Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

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

Volumn 112, Issue 33, 2015, Pages 10169-10176

  Bennett, Gordon M ^a   Moran, Nancy A ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Aphid; Buchnera; Coevolution; Muller's ratchet; Selection levels

Indexed keywords

ADAPTATION; APHID; ARTICLE; BIOSIS; BUCHNERA APHIDICOLA; COEVOLUTION; ECOLOGY; ENVIRONMENTAL FACTOR; EVOLUTION; GENOME; HOST; HOST PATHOGEN INTERACTION; IMMUNE SYSTEM; MUTATION; NONHUMAN; PRIORITY JOURNAL; RABBIT; RISK FACTOR; SPECIES DIFFERENTIATION; SYMBIONT; SYMBIOSIS; ANIMAL; BUCHNERA; GAMMAPROTEOBACTERIA; GENETIC DRIFT; GENETICS; GENOMICS; INSECT; MICROBIOLOGY; MOLECULAR EVOLUTION; PHYLOGENY; PHYSIOLOGY; SPECIES EXTINCTION;

APHIDIDAE; BUCHNERA APHIDICOLA; EUKARYOTA; HEXAPODA; ORYCTOLAGUS CUNICULUS;

ANIMALS; APHIDS; BIOLOGICAL EVOLUTION; BUCHNERA; ECOLOGY; EVOLUTION, MOLECULAR; EXTINCTION, BIOLOGICAL; GAMMAPROTEOBACTERIA; GENETIC DRIFT; GENOMICS; HOST-PATHOGEN INTERACTIONS; IMMUNE SYSTEM; INSECTS; MUTATION; PHYLOGENY; SYMBIOSIS;

EID: 84939833651     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1421388112     Document Type: Article

References (108)

1. McCutcheon JP, Moran NA (2012) Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10(1):13-26.
2. Moran NA, Bennett GM (2014) The tiniest tiny genomes. Annu Rev Microbiol 68:195-215.
3. Husnik F, et al. (2013) Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153(7):1567-1578.
4. Sloan DB, et al. (2014) Parallel histories of horizontal gene transfer facilitated extreme reduction of endosymbiont genomes in sap-feeding insects. Mol Biol Evol 31(4):857-871.
5. Nakabachi A, Ishida K, Hongoh Y, Ohkuma M, Miyagishima S-Y (2014) Aphid gene of bacterial origin encodes a protein transported to an obligate endosymbiont. Curr Biol 24(14):R640-R641.
6. Sandström J, Moran N (1999) How nutritionally imbalanced is phloem sap for aphids? Entomol Exp Appl 91(1):203-210.
7. Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17-37.
8. Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165-190.
9. Baumann P (2005) Biology bacteriocyte-associated endosymbionts of plant sapsucking insects. Annu Rev Microbiol 59:155-189.
10. Bennett GM, Moran NA (2013) Small, smaller, smallest: The origins and evolution of ancient dual symbioses in a Phloem-feeding insect. Genome Biol Evol 5(9):1675-1688.
11. Grimaldi D, Engel MS (2005) Evolution of the Insects (Cambridge Univ Press, New York).
12. Misof B, et al. (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science 346(6210):763-767.
13. Santos-Garcia D, et al. (2014) Small but powerful, the primary endosymbiont of moss bugs, Candidatus Evansia muelleri, holds a reduced genome with large biosynthetic capabilities. Genome Biol Evol 6(7):1875-1893.
14. Kuechler SM, Gibbs G, Burckhardt D, Dettner K, Hartung V (2013) Diversity of bacterial endosymbionts and bacteria-host co-evolution in Gondwanan relict moss bugs (Hemiptera: Coleorrhyncha: Peloridiidae). Environ Microbiol 15(7):2031-2042.
15. Lo N, Bandi C, Watanabe H, Nalepa C, Beninati T (2003) Evidence for cocladogenesis between diverse dictyopteran lineages and their intracellular endosymbionts. Mol Biol Evol 20(6):907-913.
16. Sabree ZL, Degnan PH, Moran NA (2010) Chromosome stability and gene loss in cockroach endosymbionts. Appl Environ Microbiol 76(12):4076-4079.
17. Sauer C, Stackebrandt E, Gadau J, Hölldobler B, Gross R (2000) Systematic relationships and cospeciation of bacterial endosymbionts and their carpenter ant host species: Proposal of the new taxon Candidatus Blochmannia gen. nov. Int J Syst Evol Microbiol 50(Pt 5):1877-1886.
18. Allen JM, Reed DL, Perotti MA, Braig HR (2007) Evolutionary relationships of "Candidatus Riesia spp.," endosymbiotic enterobacteriaceae living within hematophagous primate lice. Appl Environ Microbiol 73(5):1659-1664.
19. Heddi A, et al. (2005) Molecular and cellular profiles of insect bacteriocytes: Mutualism and harm at the initial evolutionary step of symbiogenesis. Cell Microbiol 7(2):293-305.
20. Lefèvre C, et al. (2004) Endosymbiont phylogenesis in the dryophthoridae weevils: Evidence for bacterial replacement. Mol Biol Evol 21(6):965-973.
21. Toju H, Tanabe AS, Notsu Y, Sota T, Fukatsu T (2013) Diversification of endosymbiosis: Replacements, co-speciation and promiscuity of bacteriocyte symbionts in weevils. ISME J 7(7):1378-1390.
22. Stewart FJ, Young CR, Cavanaugh CM (2008) Lateral symbiont acquisition in a maternally transmitted chemosynthetic clam endosymbiosis. Mol Biol Evol 25(4):673-687.
23. Newton ILG, et al. (2007) The Calyptogena magnifica chemoautotrophic symbiont genome. Science 315(5814):998-1000.
24. Kwan JC, et al. (2012) Genome streamlining and chemical defense in a coral reef symbiosis. Proc Natl Acad Sci USA 109(50):20655-20660.
25. Pinel N, Davidson SK, Stahl DA (2008) Verminephrobacter eiseniae gen. nov., sp. nov., a nephridial symbiont of the earthworm Eisenia foetida (Savigny). Int J Syst Evol Microbiol 58(Pt 9):2147-2157, and erratum (2013) 63(Pt 2):796.
26. Hentschel U, Piel J, Degnan SM, Taylor MW (2012) Genomic insights into the marine sponge microbiome. Nat Rev Microbiol 10(9):641-654.
27. Hendry TA, de Wet JR, Dunlap PV (2014) Genomic signatures of obligate host dependence in the luminous bacterial symbiont of a vertebrate. Environ Microbiol 16(8):2611-2622.
28. Koga R, Tsuchida T, Sakurai M, Fukatsu T (2007) Selective elimination of aphid endosymbionts: Effects of antibiotic dose and host genotype, and fitness consequences. FEMS Microbiol Ecol 60(2):229-239.
29. Wilkinson TL, Ishikawa H (2000) Injection of essential amino acids substitutes for bacterial supply in aposymbiotic pea aphids (Acyrthosiphon pisum). Entomol Exp Appl 94(1):85-91.
30. Dedeine F, et al. (2001) Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci USA 98(11):6247-6252.
31. Braendle C, et al. (2003) Developmental origin and evolution of bacteriocytes in the aphid-Buchnera symbiosis. PLoS Biol 1(1):E21.
32. Koga R, Meng X-Y, Tsuchida T, Fukatsu T (2012) Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte-embryo interface. Proc Natl Acad Sci USA 109(20):E1230-E1237.
33. Nakabachi A, et al. (2005) Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium, Buchnera. Proc Natl Acad Sci USA 102(15):5477-5482.
34. Poliakov A, et al. (2011) Large-scale label-free quantitative proteomics of the pea aphid-Buchnera symbiosis. Mol Cell Proteomics 10(6):007039.
35. Hansen AK, Moran NA (2011) Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proc Natl Acad Sci USA 108(7):2849-2854.
36. Shigenobu S, Stern DL (2013) Aphids evolved novel secreted proteins for symbiosis with bacterial endosymbiont. Proc Biol Sci 280(1750):20121952.
37. Price DRG, et al. (2014) Aphid amino acid transporter regulates glutamine supply to intracellular bacterial symbionts. Proc Natl Acad Sci USA 111(1):320-325.
38. Wang J, Wu Y, Yang G, Aksoy S (2009) Interactions between mutualist Wigglesworthia and tsetse peptidoglycan recognition protein (PGRP-LB) influence trypanosome transmission. Proc Natl Acad Sci USA 106(29):12133-12138.
39. Ratzka C, Gross R, Feldhaar H (2013) Gene expression analysis of the endosymbiont-bearing midgut tissue during ontogeny of the carpenter ant Camponotus floridanus. J Insect Physiol 59(6):611-623.
40. Gerardo NM, et al. (2010) Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol 11(2):R21.
41. International Aphid Genomics Consortium (2010) Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol 8(2):e1000313.
42. Douglas AE, Bouvaine S, Russell RR (2011) How the insect immune system interacts with an obligate symbiotic bacterium. Proc Biol Sci 278(1704):333-338.
43. Stavrinides J, McCloskey JK, Ochman H (2009) Pea aphid as both host and vector for the phytopathogenic bacterium Pseudomonas syringae. Appl Environ Microbiol 75(7):2230-2235.
44. Nakabachi A, Ishikawa H, Kudo T (2003) Extraordinary proliferation of microorganisms in aposymbiotic pea aphids, Acyrthosiphon pisum. J Invertebr Pathol 82(3):152-161.
45. Moran NA (1996) Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci USA 93(7):2873-2878.
46. Wernegreen JJ (2002) Genome evolution in bacterial endosymbionts of insects. Nat Rev Genet 3(11):850-861.
47. Rispe C, Moran NA (2000) Accumulation of deleterious mutations in endosymbionts: Muller's ratchet with two levels of selection. Am Nat 156(4):425-441.
48. Lynch M, Conery JS (2003) The origins of genome complexity. Science 302(5649):1401-1404.
49. Rispe C, Delmotte F, van Ham RCHJ, Moya A (2004) Mutational and selective pressures on codon and amino acid usage in Buchnera, endosymbiotic bacteria of aphids. Genome Res 14(1):44-53.
50. Pettersson ME, Berg OG (2007) Muller's ratchet in symbiont populations. Genetica 130(2):199-211.
51. 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(6800):81-86.
52. Tamas I, et al. (2002) 50 million years of genomic stasis in endosymbiotic bacteria. Science 296(5577):2376-2379.
53. van Ham RCHJ, et al. (2003) Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci USA 100(2):581-586.
54. Moran NA, McLaughlin HJ, Sorek R (2009) The dynamics and time scale of ongoing genomic erosion in symbiotic bacteria. Science 323(5912):379-382.
55. Pérez-Brocal V, et al. (2006) A small microbial genome: The end of a long symbiotic relationship? Science 314(5797):312-313.
56. Jiang Z, et al. (2013) Comparative analysis of genome sequences from four strains of the Buchnera aphidicola Mp endosymbion of the green peach aphid, Myzus persicae. BMC Genomics 14:917.
57. Sloan DB, Moran NA (2012) Genome reduction and co-evolution between the primary and secondary bacterial symbionts of psyllids. Mol Biol Evol 29(12):3781-3792.
58. Bennett GM, McCutcheon JP, MacDonald BR, Romanovicz D, Moran NA (2014) Differential genome evolution between companion symbionts in an insect-bacterial symbiosis. MBio 5(5):e01697-e14.
59. Rio RVM, et al. (2012) Insight into the transmission biology and species-specific functional capabilities of tsetse (Diptera: glossinidae) obligate symbiont Wigglesworthia. MBio 3(1):e00240-e11.
60. Sabree ZL, Huang CY, Okusu A, Moran NA, Normark BB (2013) The nutrient supplying capabilities of Uzinura, an endosymbiont of armoured scale insects. Environ Microbiol 15(7):1988-1999.
61. Williams LE, Wernegreen JJ (2013) Sequence context of indel mutations and their effect on protein evolution in a bacterial endosymbiont. Genome Biol Evol 5(3):599-605.
62. Nakabachi A, et al. (2006) The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314(5797):267.
63. Lambert JD, Moran NA (1998) Deleterious mutations destabilize ribosomal RNA in endosymbiotic bacteria. Proc Natl Acad Sci USA 95(8):4458-4462.
64. Herbeck JT, Funk DJ, Degnan PH, Wernegreen JJ (2003) A conservative test of genetic drift in the endosymbiotic bacterium Buchnera: Slightly deleterious mutations in the chaperonin groEL. Genetics 165(4):1651-1660.
65. Wernegreen JJ (2011) Reduced selective constraint in endosymbionts: Elevation in radical amino acid replacements occurs genome-wide. PLoS ONE 6(12):e28905.
66. Baumann P, Baumann L, Clark MA (1996) Levels of Buchnera aphidicola chaperonin GroEL during growth of the aphid Schizaphis graminum. Curr Microbiol 32:279-285.
67. Wilcox JL, Dunbar HE, Wolfinger RD, Moran NA (2003) Consequences of reductive evolution for gene expression in an obligate endosymbiont. Mol Microbiol 48(6):1491-1500.
68. Kupper M, Gupta SK, Feldhaar H, Gross R (2014) Versatile roles of the chaperonin GroEL in microorganism-insect interactions. FEMS Microbiol Lett 353(1):1-10.
69. Frank SA (1997) Models of symbiosis. Am Nat 150(Suppl 1):S80-S99.
70. Karlsson EK, Kwiatkowski DP, Sabeti PC (2014) Natural selection and infectious disease in human populations. Nat Rev Genet 15(6):379-393.
71. Watanabe K, Yukuhiro F, Matsuura Y, Fukatsu T, Noda H (2014) Intrasperm vertical symbiont transmission. Proc Natl Acad Sci USA 111(20):7433-7437.
72. Frank SA (2012) Evolution: Mitochondrial burden on male health. Curr Biol 22(18):R797-R799.
73. Werren JH, Baldo L, Clark ME (2008) Wolbachia: Master manipulators of invertebrate biology. Nat Rev Microbiol 6(10):741-751.
74. Penz T, et al. (2012) Comparative genomics suggests an independent origin of cytoplasmic incompatibility in Cardinium hertigii. PLoS Genet 8(10):e1003012.
75. Login FH, et al. (2011) Antimicrobial peptides keep insect endosymbionts under control. Science 334(6054):362-365.
76. Frank SA (2003) Perspective: Repression of competition and the evolution of cooperation. Evolution 57(4):693-705.
77. Corbett-Detig RB, Zhou J, Clark AG, Hartl DL, Ayroles JF (2013) Genetic incompatibilities are widespread within species. Nature 504(7478):135-137.
78. Moran NA, Yun Y (2015) Experimental replacement of an obligate insect symbiont. Proc Natl Acad Sci USA 112(7):2093-2096.
79. Fan Y, Wernegreen JJ (2013) Can't take the heat: High temperature depletes bacterial endosymbionts of ants. Microb Ecol 66(3):727-733.
80. Burke G, Fiehn O, Moran N (2010) Effects of facultative symbionts and heat stress on the metabolome of pea aphids. ISME J 4(2):242-252.
81. Montllor CB, Maxmen A, Purcell AH (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27(2):189-195.
82. Dunbar HE, Wilson ACC, Ferguson NR, Moran NA (2007) Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS Biol 5(5):e96.
83. Burke GR, McLaughlin HJ, Simon J-C, Moran NA (2010) Dynamics of a recurrent Buchnera mutation that affects thermal tolerance of pea aphid hosts. Genetics 186(1):367-372.
84. Wernegreen JJ (2012) Mutualism meltdown in insects: Bacteria constrain thermal adaptation. Curr Opin Microbiol 15(3):255-262.
85. McCutcheon JP, McDonald BR, Moran NA (2009) Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc Natl Acad Sci USA 106(36):15394-15399.
86. Koga R, Moran NA (2014) Swapping symbionts in spittlebugs: Evolutionary replacement of a reduced genome symbiont. ISME J 8(6):1237-1246.
87. Lamelas A, et al. (2011) Serratia symbiotica from the aphid Cinara cedri: A missing link from facultative to obligate insect endosymbiont. PLoS Genet 7(11):e1002357.
88. Gómez-Valero L, et al. (2004) Coexistence of Wolbachia with Buchnera aphidicola and a secondary symbiont in the aphid Cinara cedri. J Bacteriol 186(19):6626-6633.
89. Burke GR, Normark BB, Favret C, Moran NA (2009) Evolution and diversity of facultative symbionts from the aphid subfamily Lachninae. Appl Environ Microbiol 75(16):5328-5335.
90. Burke GR, Moran NA (2011) Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol Evol 3:195-208.
91. Koga R, Bennett GM, Cryan JR, Moran NA (2013) Evolutionary replacement of obligate symbionts in an ancient and diverse insect lineage. Environ Microbiol 15(7):2073-2081.
92. Urban JM, Cryan JR (2012) Two ancient bacterial endosymbionts have coevolved with the planthoppers (Insecta: Hemiptera: Fulgoroidea). BMC Evol Biol 12:87.
93. Toenshoff ER, Gruber D, Horn M (2012) Co-evolution and symbiont replacement shaped the symbiosis between adelgids (Hemiptera: Adelgidae) and their bacterial symbionts. Environ Microbiol 14(5):1284-1295.
94. McCutcheon JP, von Dohlen CD (2011) An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr Biol 21(16):1366-1372.
95. Thao ML, Gullan PJ, Baumann P (2002) Secondary (gamma-Proteobacteria) endosymbionts infect the primary (beta-Proteobacteria) endosymbionts of mealybugs multiple times and coevolve with their hosts. Appl Environ Microbiol 68(7):3190-3197.
96. Rosenblueth M, Sayavedra L, Sámano-Sánchez H, Roth A, Martínez-Romero E (2012) Evolutionary relationships of flavobacterial and enterobacterial endosymbionts with their scale insect hosts (Hemiptera: Coccoidea). J Evol Biol 25(11):2357-2368.
97. Wu D, et al. (2006) Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol 4(6):e188.
98. Dale C, Plague GR, Wang B, Ochman H, Moran NA (2002) Type III secretion systems and the evolution of mutualistic endosymbiosis. Proc Natl Acad Sci USA 99(19):12397-12402.
99. Rosas-Pérez T, Rosenblueth M, Rincón-Rosales R, Mora J, Martínez-Romero E (2014) Genome sequence of "Candidatus Walczuchella monophlebidarum" the flavobacterial endosymbiont of Llaveia axin axin (Hemiptera: Coccoidea: Monophlebidae). Genome Biol Evol 6(3):714-726.
100. Nakabachi A, et al. (2013) Defensive bacteriome symbiont with a drastically reduced genome. Curr Biol 23(15):1478-1484.
101. Toju H, et al. (2010) "Candidatus Curculioniphilus buchneri," a novel clade of bacterial endocellular symbionts from weevils of the genus Curculio. Appl Environ Microbiol 76(1):275-282.
102. Conord C, et al. (2008) Long-term evolutionary stability of bacterial endosymbiosis in curculionoidea: Additional evidence of symbiont replacement in the dryophthoridae family. Mol Biol Evol 25(5):859-868.
103. Kuo C-H, Moran NA, Ochman H (2009) The consequences of genetic drift for bacterial genome complexity. Genome Res 19(8):1450-1454.
104. Nachman MW (1998) Deleterious mutations in animal mitochondrial DNA. Genetica 102-103(1-6):61-69.
105. Hill JH, Chen Z, Xu H (2014) Selective propagation of functional mitochondrial DNA during oogenesis restricts the transmission of a deleterious mitochondrial variant. Nat Genet 46(4):389-392.
106. Kjeldsen KU, et al. (2012) Purifying selection and molecular adaptation in the genome of Verminephrobacter, the heritable symbiotic bacteria of earthworms. Genome Biol Evol 4(3):307-315.
107. Lund MB, Kjeldsen KU, Schramm A (2014) The earthworm-Verminephrobacter symbiosis: An emerging experimental system to study extracellular symbiosis. Front Microbiol 5:128.
108. Nikoh N, Hosokawa T, Oshima K, Hattori M, Fukatsu T (2011) Reductive evolution of bacterial genome in insect gut environment. Genome Biol Evol 3:702-714.