The Hologenome Concept

Chapter

Abstract

The hologenome theory of evolution considers the holobiont (the animal or plant with all of its associated microorganisms) as a unit of selection in evolution. The hologenome is defined as the sum of the genetic information of the host and its microbiota. The theory is based on four generalizations, each of which is supported by a large body of empirical data: (1) All animals and plants establish symbiotic relationships with microorganisms; often the genetic information of the diverse microbiota exceeds that of the host. (2) Cooperation between the host and the microbiota contributes to the fitness of the holobiont. (3) Variation in the hologenome can be brought about by changes in either the host or the microbiota genomes; under environmental stress, the symbiotic microbial community can change rapidly by a variety of mechanisms including microbial amplification, horizontal gene transfer, and acquisition of new microorganisms from the environment. (4) Symbiotic microorganisms are transmitted between generations. These points taken together suggest that the genetic wealth of diverse microbial symbionts can play an important role both in adaptation and in evolution of higher organisms. During periods of rapid change in the environment, the diverse microbial symbiont community can aid the holobiont in surviving, multiplying, and buying the time necessary for the host genome to evolve. The distinguishing feature of the hologenome theory is that it considers all of the diverse microbiota associated with the animal or the plant as part of the evolving holobiont. The hologenome theory contains Lamarckian aspects within a Darwinian framework, accentuating both cooperation and competition within the holobiont and with other holobionts.

References

  1. Abe T, Bignell DE, Higashi M (eds) (2000) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic Publishers, DordrechtGoogle Scholar
  2. Abrams GD, Bishop JE (1967) Effect of normal microbial flora on gastrointestinal motility. Proc Soc Exp Biol Med 126:301–304PubMedGoogle Scholar
  3. Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 101:15718–15723PubMedCrossRefGoogle Scholar
  4. Bäckhed F, Manchester JK, Semenkovich CF, Gordon JI (2007) Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci USA 104:979–984PubMedCrossRefGoogle Scholar
  5. Barbieri E, Paster BJ, Hughes D, Zurek L, Moser DP, Teske A, Sogin ML (2001) Phylogenetic characterization of epibiotic bacteria in the accessory nidamental gland and egg capsules of the squid Loligo pealei (Cephalopoda: Loliginidae). Environ Microbiol 3:151–167PubMedCrossRefGoogle Scholar
  6. Baumann P, Moran NA, Baumann L (2006) Bacteriocyte-associated endosymbionts of insects. In: Dworkin M, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes, vol 1. Springer, New York, pp 403–438CrossRefGoogle Scholar
  7. Beijerinck MW (1901) Über oligonitrophile mikroben, centralblatt für bakteriologie, parasitenkunde, infektionskrankheiten und hygiene. Abteilung II 7:561–582Google Scholar
  8. Ben-Yosef M, Aharon Y, Jurkevitch E, Yuval B (2010) Give us the tools and we will do the job: symbiotic bacteria affect olive fly fitness in a diet-dependent fashion. Proc Biol Sci 277:1545–1552PubMedCrossRefGoogle Scholar
  9. Breitbart M, Hewson I, Felts B, Mahaffy JM, Nulton J, Salamon P, Rohwer F (2003) Metagenomic analyses of an uncultured viral community from human feces. J Bacteriol 185:6220–6223PubMedCrossRefGoogle Scholar
  10. Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8:218–230PubMedCrossRefGoogle Scholar
  11. Brune A, Stingl U (2006) Prokaryotic symbionts of termite gut flagellates: phylogenetic and metabolic implications of a tripartite symbiosis. Prog Mol Subcell Biol 41:39–60PubMedCrossRefGoogle Scholar
  12. Burkhardt RW (1972) The inspiration of Lamarck’s belief in evolution. J Hist Biol 5:413–438PubMedCrossRefGoogle Scholar
  13. Buss LW (1987) The evolution of individuality. Princeton University Press, PrincetonGoogle Scholar
  14. Cankar K, Kraigher H, Ravnikar M, Rupnik M (2005) Bacterial endophytes from seeds of Norway spruce (Picea abies L. Karst). FEMS Microbiol Lett 244:341–345PubMedCrossRefGoogle Scholar
  15. Chelius MK, Triplett EW (2001) The diversity of Archaea and bacteria in association with the roots of Zea mays L. Microb Ecol 41:252–263PubMedGoogle Scholar
  16. Collado MC, Isolauri E, Lairinen K, Sahminen S (2010) Effect of mother’s weight on infant’s microbiota acquisition, composition, and activity during early infancy: a prospective follow-up study initiated in early pregnancy. Am J Clin Nutr 95(5):1023–1030CrossRefGoogle Scholar
  17. Coyne MJ, Reinap B, Lee MM, Comstock LE (2005) Human symbionts use a host-like pathway for surface fucosylation. Science 307:1778–1781PubMedCrossRefGoogle Scholar
  18. Dale C, Moran NA (2006) Molecular interactions between bacterial symbionts and their hosts. Cell 126:453–465PubMedCrossRefGoogle Scholar
  19. De Filippoa C, Cavalieria D, Di Paolab M et al (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 107:14691–14696CrossRefGoogle Scholar
  20. Dehority BA (2003) Rumen microbiology. Nottingham University Press, NottinghamGoogle Scholar
  21. Dethlefsen L, McFall-Ngai M, Relman DA (2007) An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449:811–818PubMedCrossRefGoogle Scholar
  22. Devi SM, Ahmed I, Khan AA et al (2006) Genomes of Helicobacter pylori from native Peruvians suggest a mixture of ancestral and modern lineages and reveal a western type cag-pathogenicity island. BMC Genomics 7:191PubMedCrossRefGoogle Scholar
  23. Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner ACR, Yu WH, Lakshmanan A, Wade WG (2010) The human oral microbiome. J Bacteriol 192:50012–50017CrossRefGoogle Scholar
  24. Dominguez-Bello MG, Costellob EK, Knight R (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA 107:11971–11975PubMedCrossRefGoogle Scholar
  25. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M et al (2005) Diversity of the human intestinal microbial flora. Science 308:1635–1638PubMedCrossRefGoogle Scholar
  26. Edwards JE, McEwan NR, Travis AJ, Wallace RJ (2004) 16S rDNA library-based analysis of ruminal bacterial diversity. Antonie van Leeuwenhoek 86:263–281CrossRefGoogle Scholar
  27. Fallowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and the bioenergetics of a symbiotic coral. Bioscience 34:705–709CrossRefGoogle Scholar
  28. Fiore CL, Jarett JK, Olson ND, Lesser MP (2010) Nitrogen fixation and nitrogen transformations in marine symbioses. Trends Microbiol 10:455–463CrossRefGoogle Scholar
  29. Foster JS, Kolenbrander PE (2004) Development of a multispecies oral bacterial community in a saliva-conditioned flow cell. Appl Environ Microbiol 70:4340–4348PubMedCrossRefGoogle Scholar
  30. Frank DN, Pace NR (2008) Gastrointestinal microbiology enters the metagenomics era. Curr Opin Gastroenterol 24:4–10PubMedCrossRefGoogle Scholar
  31. Fraune S, Bosch TCG (2007) Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proc Natl Acad Sci USA 104:13146–13151PubMedCrossRefGoogle Scholar
  32. Frias-lopez J, Zerkle AL, Bonheyo GT, Fouke BW (2002) Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces. Appl Environ Microbiol 68:2214–2228PubMedCrossRefGoogle Scholar
  33. Gilbert SF, McDonald E, Boyle N et al (2010) Symbiosis as a source of selectable epigenetic variation: taking the heat for the big guy. Philos Trans R Soc Lond B Biol Sci 365:671–678PubMedCrossRefGoogle Scholar
  34. Gould SJ (1999) A division of worms. Nat Hist 108:18–26Google Scholar
  35. Grice EA, Kong HH, Conlan S (2009) Topographical and temporal diversity of the human skin microbiome. Science 324:1190–1192PubMedCrossRefGoogle Scholar
  36. Gündüz E, Douglas AE (2009) Symbiotic bacteria enable insect to use a nutritionally inadequate diet. Proc R Soc 276:987–991CrossRefGoogle Scholar
  37. Hehemann JH, Correc G, Barbeyron T et al (2010) Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464:908–914PubMedCrossRefGoogle Scholar
  38. Heijtza RD, Wange S, Anuard F et al (2011) Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci USA. doi:10.1073/pnas.1010529108
  39. Hentschel U, Steinert M, Hacker J (2000) Common molecular mechanisms of symbiosis and pathogenesis. Trends Microbiol 8:226–231PubMedCrossRefGoogle Scholar
  40. Hongoh Y, Deevong P, Inoue T, Moriya S, Trakulnaleamsai S, Ohkuma M, VongKaluny C, Noparatnaraporn N, Kudo T (2005) Intra- and interspecific comparisons of bacterial diversity and community structure support coevolution of gut microbiota and termite host. Appl Environ Microbiol 71:6590–6599PubMedCrossRefGoogle Scholar
  41. Hooper LV, Midtvedt T, Gordon JI (2002) How host-microbial interactions shape the nutrient environment of the mammalian intestine. Ann Rev Nutr 22:283–307CrossRefGoogle Scholar
  42. Ikeda S, Okubo T, Anda M et al (2010) Community- and genome-based views of plant-associated bacteria: plant–bacterial interactions in soybean and rice. Plant Cell Physiol 51:1398–1410PubMedCrossRefGoogle Scholar
  43. Iniguez AL, Dong YM, Triplett EW (2004) Nitrogen fixation in wheat provided by Klebsiella pneumoniae 342. Mol Plant Microbe Interact 17:1078–1085PubMedCrossRefGoogle Scholar
  44. Iwanaga S, Lee BL (2005) Recent advances in the innate immunity of invertebrate animals. J Biochem Mol Biol 38:128–150PubMedCrossRefGoogle Scholar
  45. Jablonka E, Lamb MJ (2005) Evolution in four dimensions: genetic, epigenetic, behavioral, and symbolic variation in the history of life. MIT Press, CambridgeGoogle Scholar
  46. Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ (2010) Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329:212–215PubMedCrossRefGoogle Scholar
  47. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium medicago model. Nat Rev Microbiol 5:619–633PubMedCrossRefGoogle Scholar
  48. Kikuchi Y, Hosokawa T, Fukatsu T (2007) Insect–microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl Environ Microbiol 73:4308–4316Google Scholar
  49. Kneip C, Lockhart P, Voss C, Maier UG (2007) Nitrogen fixation in eukaryotes–new models for symbiosis. BMC Evol Biol 7:55. doi: 10.1186/1471-2148-7-55 PubMedCrossRefGoogle Scholar
  50. Koenig JE, Spor A, Scalfone N et al (2010) Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA 108(Suppl 1):4578–4585PubMedGoogle Scholar
  51. Koren O, Rosenberg E (2006) Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl Environ Microbiol 72:5254–5259PubMedCrossRefGoogle Scholar
  52. Laitinen K, Poussa T, Isolauri E et al (2009) Probiotic and dietary counseling contribute to glucose regulation during and after pregnancy: a randomised controlled trial. Br J Nutr 101:1679–1687PubMedCrossRefGoogle Scholar
  53. Lambais MR, Crowley DE, Cury JC, B¨ull RC, Rodrigues RR (2006) Bacterial diversity in tree canopies of the Atlantic forest. Science 312:1917PubMedCrossRefGoogle Scholar
  54. Leser TD, Amenuvor JZ, Jensen TK, Lindecrona RH, Boye M, Møller K (2002) Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl Environ Microbiol 68: 673–690PubMedCrossRefGoogle Scholar
  55. Ley RE, B¨ackhed F, Turnbaugh P, Lozupone CA, Knigh RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102:11070–11075PubMedCrossRefGoogle Scholar
  56. Ley RE, Peterson DA, Gordon JI (2006a) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–848PubMedCrossRefGoogle Scholar
  57. Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006b) Human gut microbes associated with obesity. Nature 444:1022–1023PubMedCrossRefGoogle Scholar
  58. Lilburn TG, Kim KS, Ostrom NE, Byzek KR, Leadbetter JR, Breznak JA (2001) Nitrogen fixation by symbiotic and free-living spirochetes. Science 292:2495–2498PubMedCrossRefGoogle Scholar
  59. MacConnachie AA, Fox R, Kennedy DR, Seaton RA (2009) Faecal transplant for recurrent Clostridium difficile-associated diarrhoea: a UK case series. QJM 102:781–784PubMedCrossRefGoogle Scholar
  60. Margulis L (1993) Symbiosis in Cell Evolution: Microbial Communities in the Archean and Proterozoic Eons. 2nd edn. W.H. Freeman and Co., New YorkGoogle Scholar
  61. Martens EC, Roth R, Heuser JE, Gordon JI (2009) Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont. J Biol Chem 284:18445–18457PubMedCrossRefGoogle Scholar
  62. Martínez-García M, Díaz-Valéz M, Wanner G, Ramos-Esplá A, Antón J (2007) Microbial community associated with the colonial ascidian Cyctodytes dellechiajei. Environ Microbiol 9:521–534Google Scholar
  63. Mateos M, Castrezana SJ, Nankivell BJ, Estes AM, Markow TA, Moran NA (2006) Heritable endosymbionts of Drosophila. Genetics 174:363–376PubMedCrossRefGoogle Scholar
  64. McFall-Ngai MJ (1999) Consequences of evolving with bacterial symbionts: insights from the squid–Vibrio association. Annu Rev Ecol Syst 30:235–256CrossRefGoogle Scholar
  65. McFall-Ngai MJ (2002) Unseen forces: the influence of bacteria on animal development. Dev Biol 242:1–14PubMedCrossRefGoogle Scholar
  66. Mohamed NM, Colman AS, Tal Y, Hill RT (2008) Diversity and expression of nitrogen fixation genes in bacterial symbionts of marine sponges. Environ Microbiol 10:2910–2921PubMedCrossRefGoogle Scholar
  67. Moran NA, Jarvik T (2010) Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328:624–627PubMedCrossRefGoogle Scholar
  68. Nardi JB, Mackieb RI, Dawson JO (2002) Could microbial symbionts of arthropod guts contribute significantly to nitrogen fixation in terrestrial ecosystems? J Insect Physiol 48:751–763PubMedCrossRefGoogle Scholar
  69. Ochman H, Worobey M, Kuo, CH et al. (2010) Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol. 8, e1000546Google Scholar
  70. O’Hara AM, Shanahan F (2006) The gut flora as a forgotten organ. EMBO Rep 7:688–693PubMedCrossRefGoogle Scholar
  71. Pollard JW (1984) Is Weismann’s barrier absolute? In: Ho MW, Saunders PT (eds) Beyond neo-Darwinism: introduction to the new evolutionary paradigm. Academic, London, pp 291–315Google Scholar
  72. Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E (2006) The coral probiotic hypothesis. Environ Microbiol 8:2067–2073CrossRefGoogle Scholar
  73. Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14CrossRefGoogle Scholar
  74. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10CrossRefGoogle Scholar
  75. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362PubMedCrossRefGoogle Scholar
  76. Russell JA, Latorre A, Sabater-Mũnoz B, Moya A, Moran NA (2003) Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol Ecol 12:1061–1075PubMedCrossRefGoogle Scholar
  77. Savage DC, Siegel JD, Snellen JE, Whitt DD (1981) Transit time of epithelial cells in the small intestines of germfree mice and ex-germfree mice associated with indigenous microorganisms. Appl Environ Microbiol 42:996–1001PubMedGoogle Scholar
  78. Scarborough CL, Ferrari J, Godfray HCJ (2005) Aphids protected from pathogen by endosymbiont. Science 310:1781–1783PubMedCrossRefGoogle Scholar
  79. Sharon G, Segal D, Ringo JM et al (2010) Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci USA 107:20051–20056PubMedCrossRefGoogle Scholar
  80. Sharp KH, Eam B, Faulkner DJ, Haygood MG (2007) Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl Environ Microbiol 73:622–629PubMedCrossRefGoogle Scholar
  81. Silva AM, Barbosa FHF, Duarte R, Vieira LQ, Arantes RME, Nicoli JR (2004) Effect of Bifidobacterium longum ingestion on experimental salmonellosis in mice. J Appl Microbiol 97:29–37PubMedCrossRefGoogle Scholar
  82. Skaljac M, Zanic K, Ban SG, Kontsedalov S, Ghanim M (2010) Co-infection and localization of secondary symbionts in two whitefly species. BMC Microbiol 10:142PubMedCrossRefGoogle Scholar
  83. Smith KP, Handelsman J, Goodman RM (1999) Genetic basis in plants for interactions with disease-suppressive bacteria. Proc Natl Acad Sci USA 96:4786–4790PubMedCrossRefGoogle Scholar
  84. Stougaard J (2000) Regulators and regulation of legume root nodule development. Plant Physiol 124:531–540PubMedCrossRefGoogle Scholar
  85. Sundset MA, Praesteng KE, Cann IK, Mathiesen SD, Mackie RI (2007) Novel rumen bacterial diversity in two geographically separated sub-specie of reindeer. Microb Ecol 54:424–438PubMedCrossRefGoogle Scholar
  86. Tannock G (1995) Normal microflora. Chapman & Hall, LondonGoogle Scholar
  87. Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge associated microorganisms: evolution, ecology and biotechnological potentials. Microbiol Mol Biol Rev 71:295–347PubMedCrossRefGoogle Scholar
  88. Thingstad TF, Lignell R (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat Microb Ecol 13:19–27CrossRefGoogle Scholar
  89. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031PubMedCrossRefGoogle Scholar
  90. Turnbaugh PJ, Ridaura VK, Faith JJ et al (2009) The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 1(6):6ra14PubMedCrossRefGoogle Scholar
  91. Turnes MS, Hay ME, Fenical W (1989) Symbiotic marine bacteria chemically defend crustacean embryos from a pathogenic fungus. Science 246:116CrossRefGoogle Scholar
  92. Veneti ZL, Reuter M, Montenegro H, Hornett EA, Charlat S, Hurst GD (2005) Interactions between inherited bacteria and their hosts: the Wolbachia paradigm. The influence of Cooperative Bacteria on Animal Host Biology (McFall-Ngai MJ, Henderson B & Ruby E-G, eds), pp. 119–141. Cambridge University Press, New YorkGoogle Scholar
  93. Visick KL, Foster J, Doino J, McFall-Ngai MJ, Ruby EG (2000) Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J Bacteriol 182:4578–4586PubMedCrossRefGoogle Scholar
  94. Wallace RJ (2004) Antimicrobial properties of plant secondary metabolites. Proc Nutr Soc 63:621–629PubMedCrossRefGoogle Scholar
  95. Wang B, Qui YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363PubMedCrossRefGoogle Scholar
  96. Webster NS, Wilson KJ, Blackall LL, Hill RT (2001) Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl Environ Microbiol 67:434–444PubMedCrossRefGoogle Scholar
  97. Weismann A (1893) The germ-plasm: a theory of heredity. Charles Scribner’s Sons/Electronic Scholarly Publishing, New YorkGoogle Scholar
  98. Weitz JS, Hartman H, Levin SA (2005) Coevolutionary arms races between bacteria and bacteriophage. Proc Natl Acad Sci USA 102:9535–9540PubMedCrossRefGoogle Scholar
  99. Wilson DS, Sober E (1989) Reviving the superorganism. J Theor Biol 136:337–356PubMedCrossRefGoogle Scholar
  100. Wilkinson DM (2001) Mycorrhizal evolution. Trends Ecol Evol 16:64–65PubMedCrossRefGoogle Scholar
  101. Wostmann BS (1981) The germ-free animal in nutritional studies. Annu Rev Nutr 1:257–297PubMedCrossRefGoogle Scholar
  102. Wostmann BS, Larkin C, Moriarty A, Bruckner-Kardoss E (1983) Dietary intake, energy metabolism and excretory losses of adult male germfree Wistar rats. Lab Anim Sci 33:46–50PubMedGoogle Scholar
  103. Wust PK, Horn MA, Drake HL (2011) Clostridiaceae and Enterobacteriaceae as active fermenters in earthworm gut content. ISME 5:92–106CrossRefGoogle Scholar
  104. Xu J, Mahowald MA, Ley RE (2007) Evolution of symbiotic bacteria in the distal human intestine. PLOS Biol 5:1574–1586Google Scholar
  105. Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci USA 96:1463–1468PubMedCrossRefGoogle Scholar
  106. Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735PubMedCrossRefGoogle Scholar
  107. Zoetendal EG, Akkermans ADL, van Vliet WM et al (2001) A host genotype affects the bacterial community in the human gastrointestinal tract. Microb Ecol Health Dis 13:129–134CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of Molecular Microbiology and BiotechnologyTel Aviv UniversityTel AvivIsrael

Personalised recommendations