Cronin M, Zomer A, MacSharry J, Goulding D, et al. Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proc Natl Acad Sci USA. 2012;109: 2108–2113. doi: 10.1073/pnas.1115621109 22308390

107. Mockler BK, Kwong WK, Moran NA, Koch H. Microbiome structure influences infection by the parasite Crithidia bombi in bumble bees. Appl Environ Microbiol. 2018; AEM.02335-17. doi: 10.1128/AEM.02335-17 29374030

108. Johnston PR, Rolff J. Host and symbiont jointly control gut microbiota during complete metamorphosis. PLoS Pathog. 2015;11: e1005246. doi: 10.1371/journal.ppat.1005246 26544881

109. Caccia S, Di Lelio I, La Storia A, Marinelli A, Varricchio P, Franzetti E, et al. Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism. Proc Natl Acad Sci USA. 2016;113: 9486–9491. doi: 10.1073/pnas.1521741113 27506800

110. Kwong WK, Mancenido AL, Moran NA. Immune system stimulation by the native gut microbiota of honey bees. R Soc Open Sci. 2017;4: 170003. doi: 10.1098/rsos.170003 28386455

111. Hanage WP. Microbiome science needs a healthy dose of scepticism. Nature. 2014;512: 247–248. doi: 10.1038/512247a 25143098

112. Trosvik P, de Muinck EJ, Stenseth NC. Biotic interactions and temporal dynamics of the human gastrointestinal microbiota. ISME J. 2014;9: 533–541. doi: 10.1038/ismej.2014.147 25148482

113. Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 2008;453: 620–5. doi: 10.1038/nature07008 18509436

114. Faith JJ, Colombel J-F, Gordon JI. Identifying strains that contribute to complex diseases through the study of microbial inheritance. Proc Natl Acad Sci USA. 2015;112: 201418781. doi: 10.1073/pnas.1418781112 25576328

115. Greenblum S, Carr R, Borenstein E. Extensive strain-level copy-number variation across human gut microbiome species. Cell. 2015;160: 583–594. doi: 10.1016/j.cell.2014.12.038 25640238

116. Hammer TJ, McMillan WO, Fierer N. Metamorphosis of a butterfly-associated bacterial community. PLoS ONE. 2014;9. doi: 10.1371/journal.pone.0086995 24466308

117. Sharon I, Morowitz MJ, Thomas BC, Costello EK, Relman DA, Banfield JF. Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization. Genome Res. 2013;23: 111–20. doi: 10.1101/gr.142315.112 22936250

118. Zhernakova A, Kurilshikov A, Bonder MJ, Tigchelaar EF, Schirmer M, Vatanen T, et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science. 2016;352: 565–569. doi: 10.1126/science.aad3369 27126040

119. Raubenheimer D, Simpson SJ. Nutritional pharmEcology: doses, nutrients, toxins, and medicines. Integr Comp Biol. 2009;49: 329–337. doi: 10.1093/icb/icp050 21665823