Evolutionary transitions in bacterial symbiosis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue SUPPL. 2, 2011, Pages 10800-10807

  Sachs, Joel L ^a   Skophammer, Ryan G ^a   Regus, John U ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Conflict; Cooperation; Endosymbiont; Major transition; Phylogeny

Indexed keywords

BACTERIUM; CONFERENCE PAPER; EUKARYOTE; EVOLUTIONARY ADAPTATION; HOST PATHOGEN INTERACTION; NONHUMAN; PRIORITY JOURNAL; SYMBIONT; SYMBIOSIS;

BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 79960639613     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1100304108     Document Type: Article

References (116)

1. Merhej V, Royer-Carenzi M, Pontarotti P, Raoult D (2009) Massive comparative genomic analysis reveals convergent evolution of specialized bacteria. Biol Direct 4:13.
2. Carvalho FM, Souza RC, Barcellos FG, Hungria M, Vasconcelos ATR (2010) Genomic and evolutionary comparisons of diazotrophic and pathogenic bacteria of the order Rhizobiales. BMC Microbiol 10:37.
3. Medina M, Sachs JL (2010) Symbiont genomics, our new tangled bank. Genomics 95: 129-137.
4. Toft C, Andersson SGE (2010) Evolutionary microbial genomics: Insights into bacterial host adaptation. Nat Rev Genet 11:465-475.
5. Sagan L (1967) On the origin of mitosing cells. J Theor Biol 14:255-274.
6. Stouthamer R, Breeuwer JAJ, Hurst GDD (1999) Wolbachia pipientis: Microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53:71-102. (Pubitemid 29503726)
7. Buchner P (1921) Tier Und Pflanze in Intracellular Symbiose (Borntraeger, Berlin).
8. Sachs JL, Essenberg CJ, Turcotte MM (2011) New paradigms for the evolution of beneficial infections. Trends Ecol Evol 26:202-209.
9. Wu DY, et al. (2009) A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462:1056-1060.
10. Williams KP, Sobral BW, Dickerman AW (2007) A robust species tree for the alphaproteobacteria. J Bacteriol 189:4578-4586. (Pubitemid 47025569)
11. Williams KP, et al. (2010) Phylogeny of gammaproteobacteria. J Bacteriol 192: 2305-2314.
12. Philippot L, et al. (2010) The ecological coherence of high bacterial taxonomic ranks. Nat Rev Microbiol 8:523-529.
13. Szathmáry E, Smith JM (1995) The major evolutionary transitions. Nature 374: 227-232.
14. Nyholm SV, McFall-Ngai MJ (2004) The winnowing: Establishing the squid-vibrio symbiosis. Nat Rev Microbiol 2:632-642.
15. Becking JH (1970) Plant-endophyte symbiosis in non-leguminous plants. Plant Soil 32:611-654.
16. Savage DC (1977) Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 31:107-133.
17. Sprent JI, Sutherland JM, Faria SM (1987) Some aspects of the biology of nitrogen-fixing organisms. Philos Trans R Soc Lond B Biol Sci 317:111-129.
18. Bright M, Sorgo A (2003) Ultrastructural reinvestigation of the trophosome in adults of Riftia pachyptila (Annelida, Siboglinidae). Invertebr Biol 122:347-368. (Pubitemid 38002740)
19. Currie CR, Poulsen M, Mendenhall J, Boomsma JJ, Billen J (2006) Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants. Science 311:81-83. (Pubitemid 43063062)
20. Douglas AE (1989) Mycetocyte symbiosis in insects. BiolRevCambPhilos Soc 64:409-434.
21. Nussbaumer AD, Fisher CR, Bright M (2006) Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature 441:345-348. (Pubitemid 44050198)
22. Visick KL, Ruby EG (2006) Vibrio fischeri and its host: it takes two to tango. Curr Opin Microbiol 9:632-638. (Pubitemid 44791984)
23. Goettler W, Kaltenpoth M, Herzner G, Strohm E (2007) Morphology and ultrastructure of a bacteria cultivation organ: the antennal glands of female European beewolves, Philanthus triangulum (Hymenoptera, Crabronidae). Arthropod Struct Dev 36:1-9. (Pubitemid 44880007)
24. Vaishnava S, Behrendt CL, Ismail AS, Eckmann L, Hooper LV (2008) Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal hostmicrobial interface. Proc Natl Acad Sci USA 105:20858-20863.
25. Pflugfelder B, Cary SC, Bright M (2009) Dynamics of cell proliferation and apoptosis reflect different life strategies in hydrothermal vent and cold seep vestimentiferan tubeworms. Cell Tissue Res 337:149-165.
26. Ran LA, et al. (2010) Genome erosion in a nitrogen-fixing vertically transmitted endosymbiotic multicellular cyanobacterium. PLoS ONE 5:e11486.
27. Hirose E (2000) Plant rake and algal pouch of the larvae in the tropical ascidian Diplosoma similis: An adaptation for vertical transmission of photosynthetic symbionts Prochloron sp. Zoolog Sci 17:233-240.
28. Hirose E, Neilan BA, Schmidt EW, Murakami A (2009) Enigmatic life and evolution of Prochloron and related cyanobacteria inhabiting colonial ascidians. Handbook on Cyanobacteria: Biochemistry, Biotechnology and Applications, eds Gault PM, Marler HJ (Nova Science, Hauppauge, NY), pp 161-189.
29. Kaltenpoth M, Winter SA, Kleinhammer A (2009) Localization and transmission route of Coriobacterium glomerans, the endosymbiont of pyrrhocorid bugs. FEMS Microbiol Ecol 69:373-383.
30. Hooper LV, Midtvedt T, Gordon JI (2002) How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 22:283-307. (Pubitemid 35221463)
31. Currie CR, Scott JA, Summerbell RC, Malloch D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398:701-704. (Pubitemid 29197647)
32. Kaltenpoth M, Göttler W, Herzner G, Strohm E (2005) Symbiotic bacteria protect wasp larvae from fungal infestation. Curr Biol 15:475-479. (Pubitemid 40323536)
33. Kost C, et al. (2007) Non-specific association between filamentous bacteria and fungus-growing ants. Naturwissenschaften 94:821-828. (Pubitemid 47367669)
34. Oliver KM, Campos J, Moran NA, Hunter MS (2008) Population dynamics of defensive symbionts in aphids. Proc Biol Sci 275:293-299. (Pubitemid 350295705)
35. Heath KD, Stock AJ, Stinchcombe JR (2010) Mutualism variation in the nodulation response to nitrate. J Evol Biol 23:2494-2500.
36. Weeks AR, Turelli M, Harcombe WR, Reynolds KT, Hoffmann AA (2007) From parasite to mutualist: Rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol 5:e114.
37. Sachs JL, Ehinger MO, Simms EL (2010) Origins of cheating and loss of symbiosis in wild Bradyrhizobium. J Evol Biol 23:1075-1089.
38. Frank SA (1996) Host-symbiont conflict over the mixing of symbiotic lineages. Proc Biol Sci 263:339-344.
39. Frank SA (1996) Host control of symbiont transmission: The separation of symbionts into germ and soma. Am Nat 148:1113-1124.
40. Sachs JL, Wilcox TP (2006) A shift to parasitism in the jellyfish symbiont Symbiodinium microadriaticum. Proc Biol Sci 273:425-429. (Pubitemid 46780549)
41. Simms EL, et al. (2006) An empirical test of partner choice mechanisms in a wild legume-rhizobium interaction. Proc Biol Sci 273:77-81. (Pubitemid 46768048)
42. Boussau B, Karlberg EO, Frank AC, Legault BA, Andersson SGE (2004) Computational inference of scenarios for alpha-proteobacterial genome evolution. Proc Natl Acad Sci USA 101:9722-9727. (Pubitemid 38869303)
43. Bright M, Bulgheresi S (2010) A complex journey: Transmission of microbial symbionts. Nat Rev Microbiol 8:218-230.
44. Heath KD, Tiffin P (2007) Context dependence in the coevolution of plant and rhizobial mutualists. Proc Biol Sci 274:1905-1912. (Pubitemid 47377909)
45. Moran NA, Wernegreen JJ (2000) Lifestyle evolution in symbiotic bacteria: Insights from genomics. Trends Ecol Evol 15:321-326. (Pubitemid 30484256)
46. Madigan MT, Martinko JM, Dunlap PV, Clark DP (2009) Brock Biology of Microorganisms (Pearson Benjamin-Cummings, San Francisco).
47. Snel B, Bork P, Huynen MA (2002) Genomes in flux: The evolution of archaeal and proteobacterial gene content. Genome Res 12:17-25. (Pubitemid 34065586)
48. Sawada H, Kuykendall LD, Young JM (2003) Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. J Gen Appl Microbiol 49:155-179. (Pubitemid 37160911)
49. Dale C, Young SA, Haydon DT, Welburn SC (2001) The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc Natl Acad Sci USA 98:1883-1888. (Pubitemid 32165592)
50. Ma WB, Dong FFT, Stavrinides J, Guttman DS (2006) Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race. PLoS Genet 2:e209.
51. Horn M, et al. (2004) Illuminating the evolutionary history of chlamydiae. Science 304:728-730. (Pubitemid 38560877)
52. Frank AC, Alsmark CM, Thollesson M, Andersson SGE (2005) Functional divergence and horizontal transfer of type IV secretion systems. Mol Biol Evol 22:1325-1336. (Pubitemid 40577771)
53. Ruby EG, et al. (2005) Complete genome sequence of Vibrio fischeri: A symbiotic bacterium with pathogenic congeners. Proc Natl Acad Sci USA 102:3004-3009. (Pubitemid 40299906)
54. Ewald PW (1987) Transmission modes and evolution of the parasitism-mutualism continuum. Ann N Y Acad Sci 503:295-306.
55. Corsaro D, Venditti D, Padula M, Valassina M (1999) Intracellular life. Crit Rev Microbiol 25:39-79. (Pubitemid 29169598)
56. Fine PEM (1975) Vectors and vertical transmission: An epidemiologic perspective. Ann N Y Acad Sci 266:173-194.
57. Sachs JL, Mueller UG, Wilcox TP, Bull JJ (2004) The evolution of cooperation. Q Rev Biol 79:135-160. (Pubitemid 38774264)
58. Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21:541-554. (Pubitemid 38339670)
59. Sullivan JT, Patrick HN, Lowther WL, Scott DB, Ronson CW (1995) Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proc Natl Acad Sci USA 92:8985-8989.
60. Wilkinson DM (1999) Bacterial ecology, antibiotics and selection for virulence. Ecol Lett 2:207-209.
61. Turnbaugh PJ, et al. (2009) A core gut microbiome in obese and lean twins. Nature 457:480-484.
62. Weinert LA, et al. (2009) A large new subset of TRIM genes highly diversified by duplication and positive selection in teleost fish. BMC Biol 7:7.
63. Axelrod R, Hamilton WD (1981) The evolution of cooperation. Science 211: 1390-1396. (Pubitemid 11107890)
64. Bull JJ, Rice WR (1991) Distinguishing mechanisms for the evolution of co-operation. J Theor Biol 149:63-74.
65. Foster KR, Wenseleers T (2006) A general model for the evolution of mutualisms. J Evol Biol 19:1283-1293.
66. Brown JL (1983) Cooperation-a biologist's dilemma. Adv Stud Behav 13:1-37.
67. Connor RC (1995) The benefits of mutualism: A conceptual framework. Biol Rev Camb Philos Soc 70:427-457.
68. Simms EL, Taylor DL (2002) Partner choice in nitrogen-fixing mutualisms of legumes and rhizobia. Integr Comp Biol 42:369-380.
69. Denison RF (2000) Legume sanctions and the evolution of symbiotic cooperation by rhizobia. Am Nat 6:567-576.
70. Sachs JL, Simms EL (2008) The origins of uncooperative rhizobia. Oikos 117:961-966. (Pubitemid 352032721)
71. Sonnenburg JL, et al. (2005) Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307:1955-1959. (Pubitemid 40404703)
72. West SA, Kiers ET, Pen I, Denison RF (2002a) Sanctions and mutualism stability: when should less beneficial mutualists be tolerated? J Evol Biol 15:830-837.
73. West SA, Kiers ET, Simms EL, Denison RF (2002b) Sanctions and mutualism stability: Why do rhizobia fix nitrogen? Proc Biol Sci 269:685-694.
74. Weyl EG, Frederickson ME, Yu DW, Pierce NE (2010) Economic contract theory tests models of mutualism. Proc Natl Acad Sci USA 107:15712-15716.
75. Archetti M, et al. (2011) Let the right one in: a microeconomic approach to partner choice in mutualisms. Am Nat 177:75-85.
76. Kiers ET, Rousseau RA, West SA, Denison RF (2003) Host sanctions and the legume-rhizobium mutualism. Nature 425:78-81. (Pubitemid 37101720)
77. Sachs JL, et al. (2010) Host control over infection and proliferation of a cheater symbiont. J Evol Biol 23:1919-1927.
78. Visick KL, Foster J, Doino J, McFall-Ngai M, Ruby EG (2000) Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J Bacteriol 182:4578-4586. (Pubitemid 30599822)
79. Kikuchi Y, Hosokawa T, Fukatsu T (2011) An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J 5:446-460.
80. Huss-Danell K, Frej AK (1986) Distribution of Frankia in soils from forest and afforestation sites in northern Sweden. Plant Soil 90:407-417.
81. Sachs JL, Kembel SW, Lau AH, Simms EL (2009) In situ phylogenetic structure and diversity of wild Bradyrhizobium communities. Appl Environ Microbiol 75:4727-4735.
82. Barke J, et al. (2010) A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus. BMC Biol 8:109.
83. Mueller UG, Dash D, Rabeling C, Rodrigues A (2008) Coevolution between attine ants and actinomycete bacteria: a reevaluation. Evolution 62:2894-2912.
84. Mueller UG, Ishak H, Lee JC, Sen R, Gutell RR (2010) Placement of attine ant-associated Pseudonocardia in a global Pseudonocardia phylogeny (Pseudonocardiaceae, Actinomycetales): A test of two symbiont-association models. Antonie van Leeuwenhoek 98: 195-212.
85. Carson CA, et al. (2005) Specificity of a Bacteroides thetaiotaomicron marker for human feces. Appl Environ Microbiol 71:4945-4949. (Pubitemid 41129563)
86. Nishiguchi MK, Nair VS (2003) Evolution of symbiosis in the Vibrionaceae: A combined approach using molecules and physiology. Int J Syst Evol Microbiol 53:2019-2026. (Pubitemid 37483867)
87. Wollenberg MS, Ruby EG (2009) Population structure of Vibrio fischeri within the light organs of Euprymna scolopes squid from two Oahu (Hawaii) populations. Appl Environ Microbiol 75:193-202.
88. 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 12:1061-1075. (Pubitemid 36524298)
89. Dale C, Moran NA (2006) Molecular interactions between bacterial symbionts and their hosts. Cell 126:453-465. (Pubitemid 44163611)
90. Moran NA (2003) Tracing the evolution of gene loss in obligate bacterial symbionts. Curr Opin Microbiol 6:512-518.
91. Toh H, et al. (2006) Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res 16:149-156. (Pubitemid 43200262)
92. Martin W, Herrmann RG (1998) Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol 118:9-17. (Pubitemid 128652964)
93. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407:81-86.
94. Moran NA, McLaughlin HJ, Sorek R (2009) The dynamics and time scale of ongoing genomic erosion in symbiotic bacteria. Science 323:379-382.
95. Kikuchi Y, et al. (2009) Host-symbiont co-speciation and reductive genome evolution in gut symbiotic bacteria of acanthosomatid stinkbugs. BMC Biol 7:2.
96. Kojima A, Hirose E (2010) Transfer of prokaryotic algal symbionts from a tropical ascidian (Lissoclinum punctatum) colony to its larvae. Zoolog Sci 27:124-127.
97. Kaltenpoth M, Goettler W, Koehler S, Strohm E (2010) Life cycle and population dynamics of a protective insect symbiont reveal severe bottlenecks during vertical transmission. Evol Ecol 24:463-477.
98. Ferree PM, et al. (2005) Wolbachia utilizes host microtubules and Dynein for anterior localization in the Drosophila oocyte. PLoS Pathog 1:e14.
99. Vandermeer JH, Boucher DH (1978) Varieties of mutualistic interaction in population models. J Theor Biol 74:549-558. (Pubitemid 9042120)
100. Keeler KH (1985) Cost: Benefit models of mutualism. The Biology of Mutualism, Ecology and Evolution, ed Boucher DH (Oxford Univ Press, London), pp 100-127.
101. Holland JN, DeAngelis DL, Schultz ST (2004) Evolutionary stability of mutualism: Interspecific population regulation as an evolutionarily stable strategy. Proc Biol Sci 271:1807-1814.
102. Doebeli M, Knowlton N (1998) The evolution of interspecific mutualisms. Proc Natl Acad Sci USA 95:8676-8680. (Pubitemid 28350547)
103. Ferrière R, Gauduchon M, Bronstein JL (2007) Evolution and persistence of obligate mutualists and exploiters: competition for partners and evolutionary immunization. Ecol Lett 10:115-126. (Pubitemid 46161111)
104. Douglas AE (2008) Conflict, cheats and the persistence of symbioses. New Phytol 177: 849-858.
105. Sachs JL, Simms EL (2006) Pathways to mutualism breakdown. Trends Ecol Evol 21: 585-592. (Pubitemid 44354972)
106. Keeling PJ (2010) The endosymbiotic origin, diversification and fate of plastids. Philos Trans R Soc Lond B 365:729-748.
107. 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 73:4308-4316. (Pubitemid 47068172)
108. Young JPW, Haukka KE (1996) Diversity and phylogeny of rhizobia. New Phytol 133: 87-94. (Pubitemid 126558385)
109. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696-704. (Pubitemid 37365050)
110. Wu M, Eisen JA (2008) A simple, fast, and accurate method of phylogenomic inference. Genome Biol 9:R151.
111. Maddison WP, Maddison DR (2010) Mesquite: A modular system for evolutionary analysis. Version 2.74. Available at http://mesquiteproject.org. Accessed on November 2010.
112. Normand P, et al. (1996) Molecular phylogeny of the genus Frankia and related genera and emendation of the family Frankiaceae. Int J Syst Bacteriol 46:1-9. (Pubitemid 26030464)
113. Münchhoff J, et al. (2007) Host specificity and phylogeography of the prochlorophyte Prochloron sp., an obligate symbiont in didemnid ascidians. Environ Microbiol 9: 890-899. (Pubitemid 46397086)
114. Kaltenpoth M, et al. (2006) 'Candidatus Streptomyces philanthi', an endosymbiotic streptomycete in the antennae of Philanthus digger wasps. Int J Syst Evol Microbiol 56:1403-1411. (Pubitemid 43933836)
115. Svenning MM, Eriksson T, Rasmussen U (2005) Phylogeny of symbiotic cyanobacteria within the genus Nostoc based on16S rDNA sequence analyses. Arch Microbiol 183:19-26. (Pubitemid 40142878)
116. Turner S, Pryer KM, Miao VPW, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46:327-338. (Pubitemid 29400753)