A complex journey: transmission of microbial symbionts

1. Ewald, P. W. Transmission modes and evolution of the parasitism-mutualism continuum. Ann. N. Y. Acad. Sci. 503, 295–306 (1987).

   Article  CAS  PubMed  Google Scholar 

2. Yamamura, N. Vertical transmission and evolution of mutualism from parasitism. Theor. Popul. Biol. 44, 95–109 (1993).

   Article  Google Scholar 

3. Lipsitsch, M., Siller, S. & Nowak, M. A. The evolution of virulence in pathogens with vertical and horizontal transmission. Evolution 50, 1729–1741 (1996).

   Article  Google Scholar 

4. Yamamura, N. Evolution of mutualistic symbiosis: a differential equation model. Res. Popul. Ecol. 38, 211–218 (1996).

   Article  Google Scholar 

5. Genkai-Kato, M. & Yamamura, N. Evolution of mutualistic symbiosis without vertical transmission. Theor. Popul. Biol. 55, 309–323 (1999).

   Article  CAS  PubMed  Google Scholar 

6. Sharp, K. H., Eam, B., Faulkner, D. J. & Haygood, M. G. Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl. Environ. Microbiol. 73, 622–629 (2007).

   Article  CAS  PubMed  Google Scholar 

7. Steger, D. et al. Diversity and mode of transmission of ammonia-oxidizing archaea in marine sponges. Environ. Microbiol. 10, 1087–1094 (2008).

   Article  CAS  PubMed  Google Scholar 

8. de Bary, A. Die Entstehung der Symbiose (Verlag von Karl, J. Trübner, Strassburg, 1879).

   Google Scholar 

9. McFall-Ngai, M. J. Unseen forces: the influence of bacteria on animal development. Dev. Biol. 242, 1–14 (2002).

   Article  CAS  PubMed  Google Scholar 

10. Hurek, T. & Reinhold-Hurek, B. Azoarcus sp. strain BH72 as a model for nitrogen-fixing grass endophytes. J. Biotechnol. 106, 169–178 (2003).

    Article  CAS  PubMed  Google Scholar 

11. Gage, D. J. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol. Mol. Biol. Rev. 68, 280–300 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

12. Adams, D. G., Bergman, B., Nierzwicki-Bauer, S. A., Rai, A. N. & Schüßler, A. in The Prokaryotes 331–363 (Springer, New York, 2006). This book chapter provides an excellent overview of plant–cyanobacteria symbioses.

13. Jones, K. J., Kobayashi, H., Davies, B. W., Taga, M. E. & Walker, G. C. How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model. Nature Rev. Microbiol. 5, 619–633 (2007). An excellent review of legume–rhizobia symbiosis establishment.

    Article  CAS  Google Scholar 

14. Usher, K. M., Bergman, B. & Raven, J. A. Exploring cyanobacterial mutualisms. 38, 255–273 (2007).

15. Adams, D. G. & Duggan, P. S. Cyanobacteria–bryophyte symbioses. J. Exp. Bot. 59, 1047–1058 (2008).

    Article  CAS  PubMed  Google Scholar 

16. Oldroyd, G. E. D. & Downie, J. A. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59, 519–546 (2008).

    Article  CAS  PubMed  Google Scholar 

17. Taylor, M. W., Radax, R., Steger, D. & Wagner, M. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol. Mol. Biol. Rev. 71, 295–347 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

18. Usher, K. M. The ecology and phylogeny of cyanobacterial symbionts in sponges. Mar. Ecol. 29, 178–192 (2008).

    Article  Google Scholar 

19. Dubilier, N., Bergin, C. & Lott, C. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nature Rev. Microbiol. 6, 725–740 (2008). A scrupulous account of marine chemosynthetic symbioses.

    Article  CAS  Google Scholar 

20. Vrijenhoek, R. C. in Topics in Geobiology. The Vent and Sea Biota. (ed. Kiel, S.) (Springer, Berlin, Germany) (in the press).

21. Herbert, E. E. & Goodrich-Blair, H. Friend and foe: the two faces of Xenorhabdus nematophila. Nature Rev. Microbiol. 5, 634–646 (2007). An outstanding summary of the Steinernema – Xenorhabdus symbiosis.

    Article  CAS  Google Scholar 

22. Clarke, D. J. Photorhabdus: a model for the analysis of pathogenicity and mutualism. Cell. Microbiol. 10, 2159–2167 (2008).

    Article  CAS  PubMed  Google Scholar 

23. Bright, M. & Giere, O. Microbial symbiosis in Annelida. Symbiosis 38, 1–45 (2005).

    Google Scholar 

24. Graf, J., Kikuchi, Y. & Rio, R. V. M. Leeches and their microbiota: naturally simple symbiosis models. Trends Microbiol. 14, 365–371 (2006).

    Article  CAS  PubMed  Google Scholar 

25. Buchner, P. Endosymbiosis of Animals with Plant Microorganisms (Wiley & Sons, New York, 1965). A seminal and exhaustive book on insect symbioses.

    Google Scholar 

26. Douglas, A. E. Mycetocyte symbiosis in insects. Biol. Rev. Camb. Philos. Soc. 64, 409–434 (1989). This is a fine guide to the overwhelming plethora of transmission modes of insect symbionts.

    Article  CAS  PubMed  Google Scholar 

27. Baumann, P. Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59, 155–189 (2005).

    Article  CAS  PubMed  Google Scholar 

28. Dale, C. & Moran, N. A. Molecular interactions between bacterial symbionts and their hosts. Cell 126, 453–465 (2006).

    Article  CAS  PubMed  Google Scholar 

29. Moran, N. A., McCutcheon, J. P. & Nakabachi, A. Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42, 165–190 (2008).

    Article  CAS  PubMed  Google Scholar 

30. Moya, A., Peretó, J., Gil, R. & Latorre, A. Learning how to live together: genomic insights into prokaryote–animal symbioses. Nature Rev. Genet. 9, 218–229 (2008).

    Article  CAS  PubMed  Google Scholar 

31. Nyholm, S. V. & McFall-Ngai, M.J. The winnowing: establishing the squid–Vibrio symbiosis. Nature Rev. Microbiol. 2, 632–642 (2004). A compelling overview of the establishment of the squid– Vibrio spp. symbiosis.

    Article  CAS  Google Scholar 

32. Visick, K. L. & Ruby, E. G. Vibrio fischeri and its host: it takes two to tango. Curr. Opin. Microbiol. 9, 632–638 (2006).

    Article  CAS  PubMed  Google Scholar 

33. Hooper, L. V. & Gordon, J. I. Commensal host-bacterial relationships in the gut. Science 292, 1115–1118 (2001).

    Article  CAS  PubMed  Google Scholar 

34. Sonnenburg, J. L., Angenent, L. T. & Gordon, J. I. Getting a grip on things: how do communities of bacterial symbionts become established in our intestine? Nature Immunol. 5, 569–573 (2004).

    Article  CAS  Google Scholar 

35. Cheesman, S. E. & Guillemin, K. We know you are in there: conversing with the indigenous gut microbiota. Res. Microbiol. 158, 2–9 (2007). This review ponders the parallels between vertebrate microbial mutualisms and the squid– Vibrio spp. symbiosis.

    Article  PubMed  Google Scholar 

36. Ley, R. E., Lozupone, C. A., Hamady, M., Knight, R. & Gordon, J. I. Worlds within worlds: evolution of the vertebrate gut microbiota. Nature Rev. Microbiol. 6, 776–788 (2008).

    Article  CAS  Google Scholar 

37. West, N. & Adams, D. G. Phenotypic and genotypic comparison of symbiotic and free-living cyanobacteria from a single field site. Appl. Environ. Microbiol. 63, 4479–4484 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

38. Costa, J. L., Paulsrud, P., Rikkinen, J. & Lindblad, P. Genetic diversity of Nostoc symbionts endophytically associated with two bryophyte species. Appl. Environ. Microbiol. 67, 4393–4396 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

39. Kikuchi, Y., Hosokawa, T. & Fukatsu, T. Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl. Environ. Microbiol. 73, 4308–4316 (2007). The first report of a horizontally transmitted insect symbiont.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

40. Lee, K.-H. & Ruby, E. G. Detection of the light organ symbiont, Vibrio fischeri, in hawaiian seawater by using lux gene probes. Appl. Environ. Microbiol. 58, 942–947 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

41. Gros, O., Liberge, M., Heddi, A., Khatchadourian, C. & Felbeck, H. Detection of the free-living forms of sulfide-oxidizing gill endosymbionts in the lucinid habitat (Thalassia testdinum environment). Appl. Environ. Microbiol. 69, 6264–6267 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

42. Aida, M. et al. Distribution and population of free-living cells related to endosymbiont A harboured in Oligobrachia mashikoi (a siboglinid polychaete) inhabiting Tsukumo Bay. Microbes Environ. 23, 81–88 (2008).

    Article  PubMed  Google Scholar 

43. Harmer, T. L. et al. Free-living tube worm endosymbionts found at deep-sea vents. Appl. Environ. Microbiol. 74, 3895–3898 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

44. Kiers, E. T., Rousseau, R. A., West, S. A. & Denison, R. F. Host sanctions and the legume-rhizobium mutualism. Nature 425, 78–81 (2003).

    Article  CAS  PubMed  Google Scholar 

45. Salerno, J. L. et al. Characterization of symbiont populations in life-history stages of mussels from chemosynthetic environments. Biol. Bull. 208, 145–155 (2005).

    Article  PubMed  Google Scholar 

46. Callsen-Cencic, P. & Flügel, H. J. Larval development and the formation of the gut of Siboglinum poseidoni Flügel & Langhof (Pogonophora, Perviata). Evidence of protostomian affinity. Sarsia 80, 73–89 (1995).

    Article  Google Scholar 

47. McCann, J., Stabb, E. V., Milikan, D. S. & Ruby, E. G. Population effects of Vibrio fischeri during infection of Euprymna scolopes. Appl. Environ. Microbiol. 69, 5928–5934 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

48. Gros, O., Frenkiel, L. & Moueza, M. Gill filament differentiation and experimental colonization by symbiotic bacteria in aposymbiotic juveniles of Codakia orbicuaris (Bivalvia: Lucinidae). Invertebr. Reprod. Dev. 34, 219–231 (1998).

    Article  Google Scholar 

49. Nussbaumer, A. D., Fisher, C. R. & Bright, M. Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature 441, 345–348 (2006). A groundbreaking study of the acquisition of vestimentiferan symbionts.

    Article  CAS  PubMed  Google Scholar 

50. Bates, J. M. et al. Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation. Dev. Biol. 297, 374–386 (2006).

    Article  CAS  PubMed  Google Scholar 

51. Cooper, J. E. Multiple responses of rhizobia to flavonoids during legume root infection. Adv. Bot. Res. 41, 1–62 (2004).

    Article  CAS  Google Scholar 

52. Brencic, A. & Winans, S. Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol. Mol. Biol. Rev. 69, 155–194 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

53. Robidart, J. C. et al. Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics. Environ. Microbiol. 10, 727–737 (2008).

    Article  CAS  PubMed  Google Scholar 

54. Gros, O., Darrasse, A., Durand, P., Frenkiel, L. & Moueza, M. Environmental transmission of a sulfur-oxidizing bacterial gill endosymbiont in the tropical lucinid bivalve Codakia orbicularis. Appl. Environ. Microbiol. 62, 2324–2330 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

55. Ruby, E. G. & Lee, K.-H. The Vibrio fischeri-Euprymna scolopes light orga. association: current ecological paradigms. Appl. Environ. Microbiol. 64, 805–812 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

56. Stabb, E. V. & Ruby, E. G. Contribution of pilA to competitive colonization of the squid Euprymna scolopes by Vibrio fischeri. Appl. Environ. Microbiol. 69, 820–826 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

57. Adin, D. M. et al. Characterization of htrB and msbB mutants of the light organ symbiont Vibrio fischeri. Appl. Environ. Microbiol. 74, 633–644 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

58. Fauvart, M. & Michiels, J. Rhizobial secreted proteins as determinants of host specificity in the rhizobium-legume symbiosis. FEMS Microbiol. Lett. 285, 1–9 (2008).

    Article  CAS  PubMed  Google Scholar 

59. Aeckersberg, F., Lupp, C., Feliciano, B. & Ruby, E. G. Vibrio fischeri outer membrane protein OmpU plays a role in normal symbiotic colonization. J. Bacteriol. 183, 6590–6597 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

60. Xu, J. et al. A genomic view of the human–Bacteroides thetaiotaomicron symbiosis. Science 299, 2074–2076 (2003).

    Article  CAS  PubMed  Google Scholar 

61. Chun, C. K. et al. Effects of colonization, luminescence, and autoinducer on host transcription during development of the squid-vibrio association. Proc. Natl Acad. Sci. USA. 105, 11323–11328 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

62. Bulgheresi, S., Schabussova, I., Mullin, N. P., Maizels, R. M. & Ott, J. A. A new C-type lectin similar to the human immunoreceptor DC-SIGN mediates symbiont acquisition by a marine nematode. Appl. Environ. Microbiol. 72, 2950–2956 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

63. Gourdine, J. P. & Smith-Ravin, E. J. Analysis of a cDNA-derived sequence of a novel mannose-binding lectin, codakine, from the tropical clam Codakia orbicularis. Fish Shellfish Immunol. 22, 498–509 (2007).

    Article  CAS  PubMed  Google Scholar 

64. Yip, E. S., Grublesky, B. T., Hussa, E. A. & Visick, K. L. A novel, conserved cluster of genes promotes symbiotic colonization and σ54-dependent biofilm formation by Vibrio fischeri. Mol. Microbiol. 57, 1485–1498 (2005).

    Article  CAS  PubMed  Google Scholar 

65. Hussa, E. A., O'Shea, T. M., Darnell, C. L., Ruby, E. G. & Visick, K. L. Two-component response regulators of Vibrio fischeri: identification, mutagenesis, and characterization. J. Bacteriol. 189, 5825–5838 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

66. Mandel, M. J., Wollenberg, M. S., Stabb, E. V., Visick, K. L. & Ruby, E. G. A single regulatory gene is sufficient to alter bacterial host range. Nature 458, 215–218 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

67. Hoang, H. H., Becker, A. & Gonzalez, J. E. The LuxR homolog ExpR, in combination with the Sin quorum sensing system, plays a central role in Sinorhizobium meliloti gene expression. J. Bacteriol. 186, 5460–5472 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

68. Gao, M. et al. sinI- and expR-dependent quorum sensing in Sinorhizobium meliloti. J. Bacteriol. 187, 7931–7944 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

69. Cooper, J. E. Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J. Appl. Microbiol. 103, 1355–1365 (2007).

    Article  CAS  PubMed  Google Scholar 

70. De Hoff, P. L., Brill, L. M. & Hirsch, A. M. Plant lectins: the ties that bind in root symbiosis and plant defense. Mol. Genet. Genomics 282, 1–15 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

71. Fujishige, N. A. et al. Rhizobium common nod genes are required for biofilm formation. Mol. Microbiol. 67, 504–515 (2008).

    Article  CAS  PubMed  Google Scholar 

72. Goormachtig, S., Capoen, W. & Holsters, M. Rhizobium infection: lessons from the versatile nodulation behaviour of water-tolerant legumes. Trends Plant Sci. 9, 518–522 (2004).

    Article  CAS  PubMed  Google Scholar 

73. Bartsev, A. et al. NopL, an effector protein of Rhizobium sp. NGR234, thwarts activation of plant defense reactions. Plant Physiol. 134, 871–879 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

74. Davidson, S. K., Koropatnick, T. A., Kossmehl, R., Sycuro, L. & McFall-Ngai, M. J. NO means 'yes' in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell. Microbiol. 6, 1139–1151 (2004).

    Article  CAS  PubMed  Google Scholar 

75. Moran, N. A. & Dunbar, H. E. Sexual acquisition of beneficial symbionts in aphids. Proc. Natl Acad. Sci. USA 103, 12803–12806 (2006). This is the first report of intraspecific symbiont transfer.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

76. Usher, K. M., Sutton, D. C., Toze, S., Kuo, J. & Fromont, J. Inter-generational transmission of microbial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Mar. Freshw. Res. 56, 125–131 (2005).

    Article  Google Scholar 

77. Serbus, L. R., Casper-Lindley, C., Landmann, F. & Sullivan, W. The genetics and cell biology of Wolbachia-host interactions. Annu. Rev. Genet. 42, 1–25 (2008). A must-read review on Wolbachia spp. transmission and interactions with its host.

    Article  CAS  Google Scholar 

78. Perkins, S. K. & Peters, G. A. The Azolla-Anabaena symbiosis: endophyte continuity in the Azolla life-cycle is facilitated by epidermal trichomes. I. Partitioning of the endophytic Anabaena into developing sporocarps. New Phytol. 123, 53–64 (1993).

    Article  Google Scholar 

79. Werren, J. H., Skinner, S. W., Huger, A. M. Male-killing bacteria in a parasitic wasp. Science 231, 990–992 (1986).

    Article  CAS  PubMed  Google Scholar 

80. Huigens, M. E. et al. Infectious parthenogenesis. Nature 405, 178–179 (2000).

    Article  CAS  PubMed  Google Scholar 

81. Huigens, M. E., de Almeida, R. P., Boons, P. A., Luck, R. F. & Stouthamer, R. Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. Proc. Biol. Sci. 271, 509–515 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

82. Chiel, E. et al. Almost there: transmission routes of bacterial symbionts between trophic levels. PLoS ONE 4, e4767 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

83. Brennan, L. J., Keddie, B. A., Braig, H. R. & Harris, H. L. The endosymbiont Wolbachia pipientis induces the expression of host antioxidant proteins in an Aedes albopictus cell line. PLoS ONE 3, e2083 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

84. Frank, S. A. Host control of symbiont transmission: the separation of symbionts into germ and soma. Am. Nat. 148, 1113–1124 (1996).

    Article  Google Scholar 

85. Dale, C., Plague, G. R., Wang, B., Ochman, H. & Moran, N. A. Type III secretion systems and the evolution of mutualistic endosymbiosis. Proc. Natl Acad. Sci. USA 99, 12397–12402 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

86. Giere, O. & Langheld, C. Structural organisation, transfer and biological fate of endosymbiotic bacteria in gutless oligochaetes. Mar. Biol. 93, 641–650 (1987).

    Article  Google Scholar 

87. Hirose, E. Plant rake and algal pouch of the larvae in the tropical ascidian Diplosoma similis: an adaptation for vertical transmission of photosynthetic symbionts Prochloron sp. Zool. Sci. 17, 233–240 (2000). An exquisite morphological study of ascidian adaptations to symbiont vertical transmission.

    Article  Google Scholar 

88. Hirose, E. & Fukuda, T. Vertical transmission of photosymbionts in the colonial ascidian Didemnum molle: the larval tunic prevents symbionts from attaching to the anterior part of larvae. Zool. Sci. 23, 669–674 (2006).

    Article  Google Scholar 

89. Hirose, E., Adachi, R. & Kuze, K. Sexual reproduction of the Prochloron-bearing ascidians, Trididemnum cyclops and Lissoclinum bistratum, in subtropical waters: seasonality and vertical transmission of photosymbionts. J. Mar. Biolog. Assoc. UK 86, 175–179 (2006).

    Article  Google Scholar 

90. Hirose, E. & Hirose, M. Morphological process of vertical transmission of photosymbionts in the colonial ascidian Trididemnum miniatum Kott, 1977. Mar. Biol. 150, 359–367 (2007).

    Article  Google Scholar 

91. Ereskovsky, A. V. & Boury-Esnault, N. Cleavage pattern in Oscarella species (Porifera, Demospongiae, Homoscleromorpha): transmission of maternal cells and symbiotic bacteria. J. Nat. Hist. 36, 1761–1775 (2002).

    Article  Google Scholar 

92. Kaye, H. R. Sexual reproduction in four Caribbean commercial sponges. II. Oogenesis and transfer of bacterial symbionts. Invertebr. Reprod. Dev. 19, 13–24 (1991).

    Article  Google Scholar 

93. Ereskovsky, A. V., Gonobobleva, E. & Vishnyakov, A. Morphological evidence for vertical transmission of symbiotic bacteria in the viviparous sponge Halisarca dujardini Johnston (Porifera, Demospongiae, Halisarcida). Mar. Biol. 146, 869–875 (2005).

    Article  Google Scholar 

94. Sharp, K. H., Davidson, S. K. & Haygood, M. G. Localization of 'Candidatus Endobugula sertula' and the bryostatins throughout the life cycle of the bryozoan Bugula neritina. ISME J. 1, 693–702 (2007). A first-rate description of the transmission of a bryozoan symbiont.

    Article  PubMed  Google Scholar 

95. Cary, S. C. Vertical transmission of a chemoautotrophic symbiont in the protobranch bivalve, Solemya reidi. Mol. Marine Biol. Biotechnol. 3, 121–130 (1994).

    CAS  Google Scholar 

96. Cary, S. C. & Giovannoni, S. J. Transovarial inheritance of endosymbiotic bacteria in clams inhabiting deep-sea hydrothermal vents and cold seeps. Proc. Natl Acad. Sci. USA 90, 5695–5699 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

97. Endow, K. & Ohta, S. Occurrence of bacteria in the primary oocytes of vesicomyid clam Calyptogena soyoae. Mar. Ecol. Prog. Ser. 64, 309–311 (1990).

    Article  Google Scholar 

98. Eberle, M. W. & McLean, D. L. Initiation and orientation of the symbiote migration in the human body louse Pediculus humanus L. J. Insect Physiol. 28, 417–422 (1982).

    Article  Google Scholar 

99. Eberle, M. W. & McLean, D. L. Observation of symbiote migration in human body lice with scanning and transmission electron microscopy. Can. J. Microbiol. 29, 755–762 (1983). This paper provides some marvellous micrographs of the louse symbionts on their way to the ovaries.

    Article  CAS  PubMed  Google Scholar 

100. Sasaki-Fukatsu, K. et al. Symbiotic bacteria associated with stomach discs of human lice. Appl. Environ. Microbiol. 72, 7349–7352 (2006).

     Article  CAS  PubMed  PubMed Central  Google Scholar 

101. Ciche, T. A., Kim, K.-S. & Kaufmann-Daszczuk, B. Cell invasion and matricide during Photorhabdus luminescens transmission by Heterorhabditis bacteriophora nematodes. Appl. Environ. Microbiol. 74, 2275–2287 (2008). An accurate description of a peculiar and unexpected vertical transmission route.

     Article  CAS  PubMed  PubMed Central  Google Scholar 

102. Brugirard-Ricaud, K. et al. Site-specific antiphagocytic function of the Photorhabdus luminescens type III secretion system during insect colonization. Cell. Microbiol. 7, 363–371 (2005).

     Article  CAS  PubMed  Google Scholar 

103. Martens, E. C. & Goodrich-Blair, H. The Steinernema carpocapsae intestinal vesicle contains a subcellular structure with which Xenorhabdus nematophila associates during colonization initiation. Cell. Microbiol. 7, 1723–1735 (2005).

     Article  CAS  PubMed  Google Scholar 

104. Rio, R. V., Maltz, M., McCormick, B., Reiss, A. & Graf, J. Symbiont succession during the embryonic development of the european medicinal leech, Hirudo verbana. Appl. Environ. Microbiol. 5, 6890–6895 (2009).

     Article  CAS  Google Scholar 

105. Büsing, K.-H., Döll, W. & Freytag, K. Die Bakterienflora der medizinischen medizinischen Blutegel. Arch. Mikrobiol. 19, 52–86 (1953).

     Article  PubMed  Google Scholar 

106. Silver, A. C. et al. Interaction between innate immune cells and a bacterial type III secretion system in mutualistic and pathogenic associations. Proc. Natl Acad. Sci. USA 104, 9481–9486 (2007).

     Article  CAS  PubMed  PubMed Central  Google Scholar 

107. Usher, K. M., Kuo, J., Fromont, J. & Sutton, D. C. Vertical transmission of cyanobacterial symbionts in the marine sponge Chondrilla australiensis (Demospongiae). Hydrobiologia 461, 15–23 (2001).

     Article  Google Scholar 

108. Gottlieb, Y. et al. Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies. FASEB J. 22, 2591–2599 (2008).

     Article  CAS  PubMed  Google Scholar 

109. Miura, T. et al. A comparison of parthenogenetic and sexual embryogenesis of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). J. Exp. Zool. 295B, 59–81 (2003).

     Article  Google Scholar 

110. Mira, A. & Moran, N. A. Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microb. Ecol. 44, 137–143 (2002).

     Article  CAS  PubMed  Google Scholar 

111. Cowles, C. E. & Goodrich-Blair, H. The Xenorhabdus nematophila nilABC genes confer the ability of Xenorhabdus spp. to colonize Steinernema carpocapsae nematodes. J. Bacteriol. 190, 4121–4128 (2008).

     Article  CAS  PubMed  PubMed Central  Google Scholar 

112. Chandra, H., Khandelwal, P., Khattrl, A. & Banerjee, N. Type 1 fimbriae of insecticidal bacterium Xenorhabdus nematophila is necessary for growth and colonization of its symbiotic host nematode Steinernema carpocapsiae. Environ. Microbiol. 10, 1285–1295 (2008).

     Article  CAS  PubMed  Google Scholar 

113. Davidson, S. K. & Stahl, D. A. Selective recruitment of bacteria during embryogenesis of an earthworm. ISME J. 2, 510–518 (2008). This is a high quality account of the symbiont journey to the nephridia of developing earthworms.

     Article  PubMed  Google Scholar 

114. Gustafson, R. G. & Reid, R. G. B. Larval and post-larval morphogenesis in the gutless protobranch bivalve Solemya reidi (Cryptodonta: Solemyidae). Mar. Biol. 97, 373–387 (1988).

     Article  Google Scholar 

115. Gustafson, R. G. & Reid, R. G. B. Association of bacteria with larvae of the gutless protobranch bivalve Solemya reidi (Cryptodonta: Solemyidae). Mar. Biol. 97, 389–401 (1988).

     Article  Google Scholar 

116. Ohta, T. Slightly deleterious mutant substitutions in evolution. Nature 246, 96–98 (1973).

     Article  CAS  PubMed  Google Scholar 

117. Moran, N. A. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc. Natl Acad. Sci. USA 93, 2873–2878 (1996).

     Article  CAS  PubMed  PubMed Central  Google Scholar 

118. Funk, D. J., Wernegreen, J. J. & Moran, N. A. Intraspecific variation in symbiont genomes: bottlenecks and the Aphid-Buchnera association. Genetics 157, 477–489 (2001).

     CAS  PubMed  PubMed Central  Google Scholar 

119. Shigenobu, S., Watanabe, H., Hattori, M., Sakaki, Y. & Ishikawa, H. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407, 81–86 (2000).

     Article  CAS  PubMed  Google Scholar 

120. Rio, R. V. M., Lefevre, C., Heddi, A. & Aksoy, S. Comparative genomics of insect-symbiotic bacteria: influence of host environment on microbial genome composition. Appl. Environ. Microbiol. 69, 6825–6832 (2003).

     Article  CAS  PubMed  PubMed Central  Google Scholar 

121. Woyke, T. et al. Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443, 950–955 (2006).

     Article  CAS  PubMed  Google Scholar 

122. Charles, H., Heddi, A., Guillaud, J., Nardon, C. & Nardon, P. A molecular aspect of symbiotic interactions between the weevil Sitophilus oryzae and its endosymbiotic bacteria: over-expression of a chaperonin. Biochem. Biophys. Res. 239, 769–774 (1997).

     Article  CAS  Google Scholar 

123. Plague, G. R., Dunbar, H. E., Tran, P. L. & Moran, N. A. Extensive proliferation of transposable elements in heritable bacterial symbionts. J. Bacteriol. 190, 777–779 (2008).

     CAS  PubMed  Google Scholar 

124. Mira, A., Ochman, H. & Moran, N. A. Deletional bias and the evolution of bacterial genomes. Trends Genet. 17, 589–596 (2001).

     Article  CAS  PubMed  Google Scholar 

125. Moran, N. A. & Plague, G. R. Genomic changes following host restriction in bacteria. Curr. Opin. Genet. Dev. 14, 627–633 (2004).

     Article  CAS  PubMed  Google Scholar 

126. Gros, O., Liberge, M. & Felbeck, H. Interspecific infection of aposymbiotic juveniles of Codakia orbicularis by various tropical lucinid gill-endosymbionts. Mar. Biol. 142, 57–66 (2003).

     Article  Google Scholar 

127. Kikuchi, Y., Meng, X. Y. & Fukatsu, T. Gut symbiotic bacteria of the genus Burkholderia in the broad-headed bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera: Alydidae). Appl. Environ. Microbiol. 71, 4035–4043 (2005).

     Article  CAS  PubMed  PubMed Central  Google Scholar 

128. Nishiguchi, M. K., Ruby, E. G. & McFall-Ngai, M. J. Competitive dominance among strains of luminous bacteria provides an unusual form of evidence for parallel evolution in sepiolid squid-Vibrio symbioses. Appl. Environ. Microbiol. 64, 3209–3213 (1998).

     CAS  PubMed  PubMed Central  Google Scholar 

129. Won, Y. - J., Jones, W. J. & Vrijenhoek, R. C. Absence of cospeciation between deep-sea mytilids and their thiotrophic endosymbionts. J. Shellfish Res. 27, 129–138 (2008).

     Article  Google Scholar 

130. Goffredi, S. K., Hurtado, L. A., Hallam, S. & Vrijenhoek, R. C. Evolutionary relationships of deep-sea vent and cold seep clams (Mollusca: Vesicomyidae) of the “pacifica/lepta” species complex. Mar. Biol. 142, 311–320 (2003).

     Article  Google Scholar 

131. Hurtado, L. A., Mateos, M., Lutz, R. A. & Vrijenhoek, R. C. Coupling of bacterial endosymbiont and host mitochondrial genomes in the hydrothermal vent clam Calyptogena magnifica. Appl. Environ. Microbiol. 69, 2058–2064 (2003).

     Article  CAS  PubMed  PubMed Central  Google Scholar 

132. Stewart, F. J., Young, C. R. & Cavanaugh, C. M. Lateral symbiont acquisition in a maternally transmitted chemosynthetic clam endosymbiosis. Mol. Biol. Evol. 25, 673–687 (2008).

     Article  CAS  PubMed  Google Scholar 

133. Allen, J. M., Reed, D. L., Perotti, M. A. & Braig, H. R. Evolutionary relationships of “Candidatus Riesia spp.”, endosymbiotic Enterobacteriaceae living within hematophagous primate lice. Appl. Environ. Microbiol. 73, 1659–1664 (2007).

     Article  CAS  PubMed  PubMed Central  Google Scholar 

134. Schramm, A. et al. Acidovorax-like symbionts in the nephridia of earthworms. Environ. Microbiol. 5, 804–809 (2003).

     Article  CAS  PubMed  Google Scholar 

135. Shoemaker, D. D. et al. The distribution of Wolbachia in fig wasps: correlations with host phylogeny, ecology and population structure. Proc. R. Soc. Lond., B, Biol. Sci. 269, 2257–2267 (2002).

     Article  Google Scholar 

136. Kikuchi, Y. & Fukatsu, T. Diversity of Wolbachia endosymbionts in heteropteran bugs. Appl. Environ. Microbiol. 69, 6082–6090 (2003).

     Article  CAS  PubMed  PubMed Central  Google Scholar 

137. Reuter, M. & Keller, L. High levels of multiple Wolbachia infection and recombination in the ant Formica exsecta. Mol. Biol. Evol. 20, 748–753 (2003).

     Article  CAS  PubMed  Google Scholar 

138. Münchhoff, J. et al. Host specificity and phylogeography of the prochlorophyte Prochloron sp., an obligate symbiont in didemnid ascidians. Environ. Microbiol. 9, 890–899 (2007).

     Article  PubMed  CAS  Google Scholar 

139. Blazejak, A., Kuever, J., Erseus, C., Amann, R. & Dubilier, N. Phylogeny of 16S rRNA, ribulose 1, 5-bisphosphate carboxylase/oxygenase, and adenosine 5′-phosphosulfate reductase genes from gamma- and alphaproteobacterial symbionts in gutless marine worms (Oligochaeta) from Bermuda and the Bahamas. Appl. Environ. Microbiol. 72, 5527–5536 (2006).

     Article  CAS  PubMed  PubMed Central  Google Scholar 

140. Lim-Fong, G. E., Regali, L. A. & Haygood, M. G. Evolutionary relationships of “Candidatus Endobugula” bacterial symbionts and their Bugula bryozoan hosts. Appl. Environ. Microbiol. 72, 3605–3609 (2008).

     Article  CAS  Google Scholar 

141. Krueger, D. M., Gustafson, R. G. & Cavanaugh, C. M. Vertical transmission of chemoautotrophic symbionts in the bivalve Solemya velum (Bivalvia: Protobranchia). Biol. Bull. 190, 195–202 (1996).

     Article  CAS  PubMed  Google Scholar 

142. Schmitt, S., Angermeier, H., Schiller, R., Lindquist, N. & Hentschel, U. Molecular microbial diversity survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial symbionts. Appl. Environ. Microbiol. 74, 7694–7708 (2008).

     Article  CAS  PubMed  PubMed Central  Google Scholar 

143. Davidson, S. K. & Stahl, D. A. Transmission of nephridial bacteria of the earthworm Eisenia fetida. Appl. Environ. Microbiol. 72, 769–775 (2006).

     Article  CAS  PubMed  PubMed Central  Google Scholar 

144. Perotti, M. A., Allen, J. M., Reed, D. L. & Braig, H. R. Host-symbiont interactions of the primary endosymbiont of human head and body lice. FASEB J. 21, 1058–1066 (2007).

     Article  CAS  PubMed  Google Scholar 

145. Nardon, P. Contribution à l'ètude des symbiotes ovaries de Sitophilus sasakii: localisation, histochimie et ultrastructure chez la femelle adults. C. R. Acad. Sci. III, Sci. 272, 2975–2978 (1971).

     Google Scholar 

146. Meeks, J. C. et al. An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosyn. Res. 70, 85–106 (2001).

     Article  CAS  Google Scholar 

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