Role of Microorganisms in Adaptation, Development, and Evolution of Animals and Plants: The Hologenome Concept

Reference work entry


Eukaryotes evolved from prokaryotes and have remained in close association with them. All animals and plants establish symbiotic relationships with microorganisms; often the combined genetic information of the diverse microbiota exceeds that of the host. How the genetic wealth of the microbiota affects all aspects of the holobiont’s (host plus all of its associated microorganisms) fitness (adaptation, survival, development, growth, and reproduction) and evolution is reviewed, using selected invertebrate, vertebrate, plant, and insect published experimental results. The data are discussed within the framework of the hologenome concept of evolution, which demonstrates that changes in environmental parameters, for example, diet, can cause rapid changes in the diverse microbiota, which not only can benefit the holobiont in the short term but also can be transmitted to offspring and lead to long-lasting cooperations. During periods of rapid changes in the environment, the diverse microbial symbiont community can assist the holobiont in surviving, multiplying, and buying the time necessary for the host genome to evolve. The potential application of the hologenome concept can be seen in the fields of prebiotics and probiotics.


Mating Preference Bacterial Symbiont Microbial Symbiont Bacterium Symbiosis Bifidobacterium Lactis 
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  1. Abbas Hilmi HT, Surakka A, Apajalahti J, Saris PE (2007) Identification of the most abundant Lactobacillus species in the crop of 1- and 5-week-old broiler chickens. Appl Environ Microbiol 73:7867–7873PubMedGoogle Scholar
  2. Abe T, Bignell DE, Higashi M (eds) (2000) Termites: evolution, sociality, symbioses, ecology. Kluwer, DordrechtGoogle Scholar
  3. Abrams GD, Bishop JE (1967) Effect of normal microbial flora on gastrointestinal motility. Proc Soc Exp Biol Med 126:301–304PubMedGoogle Scholar
  4. Abu-Shanab A, Eamonn MM, Quigley EMM (2010) The role of the gut microbiota in nonalcoholic fatty liver disease. Nat Rev Gastro Hepatol 7:691–701Google Scholar
  5. Akman LA, Yamashita H, Watanabe A et al (2002) Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glosssinidia. Nat Genet 32:402–407PubMedGoogle Scholar
  6. Andersson SGE, Zomorodipour A, Andersson JO (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133–143PubMedGoogle Scholar
  7. 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 3:151–167PubMedGoogle Scholar
  8. 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 104:979–984PubMedGoogle Scholar
  9. 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 403–438Google Scholar
  10. Bednarek P, Kwon C, Schulze-Lefert P (2010) Not a peripheral issue: secretion in plant–microbe interactions. Curr Opin Plant Biol 13:378–387PubMedGoogle Scholar
  11. Belden LK, Harris RN (2007) Infectious diseases in wildlife: the community ecology context. Front Ecol Environ 5(10):533–539Google Scholar
  12. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13PubMedGoogle Scholar
  13. Blaser MJ, Falkow S (2009) What are the consequences of the disappearing human microbiota? Nature Rev Microbiol 7:887–894Google Scholar
  14. Breibart M, Hewson I, Felts B et al (2003) Metagenomic analysis of an uncultured viral community from human feces. J Bacteriol 185:6220–6223Google Scholar
  15. Breznak JA, Brune A (1994) Role of microorganisms in the digestion of lignocellulose by termites. Ann Rev Entomol 39:453–487Google Scholar
  16. Brooks SPJ, McAllister M, Sandoz M, Kalmokoff ML (2003) Culture-independent phylogenetic analysis of the faecal flora of the rat. Can J Microbiol 49:589–601PubMedGoogle Scholar
  17. Broz AK, Manter DK, Vivanco JM (2007) Soil fungal abundance and diversity: another victim of the invasive plant Centaurea maculosa. ISMEJ 1:763–765Google Scholar
  18. Bucher M, Wegmüller S, Drissner D (2009) Chasing the structures of small molecules in arbuscular mycorrhizal signaling. Curr Opin Plant Biol 12:500–507PubMedGoogle Scholar
  19. Buddemeier RW, Baker AC, Fautin DG, Jacobs JR (2004) The adaptive hypothesis of bleaching. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, New York, pp 427–444Google Scholar
  20. Caesar R, Fåk F, Bäckhed F (2010) Effects of gut microbiota on obesity and atherosclerosis via modulation of inflammation and lipid metabolism. J Intern Med 268:320–328PubMedGoogle Scholar
  21. Cani PD, Delzenne NM (2009) The role of the gut microbiota in energy metabolism and metabolic disease. Curr Pharm Des 15:1546–1558PubMedGoogle Scholar
  22. Cankar K, Kraigher H, Ravnikar M, Rupnik M (2005) Bacterial endophytes from seeds of Norway spruce (Picea abies L. Karst). FEMS Microbiol Lett 244:341–345PubMedGoogle Scholar
  23. Chelius MK, Triplett EW (2001) The diversity of Archaea and bacteria in association with the roots of Zea mays. Microb Ecol 41:252–263PubMedGoogle Scholar
  24. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711–745PubMedGoogle Scholar
  25. Coyne JA (1992) Genetics and speciation. Nature 355:511–515PubMedGoogle Scholar
  26. Currie CR, Poulsen M, Mendenhall J et al (2006) Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants. Science 311:81–83PubMedGoogle Scholar
  27. Davidov Y, Jurkevitch E (2009) Predation between prokaryotes and the origin of eukaryotes. Bioessays 31:748–757PubMedGoogle Scholar
  28. Dedeine F, Vavre F, Fleury F et al (2001) Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci USA 98:6247–6252PubMedGoogle Scholar
  29. Dehority BA (2003) Rumen microbiology. Nottingham University Press, NottinghamGoogle Scholar
  30. de la Cruz F, Davies J (2005) Industrial revolution and microbial evolution. In: McFall-Ngai MJ, Henderson B, Ruby EG (eds) (2005) The influence of cooperative bacteria on animal host biology. Cambridge University Press, New York, pp 73–82Google Scholar
  31. Delmotte N, Knief C, Chaffron S et al (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci USA 106:16428–16433PubMedGoogle Scholar
  32. Dethlefsen L, Eckburg PB, Bik EM, Relman DA (2006) Assembly of the human intestinal microbiota. Trends Ecol Evol 21:517–523PubMedGoogle Scholar
  33. 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 7:191PubMedGoogle Scholar
  34. Dewhirst FE, Chen T, Izard J et al (2010) The human oral microbiome. J Bacteriol 192:341–345Google Scholar
  35. Dodd DMB (1989) Reproductive isolation as a consequence of adaptive divergence in Drosophila pseudoobscura. Evolution 43:1308–1311Google Scholar
  36. Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37PubMedGoogle Scholar
  37. Ducklow HW, Mitchel R (1979) Bacterial populations and adaptations in the mucus layers on living corals. Limnol Oceanogr 24:715–725Google Scholar
  38. Edwards JE, McEwan NR, Travis AJ, Wallace RJ (2004) 16S rDNA library-based analysis of ruminal bacterial diversity. Anton Van Leeuw 86:263–281Google Scholar
  39. Ercolani GL (1991) Distribution of epiphytic bacteria on olive leaves and the influence of leaf age and sampling time. Microb Ecol 21:35–48Google Scholar
  40. Falcon L, Magallon S, Castillo A (2010) Dating the cyanobacterial ancestor of the chloroplast. ISME J 4:777–783PubMedGoogle Scholar
  41. Fine M, Loya Y (2002) Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proc R Soc Lond B 269:1205–1210Google Scholar
  42. Fraune S, Bosch TCH (2007) Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proc Natl Acad Sci USA 104:13146–13151PubMedGoogle Scholar
  43. Frey JC, Rothman JM, Pell AN et al (2006) Fecal bacterial diversity in a wild gorilla. Appl Environ Microbiol 72:3788–3792PubMedGoogle Scholar
  44. Gibson GR, Probert HM, Van Loo J, Rastall RA, Roberfroid MB (2004) Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev 17(2):259–275PubMedGoogle Scholar
  45. 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 365:671–678Google Scholar
  46. Golichenkov MV, Kostina NV, Ul’yanova TA et al (2002) Specific features of nitrogen fixation and denitrification in termites Neotermes castaneus, Zootermopsis angusticollis, and Reticulitermes lucifugus. Biol Bull 29:172–175Google Scholar
  47. Grice EA, Kong HH, Contan S et al (2009) Topographical and temporal diversity of the human skin microbiome. Science 324:1190–1192PubMedGoogle Scholar
  48. Hapfelmeier S, Lawson MAE, Slack E et al (2010) Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses. Science 328:1705–1709PubMedGoogle Scholar
  49. Hardison RC (1996) A brief history of hemoglobins: plant, animal, protist, and bacteria. Proc Natl Acad Sci USA 93:5675–5679PubMedGoogle Scholar
  50. Herwig RP, Staley JT, Nerini MK, Braham HW (1984) Baleen whales: preliminary evidence for forestomach microbial fermentation. Appl Environ Microbiol 47:421–423PubMedGoogle Scholar
  51. Hickman CS (2005) How have bacteria contributed to the evolution of multicellular animals? In: McFall-Ngai MJ, Henderson B, Ruby EG (eds) The influence of cooperative bacteria on animal host biology. Cambridge University Press, New York, pp 3–33Google Scholar
  52. Hoffman FA, Heimbach JT, Sanders ME, Hibberd PL (2008) Executive Summary: Scientific and regulatory challenges of development of probiotics as food and drugs. Clinical Infect Dis 46:S53–S57Google Scholar
  53. Hongoh Y, Deevong P, Inoue T et al (2005) Intra- and interspecific comparisons of bacterial diversity and community structure support coevolution of gut microbiota and termite host. Appl Environ Microbiol 71:6590–6599PubMedGoogle Scholar
  54. Hooper LV, Gordon JI (2001) Commensal host-bacterial relationships in the gut. Science 292:1115–1118PubMedGoogle Scholar
  55. Hurek T, Reinhold-Hurek B (2003) Azoarcus sp. strain BH72 as a model for nitrogen-fixing grass endophytes. J Biotechnol 106:169–178PubMedGoogle Scholar
  56. Innes L, Hobbs PJ, Bardgett RD (2004) The impacts of individual plant species on rhizosphere microbial communities in soils of different fertility. Biol Fertil Soils 40:7–13Google Scholar
  57. Ivanov II, Littman DR (2011) Modulation of immune homeostasis by commensal bacteria. Curr Opin Microbiol 14:106–114PubMedGoogle Scholar
  58. Iwanaga S, Lee BL (2005) Recent advances in the innate immunity of invertebrate animals. J Biochem Mol Biol 38:128–150PubMedGoogle Scholar
  59. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium medicago model. Nat Rev Microbiol 5:619–633PubMedGoogle Scholar
  60. Kaufman MR, Ikeda Y, Patton C, Van Dykhuizen G, Epel D (1998) Bacterial symbionts colonize the accessory nidamental gland of the squid Loligo opalescens via horizontal transmission. Bio Bull 194:36–43Google Scholar
  61. 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 73:4308–4316PubMedGoogle Scholar
  62. Komai M, Shirakawa H, Kimura S (1988) Newly developed model for vitamin K deficiency in germfree mice. Int J Vitam Nutr Res 58(1):55–59PubMedGoogle Scholar
  63. Koren O, Rosenberg E (2006) Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl Environ Microbiol 72:5254–5259PubMedGoogle Scholar
  64. Lambais MR, Crowley DE, Cury JC, Büll RC, Rodrigues RR (2006) Bacterial diversity in tree canopies of the Atlantic Forest. Science 312:1917PubMedGoogle Scholar
  65. Leser TD, Amenuvor JZ, Jensen TK et al (2002) Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl Environ Microbiol 68:673–690PubMedGoogle Scholar
  66. Ley RE, Bäckhed F, Turnbaugh P et al (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102:11070–11075PubMedGoogle Scholar
  67. Ley RE, Peterson DA, Gordon JI (2006a) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–848PubMedGoogle Scholar
  68. Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006b) Human gut microbes associated with obesity. Nature 444:1022–1023PubMedGoogle Scholar
  69. Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nature Rev Microbiol 6:776–788Google Scholar
  70. Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883PubMedGoogle Scholar
  71. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting Rhizobacteria. Annu Rev Microbiol 63:541–556PubMedGoogle Scholar
  72. Luoto R, Laitinen K, Nermes M, Isolauri E (2010a) Impact of maternal probiotic-supplemented dietary counseling on pregnancy outcome and prenatal and postnatal growth: a double-blind, placebo-controlled study. Br J Nutr 103:1792–1799PubMedGoogle Scholar
  73. Luoto R, Kalliomaki M, Laitinen K, Isolalauri E (2010b) The impact of perinatal intervention on the development of overweight and obesity: follow-up study from birth to 10 years. Int J Obes 34:1531–1537Google Scholar
  74. Mai V, Ukhanova M, Baer DJ (2010) Understanding the extent and sources of variation in gut microbiota studies; a prerequisite for establishing associations with disease. Diversity 2:1085–1096Google Scholar
  75. Margulis L (1993) Symbiosis in cell evolution: microbial communities in the Archean and Proterozoic eons, 2nd edn. Freeman, New YorkGoogle Scholar
  76. Margulis L, Sagan D (2001) Marvellous microbes. Resurgence 206:10–12Google Scholar
  77. Mart´ınez-Garc´ıa M, D´ıaz-Vald´ez M,Wanner G et al (2007) Microbial community associated with the colonial ascidian Cyctodytes dellechiajei. Environ Microbiol 9:521–534Google Scholar
  78. Mateos M, Castrezana SJ, Nankivell BJ, Estes AM, Markow TA, Moran NA (2006) Heritable endosymbionts of Drosophila. Genetics 174:363–376PubMedGoogle Scholar
  79. McFall-Ngai MJ (1999) Consequences of evolving with bacterial symbionts: insights from the squid–Vibrio association. Ann Rev Ecol Syst 30:235–256Google Scholar
  80. Micallef SA, Shiaris MP, Colon-Carmona A (2009) Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation. J Exp Bot 60:1729–1742PubMedGoogle Scholar
  81. Minkley N, Fujita A, Brune A, Kirchner WH (2006) Nest specificity of the bacterial community in termite guts (Hodotermes mossambicus). Insect Soc 53:339–344Google Scholar
  82. Montgomery MK, McFall-Ngai M (1994) Bacterial symbionts induce host organ morphogenesis during early postembryonic development of the squid Euprymna scolopes. Development 120:1719–1729PubMedGoogle Scholar
  83. Mueller S, Saunier K, Hanisch C et al (2006) Differences in fecal microbiota in different European study populations in relation to age, gender and country: a cross-sectional study. Appl Environ Microbiol 72:1027–1033PubMedGoogle Scholar
  84. Nissimov J, Rosenberg E, Munn C (2009) Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microb Lett 292:210–215Google Scholar
  85. Nyholm SV, McFall-Ngai M (2004) The winnowing: establishing the squid vibrio symbiosis. Nat Rev Microbiol 2:632–642PubMedGoogle Scholar
  86. Ochman HM, Worobey CH, Kuo JB et al (2010) Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol 8:e1000546. onlineGoogle Scholar
  87. O’Hara AM, Shanahan F (2006) The gut flora as a forgotten organ. EMBO Rep 7:688–693PubMedGoogle Scholar
  88. Olsen MA, Aagnes TH, Mathiesen SD (1994) Digestion of herring by indigenous bacteria in the minke whale forestomach. Appl Environ Microbiol 60:4445–4455PubMedGoogle Scholar
  89. Ott T, Sullivan J, James EK et al (2009) Absence of symbiotic leghemoglobins alters bacteroid and plant cell differentiation during development of Lotus japonicus root nodules. Mol Plant Microbe Interact 22:800–808PubMedGoogle Scholar
  90. Pennisi E (2004) Evolutionary biology. The birth of the nucleus. Science 305:766–768PubMedGoogle Scholar
  91. Portier P (1918) Les symbiotes. Masson, ParisGoogle Scholar
  92. Qin J, Li R, Raes J et al (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65PubMedGoogle Scholar
  93. Redford AJ, Fierer N (2009) Bacterial succession on the leaf surface: a novel system for studying successional dynamics. Microb Ecol 58:189–198PubMedGoogle Scholar
  94. Redford AJ, Bowers RM, Knight R et al (2010) The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ Microbiol 12:2885–2893PubMedGoogle Scholar
  95. Reichenbach H (1984) Myxobacteria: a most peculiar group of social prokaryotes. In: Rosenberg E (ed) Myxobacteria: development and cell interactions. Springer, New York, pp 1–50Google Scholar
  96. Reid G, Younes JA, Van der Mei HC et al (2011) Microbiota restoration: natural and supplemented recovery of human microbial communities. Nat Rev Microbiol 9:27–38PubMedGoogle Scholar
  97. Reitner J, Schumann-Kindel G (1997) Pyrite in mineralized sponge tissue-product of sulfate reducing sponge related bacteria. Facies 36:272–276Google Scholar
  98. Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14Google Scholar
  99. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10Google Scholar
  100. Rosenberg E, Falkovitz L (2004) The Vibrio shiloi/Oculina patagonica model system of coral bleaching. Ann Rev Microbiol 58:143–159Google Scholar
  101. 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 5:355–362PubMedGoogle Scholar
  102. Ruby EG (1996) Lessons from a cooperative bacterial-animal association: the Vibrio fischeri-Euprymna scolopes light organ symbiosis. Annu Rev Microbiol 50:591–624PubMedGoogle Scholar
  103. Russell JB, Rychlik JL (2001) Factors that alter rumen ecology. Science 292:1119–1122PubMedGoogle Scholar
  104. Russell JA, Latorre A, Sabater-Muñoz B, Moya A, Moran NA (2003) Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol Ecol 12:1061–1075PubMedGoogle Scholar
  105. Sandström JP, Russel JA, White JP, Moran NA (2001) Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol Ecol 10:217–228PubMedGoogle Scholar
  106. 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
  107. Schluter D (2009) Evidence for ecological speciation and its alternative. Science 323:737–741PubMedGoogle Scholar
  108. Schmitt-Wagner D, Friedrich MW, Wagner B, Brune A (2003) Phylogenetic diversity, abundance, and axial distribution of bacteria in the intestinal tract of two soil-feeding termites. Appl Environ Microbiol 69:6007–6017PubMedGoogle Scholar
  109. Schopf JW (1993) Microfossils of the early Archean Apex chert: new evidence of the antiquity of life. Science 260:640–646PubMedGoogle Scholar
  110. Sharon G, Segal D, Ringo JM, Zilber-Rosenberg I, Rosenberg E (2010) Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci USA 107:20051–20056PubMedGoogle Scholar
  111. Sharp KH, Eam B, Faulkner DJ, Haygood MG (2007) Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl Environ Microbiol 73:622–629PubMedGoogle Scholar
  112. Shashar N, Cohen Y, Loya Y, Sar N (1994) Nitrogen fixation (acetylene reduction) in stony corals: evidence for coral–bacteria interactions. Mar Ecol Prog Ser 111:259–264Google Scholar
  113. She X, Jiang Z, Clark RA, Liu G et al (2004) Shotgun sequence assembly and recent segmental duplications within the human genome. Nature 431:927–930PubMedGoogle Scholar
  114. Shnit-Orland M, Kushmaro A (2009) Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol 67:371–380PubMedGoogle Scholar
  115. Silva AM, Barbosa FH, Duarte R et al (2004) Effect of Bifidobacterium longum ingestion on experimental salmonellosis in mice. J Appl Microbiol 97:29–37PubMedGoogle Scholar
  116. Singh BK, Millard P, Whiteley AS, Murrell JC (2004) Unravelling rhizosphere–microbial interactions: opportunities and limitations. Trends Microbiol 12:386–393PubMedGoogle Scholar
  117. Smith KP, Handelsman J, Goodman RM (1999) Genetic basis in plants for interactions with disease-suppressive bacteria. Proc Natl Acad Sci USA 96:4786–4790PubMedGoogle Scholar
  118. Somers E, Vanderleyden J, Srinivasan M (2004) Rhizosphere bacterial signalling: a love parade beneath our feet. Crit Rev Microbiol 30:205–240PubMedGoogle Scholar
  119. Stappenbeck TS, Hooper LV, Gordon JI (2002) Developmental regulation of intestinal angiogenesis by Peneth cells. Proc Natl Acad Sci USA 99:15451–15455PubMedGoogle Scholar
  120. Stecher B, Hardt WD (2008) The role of microbiota in infectious disease. Trends Microbiol 16:107–114PubMedGoogle Scholar
  121. Stougaard J (2000) Regulators and regulation of legume root nodule development. Plant Physiol 124:531–540PubMedGoogle Scholar
  122. Stow A, Beattie A (2008) Chemical and genetic defenses against disease in insect societies. Brain Behav Immun 22:1009–1013PubMedGoogle Scholar
  123. Sundset MA, Praesteng KE, Cann IK, Mathiesen SD, Mackie RI (2007) Novel rumen bacterial diversity in two geographically separated sub-species of reindeer. Microb Ecol 54:424–438PubMedGoogle Scholar
  124. Tannock G (1995) Normal microflora. Chapman & Hall, LondonGoogle Scholar
  125. Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge associated microorganisms: evolution, ecology and biotechnological potentials. Microbiol Mol Biol Rev 71:295–347PubMedGoogle Scholar
  126. Thingstad TF, Lignell R (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat Microb Ecol 13:19–27Google Scholar
  127. Turnbaugh PJ, Ley RE, Mahowald MA et al (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031PubMedGoogle Scholar
  128. van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310PubMedGoogle Scholar
  129. Veneti ZL, Reuter M, Montenegro H et al (2005) Interactions between inherited bacteria and their hosts: the Wolbachia paradigm. In: McFall Ngai MJ, Henderson B, Ruby EG (eds) The influence of cooperative bacteria on animal host biology. Cambridge University Press, New York, pp 119–141Google Scholar
  130. 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 Bact 182:4578–4586PubMedGoogle Scholar
  131. Wallace RJ (2004) Antimicrobial properties of plant secondary metabolites. Proc Nutr Soc 63:621–629PubMedGoogle Scholar
  132. Warnecke F, Luginbu P, Ivanova N et al (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–565PubMedGoogle Scholar
  133. Watanabe H, Tokuda G (2010) Cellulolytic systems in insects. Annu Rev Entomol 55:609–632PubMedGoogle Scholar
  134. Webster NS, Wilson KJ, Blackall LL, Hill RT (2001) Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl Environ Microbiol 67:434–444PubMedGoogle Scholar
  135. Weimer PJ, Waghorn GC, Odt CL et al (1999) Effect of diet on populations of three species of ruminal cellulolytic bacteria in lactating dairy cows. J Dairy Sci 82:122–134PubMedGoogle Scholar
  136. Weisskopf L, Abou-Mansour E, Fromin N et al (2006) White lupin has developed a complex strategy to limit microbial degradation of secreted citrate required for phosphate acquisition. Plant Cell Environ 29:919–927PubMedGoogle Scholar
  137. Weitz JS, Hartman H, Levin SA (2005) Coevolutionary arms races between bacteria and bacteriophage. Proc Natl Acad Sci USA 102:9535–9540PubMedGoogle Scholar
  138. Whipps JM, Hand P, Pink D, Bending GD (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105:1744–1755PubMedGoogle Scholar
  139. Wilkinson DM (2001) Mycorrhizal evolution. Trends Ecol Evol 16:64–65PubMedGoogle Scholar
  140. Wilson EO (1992) The diversity of life. W. W. Norton, New YorkGoogle Scholar
  141. Wostmann BS (1981) The germ-free animal in nutritional studies. Annu Rev Nutr 1:257–297PubMedGoogle Scholar
  142. 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
  143. Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci USA 96:1463–1468PubMedGoogle Scholar
  144. Yang CH, Crowley DE, Borneman J, Keen NT (2001) Microbial phyllosphere populations are more complex than previously realized. Proc Natl Acad Sci USA 98:3889–3894PubMedGoogle Scholar
  145. Yen JH, Barr AR (1971) New hypothesis of the cause of cytoplasmic incompatibility in Culex pipens. Nature 232:657–658PubMedGoogle Scholar
  146. Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735PubMedGoogle Scholar
  147. Zilber-Rosenberg I, Rosenberg E (2011) Prebiotics and probiotics within the framework of the hologenome concept. J Microb Biochem Technol
  148. Zoetendal EG, Akkermans ADL, Akkermans-van Vliet WM et al (2001) A host genotype affects the bacterial community in the human gastrointestinal tract. Microb Ecol Health Dis 13:129–134Google Scholar

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© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Molecular Microbiology and BiotechnologyTel Aviv UniversityTel AvivIsrael
  2. 2.Independant ScholarGivat ShmuelIsrael

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