title: Is eating behavior manipulated by the gastrointestinal microbiota? Evolutionary pressures and potential mechanisms.
abstract: Microbes in the gastrointestinal tract are under selective pressure to manipulate host eating behavior to increase their fitness, sometimes at the expense of host fitness. Microbes may do this through two potential strategies: (i) generating cravings for foods that they specialize on or foods that suppress their competitors, or (ii) inducing dysphoria until we eat foods that enhance their fitness. We review several potential mechanisms for microbial control over eating behavior including microbial influence on reward and satiety pathways, production of toxins that alter mood, changes to receptors including taste receptors, and hijacking of the vagus nerve, the neural axis between the gut and the brain. We also review the evidence for alternative explanations for cravings and unhealthy eating behavior. Because microbiota are easily manipulatable by prebiotics, probiotics, antibiotics, fecal transplants, and dietary changes, altering our microbiota offers a tractable approach to otherwise intractable problems of obesity and unhealthy eating.
authors.affiliation: Department of Emergency Medicine, University of New Mexico, Albuquerque, NM, USA.
authors.forename: Joe
authors.initials: J
authors.lastname: Alcock
authors.forename: Carlo C
authors.initials: CC
authors.lastname: Maley
authors.forename: C Athena
authors.initials: CA
authors.lastname: Aktipis
mesh_terms: D000818:Animals; D005075:Biological Evolution; D005247:Feeding Behavior; D041981:Gastrointestinal Tract / Q000382:microbiology*; D006801:Humans; D064307:Microbiota; D008954:Models, Biological; D009765:Obesity / Q000209:etiology
keywords: cravings; evolutionary conflict; host manipulation; microbiome; microbiota; obesity
references.citation: PLoS Comput Biol. 2010 Nov 04;6(11):e1000968
references.pmid: 21079667
references.citation: Nature. 2010 Apr 8;464(7290):908-12
references.pmid: 20376150
references.citation: Science. 2013 Sep 6;341(6150):1241214
references.pmid: 24009397
references.citation: Science. 2013 Feb 1;339(6119):548-54
references.pmid: 23363771
references.citation: Science. 1996 Sep 6;273(5280):1380-3
references.pmid: 8703071
references.citation: Mol Endocrinol. 2014 Aug;28(8):1221-38
references.pmid: 24892638
references.citation: Pediatrics. 2013 Feb;131(2):e550-8
references.pmid: 23319531
references.citation: Science. 2010 Apr 9;328(5975):228-31
references.pmid: 20203013
references.citation: mBio. 2012 Oct 16;3(5):e00280-12
references.pmid: 23073764
references.citation: Proc Natl Acad Sci U S A. 2011 Sep 20;108(38):16050-5
references.pmid: 21876150
references.citation: JAMA. 2010 Jan 20;303(3):235-41
references.pmid: 20071471
references.citation: Nature. 2007 Oct 18;449(7164):811-8
references.pmid: 17943117
references.citation: Nat Rev Microbiol. 2008 Oct;6(10):776-88
references.pmid: 18794915
references.citation: J Proteome Res. 2007 Nov;6(11):4469-77
references.pmid: 17929959
references.citation: Nature. 2006 Dec 21;444(7122):1027-31
references.pmid: 17183312
references.citation: Cell Tissue Res. 2011 Jan;343(1):23-32
references.pmid: 20941511
references.citation: N Engl J Med. 2011 Jun 23;364(25):2392-404
references.pmid: 21696306
references.citation: FEMS Microbiol Lett. 2006 Jan;254(1):1-11
references.pmid: 16451172
references.citation: N Engl J Med. 2007 Jul 26;357(4):370-9
references.pmid: 17652652
references.citation: Nat Rev Endocrinol. 2011 Aug 09;7(11):639-46
references.pmid: 21826100
references.citation: Appetite. 1990 Dec;15(3):231-46
references.pmid: 2281953
references.citation: Obes Surg. 2012 Nov;22(11):1771-82
references.pmid: 22956251
references.citation: Br J Nutr. 2011 Mar;105(5):755-64
references.pmid: 20974015
references.citation: Pers Soc Psychol Rev. 2007 May;11(2):131-49
references.pmid: 18453459
references.citation: Clin Nutr. 2010 Jun;29(3):288-303
references.pmid: 20056521
references.citation: Proc Natl Acad Sci U S A. 2004 Nov 2;101(44):15718-23
references.pmid: 15505215
references.citation: PLoS One. 2012;7(6):e39748
references.pmid: 22768116
references.citation: Physiol Behav. 2000 Jan;68(3):353-9
references.pmid: 10716545
references.citation: Psychoneuroendocrinology. 2013 Sep;38(9):1738-47
references.pmid: 23566632
references.citation: Behav Brain Sci. 2004 Aug;27(4):443-58; discussion 459-90
references.pmid: 15773426
references.citation: Int J Obes (Lond). 2013 Feb;37(2):216-23
references.pmid: 22410962
references.citation: Appetite. 1991 Dec;17(3):187-97
references.pmid: 1799281
references.citation: Neurogastroenterol Motil. 2012 May;24(5):405-13
references.pmid: 22404222
references.citation: Annu Rev Microbiol. 2011;65:411-29
references.pmid: 21682646
references.citation: Nat Rev Gastroenterol Hepatol. 2013 Oct;10(10):575-84
references.pmid: 23835488
references.citation: Nature. 2010 Mar 4;464(7285):59-65
references.pmid: 20203603
references.citation: Br J Nutr. 2002 May;87(5):517-23
references.pmid: 12010590
references.citation: PLoS Biol. 2013;11(8):e1001637
references.pmid: 23976882
references.citation: Gut. 2014 May;63(5):727-35
references.pmid: 23804561
references.citation: Surgery. 2008 Jun;143(6):723-31
references.pmid: 18549888
references.citation: Nature. 2006 Dec 21;444(7122):1022-3
references.pmid: 17183309
references.citation: Br J Pharmacol. 2013 Sep;170(1):4-16
references.pmid: 23347064
references.citation: Bioessays. 2011 Aug;33(8):574-81
references.pmid: 21732396
references.citation: Nat Rev Microbiol. 2012 Nov;10(11):735-42
references.pmid: 23000955
references.citation: Nature. 2012 May 09;486(7402):222-7
references.pmid: 22699611
references.citation: Neurosci Biobehav Rev. 1990 Summer;14(2):125-34
references.pmid: 2348939
references.citation: Nat Rev Cancer. 2004 Aug;4(8):579-91
references.pmid: 15286738
references.citation: Obesity (Silver Spring). 2010 Jan;18(1):190-5
references.pmid: 19498350
references.citation: FEMS Microbiol Lett. 2013 Mar;340(1):1-10
references.pmid: 23181549
references.citation: Am J Clin Nutr. 2013 Jul;98(1):16-24
references.pmid: 23719559
references.citation: Q Rev Biol. 2003 Jun;78(2):169-202
references.pmid: 12825417
references.citation: BMJ. 1997 May 3;314(7090):1325-8
references.pmid: 9158470
references.citation: Psychophysiology. 1993 Mar;30(2):183-96
references.pmid: 8434081
references.citation: Physiol Behav. 2011 Oct 24;104(5):709-21
references.pmid: 21827777
references.citation: Science. 2013 Mar 1;339(6123):1084-8
references.pmid: 23328391
references.citation: BMC Biol. 2013 May 21;11:61
references.pmid: 23692866
references.citation: PLoS One. 2012;7(1):e29968
references.pmid: 22272265
references.citation: Pharmacol Biochem Behav. 2000 May;66(1):3-14
references.pmid: 10837838
references.citation: Science. 2011 Oct 7;334(6052):105-8
references.pmid: 21885731
references.citation: Nat Med. 2007 Jan;13(1):35-7
references.pmid: 17159985
references.citation: Conscious Cogn. 2012 Jun;21(2):1016-22
references.pmid: 22309814
references.citation: Nature. 2009 Jan 22;457(7228):480-4
references.pmid: 19043404
references.citation: Cancer Prev Res (Phila). 2010 Nov;3(11):1388-97
references.pmid: 20947487
references.citation: Science. 2005 Mar 25;307(5717):1915-20
references.pmid: 15790844
references.citation: J Am Coll Nutr. 2003 Oct;22(5):331-9
references.pmid: 14559925
references.citation: J Clin Endocrinol Metab. 1997 Nov;82(11):3864-71
references.pmid: 9360553
references.citation: Metab Brain Dis. 2009 Mar;24(1):81-93
references.pmid: 19082698
references.citation: Elife. 2013 Apr 16;2:e00458
references.pmid: 23599893
references.citation: Mucosal Immunol. 2008 May;1(3):183-97
references.pmid: 19079178
references.citation: DNA Res. 2007 Aug 31;14(4):169-81
references.pmid: 17916580
references.citation: Biosci Biotechnol Biochem. 2010;74(8):1656-61
references.pmid: 20699581
references.citation: PLoS One. 2012;7(2):e31951
references.pmid: 22384111
references.citation: Physiol Behav. 2012 Nov 5;107(4):476-83
references.pmid: 22366157
references.citation: PLoS One. 2012;7(10):e46966
references.pmid: 23071679
references.citation: Proc Natl Acad Sci U S A. 2010 Aug 17;107(33):14691-6
references.pmid: 20679230
references.citation: Eur J Clin Nutr. 2007 Mar;61(3):355-61
references.pmid: 17151594
references.citation: Br J Nutr. 2012 Mar;107(5):621-30
references.pmid: 21781379
references.citation: Nat Rev Neurosci. 2011 Jul 13;12(8):453-66
references.pmid: 21750565
references.citation: J Biol Chem. 2013 Aug 30;288(35):25088-25097
references.pmid: 23836895
references.citation: Gastroenterology. 2011 Aug;141(2):599-609, 609.e1-3
references.pmid: 21683077
references.citation: Prikl Biokhim Mikrobiol. 2006 May-Jun;42(3):261-8
references.pmid: 16878539
references.citation: N Engl J Med. 1990 Mar 29;322(13):882-9
references.pmid: 2314422
references.citation: Infect Immun. 2012 Feb;80(2):688-703
references.pmid: 22144490
references.citation: Brain Res. 1981 Nov 30;225(2):249-69
references.pmid: 7030452
references.citation: Int J Eat Disord. 1995 Jul;18(1):79-90
references.pmid: 7670446
references.citation: Am J Clin Nutr. 2000 Mar;71(3):682-92
references.pmid: 10702160
references.citation: Eur Heart J. 1994 Aug;15(8):1113-8
references.pmid: 7988604
references.citation: Am J Gastroenterol. 2000 Oct;95(10):2698-709
references.pmid: 11051338
references.citation: Proc Natl Acad Sci U S A. 2008 Feb 12;105(6):2193-7
references.pmid: 18268332
references.citation: Nutrition. 2008 Apr;24(4):348-59
references.pmid: 18262391
references.citation: Q Rev Biol. 2011 Jun;86(2):97-120
references.pmid: 21800636
references.citation: Nature. 2013 Sep 5;501(7465):52-7
references.pmid: 23965627
references.citation: Eur J Clin Nutr. 2010 Jun;64(6):636-43
references.pmid: 20216555
references.citation: PLoS One. 2011;6(8):e23277
references.pmid: 21858053
references.citation: Auton Neurosci. 2010 Feb 16;153(1-2):41-6
references.pmid: 19674941
references.citation: Neuroscience. 2003;119(1):215-21
references.pmid: 12763082
references.citation: Neuroscience. 2010 Nov 10;170(4):1179-88
references.pmid: 20696216
references.citation: Diabetes Obes Metab. 2012 Feb;14(2):112-20
references.pmid: 21812894
references.citation: Am J Hum Biol. 2003 May-Jun;15(3):320-9
references.pmid: 12704708
references.citation: Cell Host Microbe. 2011 Aug 18;10(2):118-35
references.pmid: 21843869
references.citation: Appetite. 1991 Dec;17(3):167-75
references.pmid: 1799279
references.citation: Nat Rev Gastroenterol Hepatol. 2009 May;6(5):306-14
references.pmid: 19404271
references.citation: Bioessays. 2013 Sep;35(9):810-7
references.pmid: 23836415
references.citation: Science. 2012 Feb 24;335(6071):936-41
references.pmid: 22363001
references.citation: Biol Psychiatry. 2007 Jul 1;62(1):55-64
references.pmid: 16945350
references.citation: Brain Behav Immun. 2005 Jul;19(4):334-44
references.pmid: 15944073
references.citation: Proc Natl Acad Sci U S A. 2010 Jan 26;107 Suppl 1:1731-5
references.pmid: 19666529
references.citation: Bioessays. 2013 Jun;35(6):508-12
references.pmid: 23575749
references.citation: Clin Nutr. 2011 Apr;30(2):156-64
references.pmid: 20970896
references.citation: J Bacteriol. 2013 Feb;195(3):411-6
references.pmid: 23144247
references.citation: Transl Psychiatry. 2014 Apr 29;4:e387
references.pmid: 24780921
references.citation: J Immunol. 1985 Aug;135(2 Suppl):816s-819s
references.pmid: 2861236
references.citation: FEMS Microbiol Ecol. 2013 Jan;83(1):1-16
references.pmid: 22775757
references.citation: Appetite. 2013 Oct;69:1-7
references.pmid: 23684901