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PLOS Biology  2012 

The Evolution of Mutualism in Gut Microbiota Via Host Epithelial Selection

DOI: 10.1371/journal.pbio.1001424

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Abstract:

The human gut harbours a large and genetically diverse population of symbiotic microbes that both feed and protect the host. Evolutionary theory, however, predicts that such genetic diversity can destabilise mutualistic partnerships. How then can the mutualism of the human microbiota be explained? Here we develop an individual-based model of host-associated microbial communities. We first demonstrate the fundamental problem faced by a host: The presence of a genetically diverse microbiota leads to the dominance of the fastest growing microbes instead of the microbes that are most beneficial to the host. We next investigate the potential for host secretions to influence the microbiota. This reveals that the epithelium–microbiota interface acts as a selectivity amplifier: Modest amounts of moderately selective epithelial secretions cause a complete shift in the strains growing at the epithelial surface. This occurs because of the physical structure of the epithelium–microbiota interface: Epithelial secretions have effects that permeate upwards through the whole microbial community, while lumen compounds preferentially affect cells that are soon to slough off. Finally, our model predicts that while antimicrobial secretion can promote host epithelial selection, epithelial nutrient secretion will often be key to host selection. Our findings are consistent with a growing number of empirical papers that indicate an influence of host factors upon microbiota, including growth-promoting glycoconjugates. We argue that host selection is likely to be a key mechanism in the stabilisation of the mutualism between a host and its microbiota.

References

[1]  Sanon A, Andrianjaka ZN, Prin Y, Bally R, Thioulouse J, et al. (2009) Rhizosphere microbiota interfers with plant-plant interactions. Plant Soil 321: 259–278. doi: 10.1007/s11104-009-0010-5
[2]  Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427: 731–733. doi: 10.1038/nature02322
[3]  Ruby EG, McFall-Ngai MJ (1999) Oxygen-utilizing reactions and symbiotic colonization of the squid light organ by Vibrio fischeri. Trends Microbiol 7: 414–420. doi: 10.1016/s0966-842x(99)01588-7
[4]  Visick KL, McFall-Ngai MJ (2000) An exclusive contract: specificity in the Vibrio fischeri-Euprymna scolopes partnership. J Bacteriol 182: 1779. doi: 10.1128/jb.182.7.1779-1787.2000
[5]  Graf J (1998) Host-derived amino acids support the proliferation of symbiotic bacteria. Proc Natl Acad Sci U S A 95: 1818–1822. doi: 10.1073/pnas.95.4.1818
[6]  Dethlefsen L, McFall-Ngai M, Relman DA (2007) An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449: 811–818. doi: 10.1038/nature06245
[7]  Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124: 837–848. doi: 10.1016/j.cell.2006.02.017
[8]  Holzapfel WH, Haberer P, Snel J, Schillinger U, Huis in't Veld JH (1998) Overview of gut flora and probiotics. Int J Food Microbiol 41: 85–101. doi: 10.1016/s0168-1605(98)00044-0
[9]  Hooper LV, Macpherson AJ (2010) Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol 10: 159–169. doi: 10.1038/nri2710
[10]  Sekirov I, Russell SL, Antunes LCM, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90: 859–904. doi: 10.1152/physrev.00045.2009
[11]  Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6: 776–788. doi: 10.1038/nrmicro1978
[12]  B?ckhed F, Ley RE, Sonnenburg JL, Peterson D a, Gordon JI (2005) Host-bacterial mutualism in the human intestine. Science 307: 1915–1920. doi: 10.1126/science.1104816
[13]  B?ckhed F, Ding H, Wang T, Hooper LV, Koh GY, et al. (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 101: 15718–15723. doi: 10.1073/pnas.0407076101
[14]  Cash HL, Whitham CV, Behrendt CL, Hooper LV (2006) Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313: 1126–1130. doi: 10.1126/science.1127119
[15]  Kelly D, Campbell JI, King TP, Grant G, Jansson EA, et al. (2004) Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nat Immunol 5: 104–112. doi: 10.1038/ni1018
[16]  Martin F-PJ, Dumas M-E, Wang Y, Legido-Quigley C, Yap IKS, et al. (2007) A top-down systems biology view of microbiome-mammalian metabolic interactions in a mouse model. Mol Syst Biol 3: 112. doi: 10.1038/msb4100153
[17]  Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R (2004) Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118: 229–241. doi: 10.1016/j.cell.2004.07.002
[18]  Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL (2005) An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122: 107–118. doi: 10.1016/j.cell.2005.05.007
[19]  Frank SA (1994) Genetics of mutualism: the evolution of altruism between species. J Theor Biol 170: 393–400. doi: 10.1006/jtbi.1994.1200
[20]  West SA, Kiers ET, Simms EL, Denison RF (2002) Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proc Biol Sci 269: 685–694. doi: 10.1098/rspb.2001.1878
[21]  Sachs JL, Mueller UG, Wilcox TP, Bull JJ (2004) The evolution of cooperation. Q Rev Biol 79: 135–160. doi: 10.1086/383541
[22]  Foster KR, Wenseleers T (2006) A general model for the evolution of mutualisms. J Evol Biol 19: 1283–1293. doi: 10.1111/j.1420-9101.2005.01073.x
[23]  Poulsen M, Boomsma JJ (2005) Mutualistic fungi control crop diversity in fungus-growing ants. Science 307: 741–744. doi: 10.1126/science.1106688
[24]  Kiers ET, Rousseau RA, West SA, Denison RF (2003) Host sanctions and the legume-rhizobium mutualism. Nature 425: 78–81. doi: 10.1038/nature01931
[25]  Nyholm SV, McFall-Ngai MJ (2004) The winnowing: establishing the squid-vibrio symbiosis. Nat Rev Microbiol 2: 632–642. doi: 10.1038/nrmicro957
[26]  Muegge BD, Kuczynski J, Knights D, Clemente JC, González A, et al. (2011) Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332: 970–974. doi: 10.1126/science.1198719
[27]  Faith JJ, McNulty NP, Rey FE, Gordon JI (2011) Predicting a human gut microbiota's response to diet in gnotobiotic mice. Science 333: 101–104. doi: 10.1126/science.1206025
[28]  Salzman N (2010) Paneth cell defensins and the regulation of the microbiome: Détente at mucosal surfaces. Gut Microbes 1: 401. doi: 10.4161/gmic.1.6.14076
[29]  Peterson DA, McNulty NP, Guruge JL, Gordon JI, McNutty NP (2007) IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2: 328–339. doi: 10.1016/j.chom.2007.09.013
[30]  Vaishnava S, Yamamoto M, Severson KM, Ruhn KA, Yu X, et al. (2011) The antibacterial lectin RegIII promotes the spatial segregation of microbiota and host in the intestine. Science 334: 255–258. doi: 10.1126/science.1209791
[31]  Salzman NH, Hung K, Haribhai D, Chu H, Karlsson-Sj?berg J, et al. (2010) Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 11: 76–83. doi: 10.1038/ni.1825
[32]  Atuma C, Strugala V, Allen A, Holm L (2001) The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. Am J Physiol-Gastr L 280: G922–G929.
[33]  Brugman S, Nieuwenhuis EES (2010) Mucosal control of the intestinal microbial community. J Mol Med 88: 881–888. doi: 10.1007/s00109-010-0639-9
[34]  Olmsted SS, Padgett JL, Yudin AI, Whaley KJ, Moench TR, et al. (2001) Diffusion of macromolecules and virus-like particles in human cervical mucus. Biophys J 81: 1930–1937. doi: 10.1016/s0006-3495(01)75844-4
[35]  Cone RA (2009) Barrier properties of mucus. Adv Drug Deliver Rev 61: 75–85. doi: 10.1016/j.addr.2008.09.008
[36]  Johansson MEV, Holmén Larsson JM, Hansson GC (2010) Microbes and Health Sackler Colloquium: the two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc Natl Acad Sci U S A 108: 4659–4665. doi: 10.1073/pnas.1006451107
[37]  Hooper LV, Xu J, Falk PG, Midtvedt T, Gordon JI (1999) A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. Proc Natl Acad Sci U S A 96: 9833–9838. doi: 10.1073/pnas.96.17.9833
[38]  Fabich AJ, Jones SA, Chowdhury FZ, Cernosek A, Anderson A, et al. (2008) Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine. Infect Immun 76: 1143–1152. doi: 10.1128/iai.01386-07
[39]  Hooper LV (2001) Commensal host-bacterial relationships in the gut. Science 292: 1115–1118. doi: 10.1126/science.1058709
[40]  Sonnenburg JL, Xu J, Leip DD, Chen C-H, Westover BP, et al. (2005) Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307: 1955–1959. doi: 10.1126/science.1109051
[41]  Bevins CL, Salzman NH (2011) The potter's wheel: the host's role in sculpting its microbiota. Cell Mol Life Sci 68: 3675–3685. doi: 10.1007/s00018-011-0830-3
[42]  Petnicki-Ocwieja T, Hrncir T, Liu Y-J, Biswas A, Hudcovic T, et al. (2009) Nod2 is required for the regulation of commensal microbiota in the intestine. Proc Natl Acad Sci U S A 106: 15813–15818. doi: 10.1073/pnas.0907722106
[43]  Girardin SE, Boneca IG, Viala J, Chamaillard M, Labigne A, et al. (2003) Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 278: 8869–8872. doi: 10.1074/jbc.c200651200
[44]  Macpherson AJ, Uhr T (2004) Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303: 1662–1665. doi: 10.1126/science.1091334
[45]  Kawamoto S, Tran TH, Maruya M, Suzuki K, Doi Y, et al. (2012) The inhibitory receptor PD-1 regulates IgA selection and bacterial composition in the gut. Science 336: 485–489. doi: 10.1126/science.1217718
[46]  Wehkamp J, Harder J, Weichenthal M, Schwab M, Sch?ffeler E, et al. (2004) NOD2 (CARD15) mutations in Crohn's disease are associated with diminished mucosal alpha-defensin expression. Gut 53: 1658–1664. doi: 10.1136/gut.2003.032805
[47]  Wehkamp J, Salzman NH, Porter E, Nuding S, Weichenthal M, et al. (2005) Reduced Paneth cell alpha-defensins in ileal Crohn's disease. Proc Natl Acad Sci U S A 102: 18129–18134. doi: 10.1073/pnas.0505256102
[48]  Van den Abbeele P, Van de Wiele T, Verstraete W, Possemiers S (2011) The host selects mucosal and luminal associations of coevolved gut microorganisms: A novel concept. FEMS Microbiol Rev 35: 681–704. doi: 10.1111/j.1574-6976.2011.00270.x
[49]  McFall-Ngai M (2007) Adaptive immunity: care for the community. Nature 445: 153. doi: 10.1038/445153a
[50]  dos Santos VM, Müller M, de Vos WM (2010) Systems biology of the gut: the interplay of food, microbiota and host at the mucosal interface. Curr Opin Biotechnol 21: 539–550. doi: 10.1016/j.copbio.2010.08.003
[51]  Gudelj I, Weitz JS, Ferenci T, Claire Horner-Devine M, Marx CJ, et al. (2010) An integrative approach to understanding microbial diversity: from intracellular mechanisms to community structure. Ecol Lett 13: 1073–1084. doi: 10.1111/j.1461-0248.2010.01507.x
[52]  Rang CU, Licht TR, Midtvedt T, Conway PL, Chao L, et al. (1999) Estimation of growth rates of Escherichia coli BJ4 in streptomycin-treated and previously germfree mice by in situ rRNA hybridization. Clin Diagn Lab Immunol 6: 434–436.
[53]  Lozupone C, Faust K, Raes J, Faith JJ, Frank DN, et al. (2012) Identifying genomic and metabolic features that can underlie early successional and opportunistic lifestyles of human gut symbionts. Genome Res 22: 1974–1984. doi: 10.1101/gr.138198.112
[54]  Kreft J-U (2004) Biofilms promote altruism. Microbiology 150: 2751–2760. doi: 10.1099/mic.0.26829-0
[55]  Nadell CD, Foster KR, Xavier JB (2010) Emergence of spatial structure in cell groups and the evolution of cooperation. PLoS Comp Biol 6: e1000716 doi:10.1371/journal.pcbi.1000716.
[56]  Kreft J-U, Bonhoeffer S (2005) The evolution of groups of cooperating bacteria and the growth rate versus yield trade-off. Microbiology 151: 637–641. doi: 10.1099/mic.0.27415-0
[57]  Varum FJO, Veiga F, Sousa JS, Basit AW (2012) Mucus thickness in the gastrointestinal tract of laboratory animals. J Pharm Pharmacol 64: 218–227. doi: 10.1111/j.2042-7158.2011.01399.x
[58]  Matsuo K, Ota H, Akamatsu T, Sugiyama A (1997) Histochemistry of the surface mucous gel layer of the human colon. Gut 40: 782. doi: 10.1136/gut.40.6.782
[59]  McGuckin MA, Lindén SK, Sutton P, Florin TH (2011) Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9: 265–278. doi: 10.1038/nrmicro2538
[60]  Foster KR (2004) Diminishing returns in social evolution: the not-so-tragic commons. J Evol Biol 17: 1058–1072. doi: 10.1111/j.1420-9101.2004.00747.x
[61]  Foster KR (2011) The sociobiology of molecular systems. Nat Rev Genet 12: 193–203. doi: 10.1038/nrg2903
[62]  Hooper LV, Gordon JI (2001) Glycans as legislators of host-microbial interactions: spanning the spectrum from symbiosis to pathogenicity. Glycobiology 11: 1R–10R. doi: 10.1093/glycob/11.2.1r
[63]  Hooper LV (2009) Do symbiotic bacteria subvert host immunity? Nat Rev Microbiol 7: 367–374. doi: 10.1038/nrmicro2114
[64]  LoCascio RG, Ninonuevo MR, Freeman SL, Sela DA, Grimm R, et al. (2007) Glycoprofiling of bifidobacterial consumption of human milk oligosaccharides demonstrates strain specific, preferential consumption of small chain glycans secreted in early human lactation. J Agric Food Chem 55: 8914–8919. doi: 10.1021/jf0710480
[65]  Stahl M, Friis LM, Nothaft H, Liu X, Li J, et al. (2011) L-fucose utilization provides Campylobacter jejuni with a competitive advantage. Proc Natl Acad Sci U S A 108: 7194–7199. doi: 10.1073/pnas.1014125108
[66]  Nadell CD, Xavier JB, Foster KR (2009) The sociobiology of biofilms. FEMS Microbiol Rev 33: 206–224. doi: 10.1111/j.1574-6976.2008.00150.x
[67]  Gilman RT, Nuismer SL, Jhwueng D-C (2012) Coevolution in multidimensional trait space favours escape from parasites and pathogens. Nature 483: 328–330. doi: 10.1038/nature10853
[68]  Bucci V, Bradde S, Biroli G, Xavier JB (2012) Social interaction, noise and antibiotic-mediated switches in the intestinal microbiota. PLoS Comp Biol 8: e1002497 doi:10.1371/journal.pcbi.1002497.
[69]  Xavier JB, Picioreanu C, van Loosdrecht MCM (2005) A framework for multidimensional modelling of activity and structure of multispecies biofilms. Environ Microbiol 7: 1085–1103. doi: 10.1111/j.1462-2920.2005.00787.x
[70]  Xavier JB, De Kreuk MK, Picioreanu C, van Loosdrecht MCM (2007) Multi-scale individual-based model of microbial and bioconversion dynamics in aerobic granular sludge. Environ Sci Technol 41: 6410–6417. doi: 10.1021/es070264m
[71]  Picioreanu C, van Loosdrecht MC, Heijnen JJ (1998) Mathematical modeling of biofilm structure with a hybrid differential-discrete cellular automaton approach. Biotechnol Bioeng 58: 101–116. doi: 10.1002/(sici)1097-0290(19980405)58:1<101::aid-bit11>3.0.co;2-m
[72]  Kreft JU, Picioreanu C, Wimpenny JW, van Loosdrecht MC (2001) Individual-based modelling of biofilms. Microbiology 147: 2897–2912.
[73]  Nadell CD, Xavier JB, Levin SA, Foster KR (2008) The evolution of quorum sensing in bacterial biofilms. PLoS Biol 6: e14 doi:10.1371/journal.pbio.0060014.
[74]  Mitri S, Xavier JB, Foster KR (2011) Colloquium Paper: social evolution in multispecies biofilms. Proc Natl Acad Sci U S A 108: 10839–10846. doi: 10.1073/pnas.1100292108
[75]  Xavier JB, Foster KR (2007) Cooperation and conflict in microbial biofilms. Proc Natl Acad Sci U S A 104: 876–881. doi: 10.1073/pnas.0607651104
[76]  Korolev KS, Xavier JB, Nelson DR, Foster KR (2011) A quantitative test of population genetics using spatiogenetic patterns in bacterial colonies. Am Nat 178: 538–552. doi: 10.1086/661897
[77]  Nadell CD, Bassler BL (2011) A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms. Proc Natl Acad Sci U S A 108: 14181–14185. doi: 10.1073/pnas.1111147108
[78]  Lardon LA, Merkey BV, Martins S, Dotsch A, Picioreanu C, et al. (2011) iDynoMiCS: next generation of individual-based modelling of biofilms. Environ Microbiol 13: 2416–2434. doi: 10.1111/j.1462-2920.2011.02414.x
[79]  Spor A, Koren O, Ley R (2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol 9: 279–290. doi: 10.1038/nrmicro2540
[80]  Rezzonico E, Mestdagh R, Delley M, Combremont S, Dumas M-E, et al. (2011) Bacterial adaptation to the gut environment favors successful colonization: microbial and metabonomic characterization of a simplified microbiota mouse model. Gut Microbes 2: 307–318. doi: 10.4161/gmic.18754
[81]  Johansson MEV, Phillipson M, Petersson J, Velcich A, Holm L, et al. (2008) The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci U S A 105: 15064–15069. doi: 10.1073/pnas.0803124105
[82]  Krivan V (2006) The ideal free distribution and bacterial growth on two substrates. Theor Popul Biol 69: 181–191. doi: 10.1016/j.tpb.2005.07.006
[83]  Stecher B, Robbiani R, Walker AW, Westendorf AM, Barthel M, et al. (2007) Salmonella enterica Serovar Typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol 5: 2177–2189 doi:10.1371/journal.pbio.0050244.

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