Chapter 9 : Experimental Models of Symbiotic Host-Microbial Relationships: Understanding the Underpinnings of Beneficence and the Origins of Pathogenesis

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Experimental Models of Symbiotic Host-Microbial Relationships: Understanding the Underpinnings of Beneficence and the Origins of Pathogenesis, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555815622/9781555813000_Chap09-1.gif /docserver/preview/fulltext/10.1128/9781555815622/9781555813000_Chap09-2.gif


The study of beneficial associations of plants and animals with microorganisms is in its infancy. This chapter describes the very beginnings of a characterization. The understandable historical focus on determining the basis of devastating pathogenic diseases, as well as technical impediments to studying the dynamic and complex interactions between microbial communities and their hosts, have hindered one's ability to obtain an accurate understanding of the relationships of animals and plants with the microbial world. Studies of mutants in rhizobia indicate that components of the symbiont’s lipopolysaccharide (LPS) are also important in inducing normal infection thread formation and the eventual release of the symbionts into host cortical cells. Overall, a remarkable number of host mechanisms used to avoid infection by pathogenic microbes, such as production of reactive oxygen species (ROS) and “antimicrobial” proteins and peptides, appear to play significant roles in the legume-rhizobium (LR) and squid-vibrio (SV) associations. Taken together, the available data on the LR and SV symbioses suggest that interactions between the partners involve molecules traditionally associated with host defense, although they appear to be modulated differently in these beneficial associations. Studies of the coevolution and coadaptation of humans and their microbial communities present an opportunity to gain new understanding about how our ancient migrations, dietary changes, and social innovations helped shaped our current biology, and how they influenced the origins of, our susceptibilities to, and the spread of various pathogenic symbioses.

Citation: McFall-Ngai M, Gordon J. 2006. Experimental Models of Symbiotic Host-Microbial Relationships: Understanding the Underpinnings of Beneficence and the Origins of Pathogenesis, p 147-166. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch9
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

Symbiont-induced development of the host tissues in the squid-vibrio association. (Upper left) Diagram of a ventral dissection of a newly hatched , revealing the position of the light organ in the animal’s body cavity (dashed line to an expanded view of the organ). (Upper half, light organ surface) Each complex ciliated field on the lateral surface of the organ is composed of an anterior appendage (aa) and a posterior appendage (pa), which are single layers of epithelial cells overlying a blood sinus (bs). At the base of these appendages is a ciliated field that surrounds the three pores (p) where the symbionts will enter host tissues. This ciliated epithelium serves two functions: the beat of the cilia entrains environmental bacteria into the vicinity of the pores, and the cells of the field secrete mucus in which symbionts will be harvested. Both nonspecific environmental bacteria and bacterial symbionts induce a series of dramatic alterations in this superficial ciliated epithelium in the hours to days following hatching of the host from the egg. First ( ), interactions with nonspecific environmental bacteria and their associated peptidoglycan induce mucus shedding from the ciliated epithelium. Gram-negative bacteria begin to aggregate in this mucus and, concomitantly, macrophagelike hemocytes traffic into the blood sinuses underlying the superficial epithelium. In a second phase ( ), symbiont cells () become numerically dominant in the mucus. They then enter pores on the organ surface (arrow) and travel down ducts (d) into crypts (c), where the symbiont population grows to fill to the crypt spaces. Hemocyte number continues to increase in the blood sinuses, and the first signs of apoptosis in the ciliated epithelium occur around the time that the aggregated symbionts are in the ducts of the organ. Once inside the crypt spaces ( ), cells induce regression of the superficial ciliated epithelium of the light organ, which is remote from the population of colonizing symbionts. By 12 hours, a large proportion of the epithelial cells are undergoing apoptosis, and the blood sinus is filled with hemocytes. Upon continued colonization of the crypts with symbionts ( ), further mucus production and harvesting of symbionts ceases, although this behavior can be restored by antibiotic-curing the light organ of its symbionts. By 4 to 5 days following colonization ( ), the ciliated epithelium of the light organ has been completely lost. The lipopolysaccharide (LPS) and peptidoglycan (PGN) of the symbiont act synergistically to induce the complete regression of these ciliated fields. (Lower half, light organ interior) In response to interactions with the symbionts, the ducts constrict, a behavior that can be mimicked by exposure to PGN alone. The crypt cells exhibit a dramatic increase in the density of the microvilli. In addition, they show a fourfold increase in volume in response to interactions with the symbiont. mutants defective in light production do not induce cell swelling and are incapable of maintaining a persistent normal symbiosis.

Citation: McFall-Ngai M, Gordon J. 2006. Experimental Models of Symbiotic Host-Microbial Relationships: Understanding the Underpinnings of Beneficence and the Origins of Pathogenesis, p 147-166. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch9
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Composite of characters shared between mutualistic and pathogenic symbiotic associations. In both types of associations, the bacterial partners may have genomic elements that are involved in the dynamics of the symbiosis, including plasmids (sym), phages (ph), genomic (pathogenicity) islands (gi), transposons (tp), and mobilization loci (mob). In addition, the induction of similar, if not homologous, mechanisms for sensing and responding to the environment have been reported, including two-component regulatory systems (tcr), iron acquisition (Fe), and specific outer membrane proteins (omp), and autoinducers (ai) that enable the bacteria to sense and respond to being at high population density. The bacterial partner may interact directly with the host cells through conserved bacterial surface molecules such as lipopolysaccharide (LPS) and peptidoglycan (PGN), and/or through more specific exopolysaccharides (EPS), a type III secretion system (tss), lectins (le), or fimbriae (fim). Studies thus far on host cells demonstrate shared responses to mutualistic or pathogenic associations. In a number of cases, various bacterial ligands have been shown to interact with receptor proteins on host cell surfaces that include an extracellular leucine-rich repeat domain (LRR), a transmembrane domain (tm), and a kinase domain (kd). Circumstantial evidence exists that signal transduction pathways similar to the NF-КB and JAK/STAT pathways, which mediate responses to pathogens, are also present in beneficial associations. Reactive oxygen species, including nitric oxide (NO), hydrogen peroxide (HO), and hypohalous acid (HOCl), are host molecules also involved in the communication between host and symbiont in both beneficial and pathogenic associations.

Citation: McFall-Ngai M, Gordon J. 2006. Experimental Models of Symbiotic Host-Microbial Relationships: Understanding the Underpinnings of Beneficence and the Origins of Pathogenesis, p 147-166. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch9
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Aiello, L. C., and, P. Wheeler. 1995. The expensive-tissue hypothesis. Curr. Anthropol. 36: 199221.
2. Berg, R. 1996. The indigenous gastrointestinal microflora. Trends Microbiol. 4: 430435.
3. Bry, L.,, P. G. Falk,, T. Midtvedt, and, J. I. Gordon. 1996. A model of host-microbial interactions in an open mammalian ecosystem. Science 273: 13801383.
4. Cano, R. J.,, F. Tiefenbrunner,, M. Ubaldi,, C. del Cueto,, S. Luciani,, T. Cox,, P. Orkand,, K. H. Kunzel, and, F. Rollo. 2000. Sequence analysis of bacterial DNA in the colon and stomach of the Tyrolean iceman. Am. J. Phys. Anthropol. 112: 297309.
5. Capela, D.,, F. Barloy-Hubler,, J. Gouzy,, G. Bothe,, F. Ampe,, J. Batut,, P. Boistard,, A. Becker,, M. Boutry,, E. Cadieu,, S. Dreano,, S. Gloux,, T. Godrie,, A. Goffeau,, D. Kahn,, E. Kiss,, V. Lelaure,, D. Masuy,, T. Pohl,, D. Portetelle,, A. Puhler,, B. Purnelle,, U. Ramsperger,, C. Renard,, P. Thebault,, M. Vandenbol,, S. Weidner, and, F. Galibert. 2001. Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti strain 1021. Proc. Natl. Acad. Sci. USA 98: 98779882.
6. Cary, S. C., and, S. J. Giovannoni. 1993. Transovarial inheritance of endosymbiotic bacteria in clams inhabiting deep-sea hydrothermal vents and cold seeps. Proc. Natl. Acad. Sci. USA 90: 56955699.
7. Ciesiolka, L. D.,, T. Hwin,, J. D. Gearlds,, G. V. Minsavage,, R. Saenz,, M. Bravo,, V. Handley,, S. M. Conover,, H. Zhang,, J. Caporgno,, N. B. Phengrasamy,, A. O. Toms,, R. E. Stall, and, M. C. Whalen. 1999. Regulation of expression of avirulence gene avrRxv and identification of a family of host interaction factors by sequence analysis of avrBsT. Mol. Plant Microbe Interact. 12: 3544.
8. Cossart, P.,, S. Boquet,, S. Normark, and, R. Rappuoli (ed.). 2000. Cellular Microbiology. ASM Press, Washington, D. C.
9. Dale, C.,, G. R. Plague,, B. Wang,, H. Ochman, and, N. Moran. 2002. Type III secretion systems and the evolution of mutualistic endosymbioses. Proc. Natl. Acad. Sci. USA 99: 1239712402.
10. Davidson, S. K.,, T. A. Koropatnick,, R. Kossmehl,, L. Sycuro, and, M. J. McFall-Ngai. 2004. NO means ‘yes’ in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell Microbiol. 6: 11391151.
11. Dazzo, F. B.,, G. L. Truchet,, R. I. Hollingsworth,, E. M. Hrabak,, H. S. Pankratz,, S. Philip-Hollingsworth,, J. L. Salzwedel,, K. Chapman,, L. Appenzeller, and, A. Squartini. 1991. Rhizobium lipopolysaccharide modulates infection thread development in white clover root hairs. J. Bacteriol. 173: 53715384.
12. Distel, D. L.,, H. K.-W. Lee, and, C. M. Cavanaugh. 1995. Intracellular coexistence of methano- and thioautotrophic bacteria in a hydrothermal vent mussel. Proc. Natl. Acad. Sci. USA 92: 95989602.
13. Doino J. A., and, M. J. McFall-Ngai. 1995. A transient exposure to symbiosis-competent bacteria induces light organ morphogenesis in the host squid. Biol. Bull. 189: 347355.
14. Douglas, A. E. 1989. Mycetocyte symbiosis in insects. Biol. Rev. 69: 409434.
15. Douglas, A. E. 1997. Parallels and contrasts between symbiotic bacteria and bacterial-derived organelles: evidence from Buchnera, the bacterial symbiont of aphids. FEMS Microbiol. Ecol. 24: 19.
16. Douglas, A. E. 1994. Symbiotic Interactions. Oxford University Press, Oxford, United Kingdom.
17. Downie, J. A., and, M. Parniske. 2002. Fixation with regulation. Nature 420: 369370.
18. Doyle, J. J. 1994. Phylogeny of the legume family: an approach to understanding the origin of nodulation. Annu. Rev. Ecol. Syst. 25: 325349.
19. Falush, D.,, T. Wirth,, B. Linz,, J. K. Pritchard,, M. Stephens,, M. Kidd,, M. J. Blaser,, D. Y. Graham,, S. Vacher,, G. I. Perez-Perez,, Y. Yamaoka,, F. Megraud,, K. Otto,, U. Reichard,, E. Katzowitsch,, X. Wang,, M. Achtman, and, S. Suerbaum. 2003. Traces of human migrations in Helicobacter pylori populations. Science 299: 15821585.
20. Favier, C. F.,, E. E. Vaughan,, W. M. De Vos, and, A. D. L. Akkermans. 2002. Molecular monitoring of succession of bacterial communities in human neonates. Appl. Environ. Microbiol. 68: 219236.
21. Gagneux, P., and, A. Varki. 1999. Evolutionary considerations in relating oligosaccharide diversity to biological function. Glycobiology 9: 747755.
22. Girardin, S. E.,, I. G. Boneca,, J. Viala,, M. Chamaillard,, A. Labigne,, G. Thomas,, D. J. Philpott, and, P. J. Sansonetti. 2003. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem. 278: 88698872.
23. Goosen-de Roo, L.,, R. A. de Maagd, and, B. J. Lugtenberg. 1991. Antigenic changes in lipopolysaccharide I of Rhizobium leguminosarum bv. viciae in root nodules of Vicia sativa subsp. nigra occur during release from infection threads. J. Bacteriol. 173: 31773183.
24. Graf, J.,, P. V. Dunlap, and, E. G. Ruby. 1994. Effect of transposon-induced motility mutations on colonization of the host light organ by Vibrio fischeri. J. Bacteriol. 176: 69866991.
25. Graf, J., and, E. G. Ruby. 1998. Characterization of the nutritional environment of a symbiotic light organ using bacterial mutants and chemical analyses. Proc. Natl. Acad. Sci. USA 95: 18181822.
26. Gualtieri, G., and, T. Bisseling. 2000. The evolution of nodulation. Plant Mol. Biol. 42: 181194.
27. Hampe, J.,, A. Cuthbert,, P. J. Croucher,, M. M. Mirza,, S. Mascheretti,, S. Fisher,, H. Frenzel,, K. King,, A. Hasselmeyer,, A. J. MacPherson,, S. Bridger,, S. van Deventer,, A. Forbes,, S. Nikolaus,, J. E. Lennard-Jones,, U. R. Foelsch,, M. Krawczak,, C. Lewis,, S. Schreiber, and, C. G. Mathew. 2001. Association between insertion mutation in NOD2 gene and Crohn’s disease in German and British populations. Lancet 357: 19251928.
28. Haygood, M. G., and, S. K. Davidson. 1997. Small-subunit rRNA genes and in situ hybridization with oligonucleotides specific for the bacterial symbionts in the larvae of the bryozoan Bugula neritina and proposal of “ Candidatus endobugula sertula”. Appl. Environ. Microbiol. 63: 46124616.
29. Helmann, J. D. 2002. The extracytoplasmic function (ECF) sigma factors. Adv. Microb. Physiol. 46: 47110.
30. Henderson, B.,, M. Wilson,, R. McNab, and, A. J. Lax. 1999. Cellular Microbiology. Bacteria-Host Interactions in Health and Disease. Wiley and Sons, Chicester, United Kingdom.
31. Hentschel, U., and, J. Hacker. 2001. Pathogenicity islands: the tip of the iceberg. Microbes Infect. 3: 545548.
32. Hentschel, U.,, M. Steinert, and, J. Hacker. 2000. Common molecular mechanisms of symbiosis and pathogenesis. Trends Microbiol. 8: 226231.
33. Hirsch, A., and, M. J. McFall-Ngai. 2000. Fundamental concepts in symbiotic interactions. J. Plant Growth Regul. 19: 113130.
34. Hooper, L., and, J. I. Gordon. 2001. Glycans as legislators of host-microbial interactions: spanning the spectrum from symbiosis to pathogenicity. Glycobiology 11: 1R10R.
35. Hooper, L.,, M. Wong,, A. Thelin,, L. Hansson,, P. Falk, and, J. I. Gordon. 2001. Molecular analysis of commensal host-microbial relationships in the intestine. Science 291: 881884.
36. Hooper, L. V.,, T. Midtvedt, and, J. I. Gordon. 2002. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu. Rev. Nutr. 22: 283307.
37. Hooper, L. V.,, J. C. Mills,, K. A. Roth,, T. S. Stappenbeck,, M. H. Wong, and, J. I. Gordon. 2002. Combining gnotobiotic mouse models with functional genomics to define the impact of the microflora on host physiology. Methods Microbiol. 31: 559589.
38. Hooper, L. V.,, T. S. Stappenbeck,, C. V. Hong, and, J. I. Gordon. 2003. Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat. Immunol. 4: 269273.
39. Hooper, L. V.,, J. Xu,, P. G. Falk,, T. Midtvedt, and, J. I. Gordon. 1999. A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. Proc. Natl. Acad. Sci. USA 96: 98339838.
40. Hughes, D. S.,, H. Felbeck, and, J. L. Stein. 1997. A histidine protein kinase homolog from the endosymbiont of the hydrothermal vent tube-worm Riftia pachyptila. Appl. Environ. Microbiol. 63: 34943498.
41. Hugot, J. P.,, M. Chamaillard,, H. Zouali,, S. Lesage,, J. P. Cezard,, J. Belaiche,, S. Almer,, C. Tysk,, C. A. O’Morain,, M. Gassull,, V. Binder,, Y. Finkel,, A. Cortot,, R. Modigliani,, P. Laurent-Puig,, C. Gower-Rousseau,, J. Macry,, J. F. Colombel,, M. Sahbatou, and, G. Thomas. 2001. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn’s disease. Nature 411: 599603.
42. Inohara, N.,, Y. Ogura, and, G. Nunez. 2002. Nods: a family of cytosolic proteins that regulate the host response to pathogens. Curr. Opin. Micro-biol. 5: 7680.
43. Kaneko, T.,, Y. Nakamura,, S. Sato,, E. Asamizu,, T. Kato,, S. Sasamoto,, A. Watanabe,, K. Idesawa,, A. Ishikawa,, K. Kawashima,, T. Kimura,, Y. Kishida,, C. Kiyokawa,, M. Kohara,, M. Matsumoto,, A. Matsuno,, Y. Mochizuki,, S. Nakayama,, N. Nakazaki,, S. Shimpo,, M. Sugimoto,, C. Takeuchi,, M. Yamada, and, S. Tabata. 2000. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res. 7: 331338.
44. Kimbell, J. R., and, M. J. McFall-Ngai. 2002. Symbiont-induced changes in host cytoskeletal actin. Mol. Biol. Cell. Suppl. 13: 450a.
45. Koropatnick, T. A.,, J. T. Engle,, M. A. Apicella,, E. V. Stabb,, W. E. Goldman, and, M. J. McFallNgai. 2004. Microbial factor-mediated development in a host-bacterial mutualism. Science 306: 11861188.
46. Krueger, D. M., and, C. M. Cavanaugh. 1997. Phylogenetic diversity of bacterial symbionts of Solemya hosts based on comparative sequence analysis of 16S rRNA genes. Appl. Environ. Micro-biol. 63: 9198.
47. Krueger, D. M.,, R. G. Gustafson, and, C. M. Cavanaugh. 1996. Vertical transmission of chemoautotrophic symbionts in the bivalve Solemya velum (Bivalvia: Protobranchia). Biol. Bull. 190: 195202.
48. Leonard, W. R. 2002. Food for thought: dietary change was a driving force in human evolution. Sci. Am. 287: 108115.
49. Lum, M. R. and, A. M. Hirsch. 2003. Roots and their symbiotic microbes: strategies to obtain nitrogen and phosphorus in a nutrient-limiting environment. J. Plant Growth Regul. 21: 368382.
50. Mackie, R. I.,, A. Sghir, and, H. R. Gaskins. 1999. Developmental microbial ecology of the neonatal gastrointestinal tract. Am. J. Clin. Nutr. 69: 1035S1045S.
51. Margulis, L. 1970. Origin of Eukaryotic Cells. Yale University Press, New Haven, Conn.
52. Margulis, L., and, R. Fester (ed.). 1991. Symbiosis as a Source of Evolutionary Innovation. The MIT Press, Cambridge, Mass.
53. McFall-Ngai, M.,, C. Brennan,, V. Weis, and, L. Lamarcq. 1998. Mannose adhesin-glycan interactions in the Euprymna scolopes-Vibrio fischeri symbiosis, p. 273–277. In Y. LeGal and, H. O. Halvorson (ed.), New Developments in Marine Biology. Plenum Publishing Co., New York, N. Y.
54. McFall-Ngai, M. J. 2001. Identifying prime suspects: symbioses and the evolution of multicellularity. Comp. Biochem. Physiol. 129: 711723.
55. Montgomery, M. K., and, M. J. McFall-Ngai. 1993. Embryonic development of the light organ of the sepiolid squid Euprymna scolopes Berry. Biol. Bull. 184: 296308.
56. Moore, W. E., and, L. V. Holdeman. 1974. Human fecal flora: the normal flora of 20 Japanese-Hawaiians. Appl. Microbiol. 27: 961979.
57. Moran, N. A. 2002. Microbial minimalism: genome reduction in bacterial pathogens. Cell 108: 583586.
58. Nishiguchi, M. K.,, E. G. Ruby, and, M. J. McFall-Ngai. 1998. Competitive dominance among strains of luminous bacteria provides an unusual form of evidence for parallel evolution in the sepiolid squid-vibrio symbioses. Appl. Environ. Microbiol. 64: 32093213.
59. Nyholm, S. V.,, B. Deplancke,, H. R. Gaskins,, M. A. Apicella, and, M. J. McFall-Ngai. 2002. Roles of Vibrio fischeri and nonsymbiotic bacteria in the dynamics of mucus secretion during symbiont colonization of the Euprymna scolopes light organ. Appl. Environ. Microbiol. 68: 51135122.
60. Nyholm, S. V., and, M. J. McFall-Ngai. 2003. Dominance of Vibrio fischeri in secreted mucus outside the light organ of Euprymna scolopes: the first site of symbiont specificity. Appl. Environ. Microbiol. 69: 39323937.
61. Nyholm, S. V., and, M. J. McFall-Ngai. 2004. The winnowing: establishing the squid-vibrio symbiosis. Nat. Rev. Microbiol. 2: 632642.
62. Nyholm, S. V.,, E. V. Stabb,, E. G. Ruby, and, M. J. McFall-Ngai. 2000. Harvesting symbiotic vibrios: imposing a magnet on the environmental haystack. Proc. Natl. Acad. Sci. USA 97: 1023110294.
63. Ogura, Y.,, D. K. Bonen,, N. Inohara,, D. L. Nicolae,, F. F. Chen,, R. Ramos,, H. Britton,, T. Moran,, R. Karaliuskas,, R. H. Duerr,, J. P. Achkar,, S. R. Brant,, T. M. Bayless,, B. S. Kirschner,, S. B. Hanauer,, G. Nunez, and, J. H. Cho. 2001. A frameshift mutation in NOD2 associated with susceptibility to Crohn’s disease. Nature 411: 603606.
64. Perret, X.,, C. Staehelin, and, W. J. Broughton. 2000. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64: 180201.
65. Ruby, E. G., and, M. J. McFall-Ngai. 1999. The many roles of oxygen in the symbiotic bacterial colonization of an animal epithelium. Trends Microbiol. 7: 414419.
66. Salyers, A. A.,, G. Bonheyo, and, N. B. Shoemaker. 2000. Starting a new genetic system: lessons from bacteroides. Methods 20: 3546.
67. Savage, D. C. 1977. Microbial ecology of the gastrointestinal tract. Annu. Rev. Microbiol. 31: 107133.
68. Smith, S. E., and, F. A. Read. 1997. Mycorrhizal Symbiosis. Academic Press, London, United Kingdom.
69. Stougaerd, J. 2000. Regulators and regulation of legume root nodule development. Plant Physiol. 124: 532539.
70. Trench, R. K. 1987. Dinoflagellates in non-parasitic symbioses, p. 530–570. In F. J. R. Taylor (ed.), The Biology of Dinoflagellates. Blackwell Scientific Publishers, Oxford, United Kingdom.
71. Turelli, M., and, A. A. Hoffmann. 1991. Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353: 440442.
72. Van Rhijn, P., and, J. Vanderleyden. 1995. The Rhizobium-plant symbiosis. Microbiol. Rev. 59: 124142.
73. Visick, K. L.,, J. S. Foster,, J. Doino Lemus,, M. J. McFall-Ngai, and, E. G. Ruby. 2000. Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J. Bacteriol. 182: 45784586.
74. Visick, K. L., and, M. J. McFall-Ngai. 2000. An exclusive contract: specificity in the Vibrio fischeri-Euprymna scolopes partnership. J. Bacteriol. 182: 17791787.
75. Woollacott, R. M. 1981. Association of bacteria with bryozoan larvae. Mar. Biol. 65: 155158.
76. Xu, J.,, M. K. Bjursell,, J. Himrod,, S. Deng,, L. K. Carmichael,, H. C. Chiang,, L. V. Hooper, and, J. I. Gordon. 2003. A genomic view of the human- Bacteroides thetaiotaomicron symbiosis. Science 299: 20742076.
77. Xu, J., and, J. I. Gordon. 2003. Honor thy symbionts. Proc. Natl. Acad. Sci. USA 100: 1045210459.
78. Yachi, S., and, M. Loreau. 1999. Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc. Natl. Acad. Sci. USA 96: 14631468.
79. Zoetendal, E. G.,, A. D. L. Akkermans,, W. M. Akkermans-van Vliet,, J. A. G. M. deVisser, and, W. M. deVos. 2001. The host genotype affects the bacterial community in the human gastrointestinal tract. Microb. Ecol. Health Dis. 13: 129134.


Generic image for table

The types of symbioses based on the effect of the association on the fitness of the partners

Citation: McFall-Ngai M, Gordon J. 2006. Experimental Models of Symbiotic Host-Microbial Relationships: Understanding the Underpinnings of Beneficence and the Origins of Pathogenesis, p 147-166. In Seifert H, DiRita V (ed), Evolution of Microbial Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815622.ch9

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error