Diverse Bacteriophage Roles in an Aphid-Bacterial Defensive Mutualism
- ️Thu May 19 2016
Abedon ST (2008) Bacteriophage ecology: population growth, evolution, and impact of bacterial viruses. Cambridge University Press, Cambridge
Akman L, Yamashita A, Watanabe H, Oshima K, Shiba T, Hattori M, Aksoy S (2002) Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat Genet 32(3):402–407. doi:10.1038/ng986
Asakura M, Hinenoya A, Alam MS, Shima K, Zahid SH, Shi L, Sugimoto N, Ghosh AN, Ramamurthy T, Faruque SM, Nair GB, Yamasaki S (2007) An inducible lambdoid prophage encoding cytolethal distending toxin (Cdt-I) and a type III effector protein in enteropathogenic Escherichia coli. Proc Natl Acad Sci USA 104(36):14483–14488. doi:10.1073/pnas.0706695104
Asplen MK, Bano N, Brady CM, Desneux N, Hopper KR, Malouines C, Oliver KM, White JA, Heimpel GE (2014) Specialisation of bacterial endosymbionts that protect aphids from parasitoids. Ecol Entomol 39(6):736–739
Baldo L, Bordenstein S, Wernegreen JJ, Werren JH (2006) Widespread recombination throughout Wolbachia genomes. Mol Biol Evol 23(2):437–449. doi:10.1093/molbev/msj049
Barton ES, White DW, Cathelyn JS, Brett-McClellan KA, Engle M, Diamond MS, Miller VL, Virgin HW (2007) Herpesvirus latency confers symbiotic protection from bacterial infection. Nature 447 (7142):326–U327. doi:10.1038/Nature05762
Baumann P (2005) Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59:155–189. doi:10.1146/annurev.micro.59.030804.121041
Belda E, Moya A, Bentley S, Silva FJ (2010) Mobile genetic element proliferation and gene inactivation impact over the genome structure and metabolic capabilities of Sodalis glossinidius, the secondary endosymbiont of tsetse flies. BMC Genomics 11(1):449
Bensadia F, Boudreault S, Guay JF, Michaud D, Cloutier C (2006) Aphid clonal resistance to a parasitoid fails under heat stress. J Insect Physiol 52(2):146–157. doi:10.1016/j.jinsphys.2005.09.011
Bordenstein SR, Bordenstein SR (2011) Temperature affects the tripartite interactions between bacteriophage WO, Wolbachia, and cytoplasmic incompatibility. PLoS One 6(12), e29106
Bordenstein SR, Reznikoff WS (2005) Mobile DNA in obligate intracellular bacteria. Nat Rev Microbiol 3(9):688–699. doi:10.1038/nrmicro1233
Bordenstein SR, Wernegreen JJ (2004) Bacteriophage flux in endosymbionts (Wolbachia): infection frequency, lateral transfer, and recombination rates. Mol Biol Evol 21(10):1981–1991. doi:10.1093/molbev/msh211
Bordenstein SR, Marshall ML, Fry AJ, Kim U, Wernegreen JJ (2006) The tripartite associations between bacteriophage, Wolbachia, and arthropods. PLoS Pathog 2(10):1024. doi:10.1371/journal.ppat.0020106
Botstein D (1980) A theory for the modular evolution of bacteriophages. Ann NY Acad Sci 354:484–490. doi:10.1111/j.1749-6632.1980.tb27987.x
Brady CM, White JA (2013) Cowpea aphid (Aphis craccivora) associated with different host plants has different facultative endosymbionts. Ecol Entomol 38(4):433–437
Burke GR, Moran NA (2011) Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol Evol 3:195–208. doi:10.1093/Gbe/Evr002
Caccia S, Leonardi MG, Casartelli M, Grimaldi A, de Eguileor M, Pennacchio F, Giordana B (2005) Nutrient absorption by Aphidius ervi larvae. J Insect Physiol 51(11):1183–1192. doi:10.1016/j.jinsphys.2005.06.010
Calendar R, Abedon ST (2005) The bacteriophages, 2nd edn. Oxford University Press, Oxford
Carver M, Sullivan D (1988) Encapsulative defence reactions of aphids (Hemiptera: Aphididae) to insect parasitoids (Hymenoptera: Aphidiidae and Aphelinidae). Ecology and Effectiveness of Aphidophaga: 299–303
Cayetano L, Vorburger C (2015) Symbiont‐conferred protection against Hymenopteran parasitoids in aphids: how general is it? Ecol Entomol 40(1):85–93. doi:10.1111/een.12161
Chafee ME, Funk DJ, Harrison RG, Bordenstein SR (2010) Lateral phage transfer in obligate intracellular bacteria (Wolbachia): verification from natural populations. Mol Biol Evol 27(3):501–505. doi:10.1093/molbev/msp275
Chafee ME, Zecher CN, Gourley ML, Schmidt VT, Chen JH, Bordenstein SR, Clark ME (2011) Decoupling of host-symbiont-phage coadaptations following transfer between insect species. Genetics 187(1):203–215. doi:10.1534/genetics.110.120675
Chen DQ, Purcell AH (1997) Occurrence and transmission of facultative endosymbionts in aphids. Curr Microbiol 34(4):220–225
Clark MA, Moran NA, Baumann P, Wernegreen JJ (2000) Cospeciation between bacterial endosymbionts (Buchnera) and a recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution 54(2):517–525. doi:10.1554/0014-3820(2000)054[0517:Cbbeba]2.0.Co;2
Clark AJ, Pontes M, Jones T, Dale C (2007) A possible heterodimeric prophage-like element in the genome of the insect endosymbiont Sodalis glossinidius. J Bacteriol 189(7):2949–2951. doi:10.1128/Jb.00913-06
Cloutier C, Douglas AE (2003) Impact of a parasitoid on the bacterial symbiosis of its aphid host. Entomol Exp Appl 109(1):13–19
Darby AC, Birkle LM, Turner SL, Douglas AE (2001) An aphid-borne bacterium allied to the secondary symbionts of whitefly. FEMS Microbiol Ecol 36(1):43–50
Darby AC, Chandler SM, Welburn SC, Douglas AE (2005) Aphid-symbiotic bacteria cultured in insect cell lines. Appl Environ Microbiol 71(8):4833–4839. doi:10.1128/Aem.71.8.4833-4839.2005
Darby AC, Choi JH, Wilkes T, Hughes MA, Werren JH, Hurst GDD, Colbourne JK (2010) Characteristics of the genome of Arsenophonus nasoniae, son-killer bacterium of the wasp Nasonia. Insect Mol Biol 19:75–89. doi:10.1111/j.1365-2583.2009.00950.x
Degnan PH, Moran NA (2008a) Diverse phage-encoded toxins in a protective insect endosymbiont. Appl Environ Microbiol 74(21):6782–6791. doi:10.1128/Aem.01285-08
Degnan PH, Moran NA (2008b) Evolutionary genetics of a defensive facultative symbiont of insects: exchange of toxin-encoding bacteriophage. Mol Ecol 17(3):916–929
Degnan PH, Lazarus AB, Wernegreen JJ (2005) Genome sequence of Blochmannia pennsylvanicus indicates parallel evolutionary trends among bacterial mutualists of insects. Genome Res 15(8):1023–1033
Degnan PH, Yu Y, Sisneros N, Wing RA, Moran NA (2009) Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc Natl Acad Sci USA 106(22):9063–9068. doi:10.1073/pnas.0900194106
Degnan PH, Leonardo TE, Cass BN, Hurwitz B, Stern D, Gibbs RA, Richards S, Moran NA (2010) Dynamics of genome evolution in facultative symbionts of aphids. Environ Microbiol 12(8):2060–2069. doi:10.1111/j.1462-2920.2009.02085.x
Digilio MC, Isidoro N, Tremblay E, Pennacchio F (2000) Host castration by Aphidius ervi venom proteins. J Insect Physiol 46(6):1041–1050
Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92. doi:10.1146/annurev.ento.49.061802.123416
Douglas AE (1989) Mycetocyte symbiosis in insects. Biol Rev 64(4):409–434. doi:10.1111/j.1469-185X.1989.tb00682.x
Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37
Duron O (2014) Arsenophonus insect symbionts are commonly infected with APSE, a bacteriophage involved in protective symbiosis. FEMS Microbiol Ecol 90(1):184–194
Dykstra HR, Weldon SR, Martinez AJ, White JA, Hopper KR, Heimpel GE, Asplen MK, Oliver KM (2014) Factors limiting the spread of the protective symbiont Hamiltonella defensa in Aphis craccivora aphids. Appl Environ Microbiol 80(18):5818–5827
Endo Y, Tsurugi K, Yutsudo T, Takeda Y, Ogasawara T, Igarashi K (1988) Site of action of a vero toxin (Vt2) from Escherichia coli O157-H7 and of shiga toxin on eukaryotic ribosomes - RNA N-glycosidase activity of the toxins. Eur J Biochem 171(1–2):45–50
Engel P, Moran NA (2013) The gut microbiota of insects - diversity in structure and function. FEMS Microbiol Rev 37(5):699–735. doi:10.1111/1574-6976.12025
Engelberg-Kulka H, Glaser G (1999) Addiction modules and programmed cell death and antideath in bacterial cultures. Annu Rev Microbiol 53:43–70. doi:10.1146/annurev.micro.53.1.43
Falabella P, Tremblay E, Pennacchio F (2000) Host regulation by the aphid parasitoid Aphidius ervi: the role of teratocytes. Entomol Exp Appl 97(1):1–9
Falabella P, Riviello L, De Stradis ML, Stigliano C, Varricchio P, Grimaldi A, de Eguileor M, Graziani F, Gigliotti S, Pennacchio F (2009) Aphidius ervi teratocytes release an extracellular enolase. Insect Biochem Mol 39(11):801–813. doi:10.1016/j.ibmb.2009.09.005
Fan L, Reynolds D, Liu M, Stark M, Kjelleberg S, Webster NS, Thomas T (2012) Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. Proc Natl Acad Sci USA 109(27):E1878–E1887. doi:10.1073/pnas.1203287109
Feldhaar H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36(5):533–543. doi:10.1111/j.1365-2311.2011.01318.x
Ferrari J, Scarborough CL, Godfray HCJ (2007) Genetic variation in the effect of a facultative symbiont on host-plant use by pea aphids. Oecologia 153(2):323–329. doi:10.1007/s00442-007-0730-2
Flores CO, Meyer JR, Valverde S, Farr L, Weitz JS (2011) Statistical structure of host-phage interactions. Proc Natl Acad Sci USA 108(28):E288–E297. doi:10.1073/pnas.1101595108
Flyg C, Kenne K, Boman HG (1980) Insect pathogenic properties of Serratia marcescens – phage-resistant mutants with a decreased resistance to Cecropia immunity and a decreased virulence to Drosophila. J Gen Microbiol 120(1):173–181
Foster J, Ganatra M, Kamal I, Ware J, Makarova K, Ivanova N, Bhattacharyya A, Kapatral V, Kumar S, Posfai J, Vincze T, Ingram J, Moran L, Lapidus A, Omelchenko M, Kyrpides N, Ghedin E, Wang S, Goltsman E, Joukov V, Ostrovskaya O, Tsukerman K, Mazur M, Comb D, Koonin E, Slatko B (2005) The Wolbachia genome of Brugia malayi: Endosymbiont evolution within a human pathogenic nematode. PLos Biol 3(4):599–614. ARTN e121
Frantz A, Plantegenest M, Mieuzet L, Simon JC (2006) Ecological specialization correlates with genotypic differentiation in sympatric host-populations of the pea aphid. J Evol Biol 19(2):392–401. doi:10.1111/j.1420-9101.2005.01025.x
Frentiu FD, Robinson J, Young PR, McGraw EA, O’Neill SL (2010) Wolbachia-mediated resistance to dengue virus infection and death at the cellular level. PLoS One 5(10):e13398. doi:10.1371/journal.pone.0013398
Fukatsu T, Nikoh N, Kawai R, Koga R (2000) The secondary endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum (Insecta : Homoptera). Appl Environ Microbiol 66(7):2748–2758
Gavotte L, Henri H, Stouthamer R, Charif D, Charlat S, Boulétreau M, Vavre F (2007) A survey of the bacteriophage WO in the endosymbiotic bacteria Wolbachia. Mol Biol Evol 24(2):427–435
Gibson CM, Hunter MS (2010) Extraordinarily widespread and fantastically complex: comparative biology of endosymbiotic bacterial and fungal mutualists of insects. Ecol Lett 13(2):223–234. doi:10.1111/j.1461-0248.2009.01416.x
Gil R, Sabater-Munoz B, Latorre A, Silva FJ, Moya A (2002) Extreme genome reduction in Buchnera spp.: toward the minimal genome needed for symbiotic life. Proc Natl Acad Sci USA 99(7):4454–4458. doi:10.1073/pnas.062067299
Gil R, Silva FJ, Zientz E, Delmotte F, Gonzalez-Candelas F, Latorre A, Rausell C, Kamerbeek J, Gadau J, Holldobler B, van Ham RCHJ, Gross R, Moya A (2003) The genome sequence of Blochmannia floridanus: comparative analysis of reduced genomes. Proc Natl Acad Sci USA 100(16):9388–9393. doi:10.1073/pnas.1533499100
Gottlieb Y, Ghanim M, Gueguen G, Kontsedalov S, Vavre F, Fleury F, Zchori-Fein E (2008) Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies. FASEB J 22(7):2591–2599. doi:10.1096/fj.07-101162
Granberg F, Vicente-Rubiano M, Rubio-Guerri C, Karlsson OE, Kukielka D, Belak S, Sanchez-Vizcaino JM (2013) Metagenomic detection of viral pathogens in Spanish honeybees: co-infection by aphid lethal paralysis, Israel acute paralysis and Lake Sinai viruses. PLoS One 8(2), e57459
Grbic M, Strand MR (1998) Shifts in the life history of parasitic wasps correlate with pronounced alterations in early development. Proc Natl Acad Sci USA 95(3):1097–1101
Guay JF, Boudreault S, Michaud D, Cloutier C (2009) Impact of environmental stress on aphid clonal resistance to parasitoids: role of Hamiltonella defensa bacterial symbiosis in association with a new facultative symbiont of the pea aphid. J Insect Physiol 55(10):919–926. doi:10.1016/j.jinsphys.2009.06.006
Hamilton PT, Perlman SJ (2013) Host defense via symbiosis in Drosophila. Plos Pathog 9(12). doi:10.1371/journal.ppat.1003808
Hansen AK, Vorburger C, Moran NA (2012) Genomic basis of endosymbiont-conferred protection against an insect parasitoid. Genome Res 22(1):106–114
Hatfull GF (2008) Bacteriophage genomics. Curr Opin Microbiol 11(5):447–453. doi:10.1016/j.mib.2008.09.004
He XZ (2008) Reproductive behavior of Aphidius ervi Haliday (Hymenoptera: Aphidiidae). Massey University Dissertation, Palmerston North, New Zealand
Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322(5902):702. doi:10.1126/science.1162418
Heilmann S, Sneppen K, Krishna S (2010) Sustainability of virulence in a phage-bacterial ecosystem. J Virol 84(6):3016–3022. doi:10.1128/Jvi.02326-09
Henry LM, Peccoud J, Simon JC, Hadfield JD, Maiden MJC, Ferrari J, Godfray HCJ (2013) Horizontally transmitted symbionts and host colonization of ecological niches. Curr Biol 23(17):1713–1717
Henter HJ, Via S (1995) The potential for coevolution in a host-parasitoid system. 1. Genetic-variation within an aphid population in susceptibility to a parasitic wasp. Evolution 49(3):427–438. doi:10.2307/2410267
Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14(2):49–53. doi:10.1016/S0169-5347(98)01529-8
Horvath P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327(5962):167–170. doi:10.1126/science.1179555
Hurst GDD, Johnson AP, von der Schulenburg JHG, Fuyama Y (2000) Male-killing Wolbachia in Drosophila: a temperature-sensitive trait with a threshold bacterial density. Genetics 156(2):699–709
Ikeda T, Ishikawa H, Sasaki T (2003) Infection density of Wolbachia and level of cytoplasmic incompatibility in the Mediterranean flour moth, Ephestia kuehniella. J Invertebr Pathol 84(1):1–5. doi:10.1016/S0022-2011(03)00106-X
Jaenike J (2009) Coupled population dynamics of endosymbionts within and between hosts. Oikos 118(3):353–362. doi:10.1111/j.1600-0706.2008.17110.x
Jaenike J (2012) Population genetics of beneficial heritable symbionts. Trends Ecol Evol 27(4):226–232. doi:10.1016/j.tree.2011.10.005
Johnson WM, Lior H (1987) Response of Chinese-hamster ovary cells to a cytolethal distending toxin (Cdt) of Escherichia coli and possible misinterpretation as heat-labile (Lt) enterotoxin. FEMS Microbiol Lett 43(1):19–23
Kent BN, Bordenstein SR (2010) Phage WO of Wolbachia: lambda of the endosymbiont world. Trends Microbiol 18(4):173–181. doi:10.1016/j.tim.2009.12.011
Klasson L, Westberg J, Sapountzis P, Nasiund K, Lutnaes Y, Darby AC, Veneti Z, Chen LM, Braig HR, Garrett R, Bourtzis K, Andersson SGE (2009) The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proc Natl Acad Sci USA 106(14):5725–5730. doi:10.1073/pnas.0810753106
Koga R, Tsuchida T, Fukatsu T (2003) Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc R Soc Lond B Biol 270(1533):2543–2550. doi:10.1098/rspb.2003.2537
Krupovic M, Prangishvili D, Hendrix RW, Bamford DH (2011) Genomics of bacterial and archaeal viruses: dynamics within the prokaryotic virosphere. Microbiol Mol Biol Rev 75(4):610. doi:10.1128/Mmbr.00011-11
Kuo CH, Moran NA, Ochman H (2009) The consequences of genetic drift for bacterial genome complexity. Genome Res 19(8):1450–1454. doi:10.1101/gr.091785.109
Laughton AM, Garcia JR, Altincicek B, Strand MR, Gerardo NM (2011) Characterisation of immune responses in the pea aphid, Acyrthosiphon pisum. J Insect Physiol 57(6):830–839. doi:10.1016/j.jinsphys.2011.03.015
Lawrence PO (1990) Serosal cells of Biosteres longicaudatus (Hymenoptera, Braconidae) – ultrastructure and release of polypeptides. Arch Insect Biochem 13(3–4):199–216
Lenski RE (1988) Dynamics of interactions between bacteria and virulent bacteriophage. Adv Microb Ecol 10:1–44
Lin L, Bitner R, Edlin G (1977) Increased reproductive fitness of Escherichia coli Lambda-lysogens. J Virol 21(2):554–559
Lukasik P, Dawid MA, Ferrari J, Godfray HC (2013a) The diversity and fitness effects of infection with facultative endosymbionts in the grain aphid, Sitobion avenae. Oecologia. doi:10.1007/s00442-013-2660-5
Lukasik P, van Asch M, Guo HF, Ferrari J, Godfray HCJ (2013b) Unrelated facultative endosymbionts protect aphids against a fungal pathogen. Ecol Lett 16(2):214–218. doi:10.1111/Ele.12031
Lukasik P, Weldon SR, van Asch M, Patel V, Dennis A, Husnik F, Vorburger C, Ferrari J, Godfray HCJ, Oliver KM, Russell JA (2016) Strain diversity of parasitoid-protective endosymbionts of aphids: correlating phenotype with genotype (in prep)
Martinez AJ, Ritter SG, Doremus MR, Russell JA, Oliver KM (2014a) Aphid-encoded variability in susceptibility to a parasitoid. BMC Evol Biol 14(1):127. doi:10.1186/1471-2148-14-127
Martinez AJ, Weldon SR, Oliver KM (2014b) Effects of parasitism on aphid nutritional and protective symbioses. Mol Ecol 23(6):1594–1607. doi:10.1111/mec.12550
Martinez AJ, Kim KL, Harmon JP, Oliver KM (2016) Specificity of multi-modal aphid defenses against two rival parasitoids. PLoS One
Masui S, Kamoda S, Sasaki T, Ishikawa H (2000) Distribution and evolution of bacteriophage WO in Wolbachia, the endosymbiont causing sexual alterations in arthropods. J Mol Evol 51(5):491–497
McCutcheon JP, Moran NA (2012) Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10(1):13–26. doi:10.1038/Nrmicro2670
McDaniel L, Houchin LA, Williamson SJ, Paul JH (2002) Plankton blooms – Lysogeny in marine Synechococcus. Nature 415(6871):496. doi:10.1038/415496a
McGrath S, Fitzgerald GF, van Sinderen D (2002) Identification and characterization of phage-resistance genes in temperate lactococcal bacteriophages. Mol Microbiol 43(2):509–520. doi:10.1046/j.1365-2958.2002.02763.x
McLean AH, Godfray HCJ (2015) Evidence for specificity in symbiont-conferred protection against parasitoids. Proc R Soc B Biol Sci 282(1811):20150977. doi:10.1098/rspb.2015.0977
Mendes-Soares H, Chen I-CK, Fitzpatrick K, Velicer GJ (2014) Chimaeric load among sympatric social bacteria increases with genotype richness. Proc R Soc B Biol Sci 281(1787). doi:10.1098/rspb.2014.0285
Metcalf JA, Bordenstein SR (2012) The complexity of virus systems: the case of endosymbionts. Curr Opin Microbiol 15(4):546–552. doi:10.1016/j.mib.2012.04.010
Middelboe M, Holmfeldt K, Riemann L, Nybroe O, Haaber J (2009) Bacteriophages drive strain diversification in a marine Flavobacterium: implications for phage resistance and physiological properties. Environ Microbiol 11(8):1971–1982. doi:10.1111/j.1462-2920.2009.01920.x
Minot S, Sinha R, Chen J, Li HZ, Keilbaugh SA, Wu GD, Lewis JD, Bushman FD (2011) The human gut virome: inter-individual variation and dynamic response to diet. Genome Res 21(10):1616–1625. doi:10.1101/gr.122705.111
Montllor CB, Maxmen A, Purcell AH (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27(2):189–195
Moran NA (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci USA 104:8627–8633. doi:10.1073/pnas.0611659104
Moran NA, Plague GR (2004) Genornic changes following host restriction in bacteria. Curr Opin Genet Dev 14(6):627–633. doi:10.1016/j.gde.2004.09.003
Moran NA, Wernegreen JJ (2000) Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol Evol 15(8):321–326
Moran NA, Munson MA, Baumann P, Ishikawa H (1993) A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc R Soc Lond B Biol 253(1337):167–171
Moran NA, Degnan PH, Santos SR, Dunbar HE, Ochman H (2005) The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proc Natl Acad Sci USA 102(47):16919–16926. doi:10.1073/pnas.0507029102
Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190. doi:10.1146/annurev.genet.41.110306.130119
Moya A, Pereto J, Gil R, Latorre A (2008) Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat Rev Genet 9(3):218–229. doi:10.1038/Nrg2319
Nakabachi A, Ueoka R, Oshima K, Teta R, Mangoni A, Gurgui M, Oldham NJ, van Echten-Deckert G, Okamura K, Yamamoto K, Inoue H, Ohkuma M, Hongoh Y, Miyagishima S, Hattori M, Piel J, Fukatsu T (2013) Defensive bacteriome symbiont with a drastically reduced genome. Curr Biol 23(15):1478–1484. doi:10.1016/j.cub.2013.06.027
Newton ILG, Bordenstein SR (2011) Correlations between bacterial ecology and mobile DNA. Curr Microbiol 62(1):198–208. doi:10.1007/s00284-010-9693-3
Ng TFF, Willner DL, Lim YW, Schmieder R, Chau B, Nilsson C, Anthony S, Ruan YJ, Rohwer F, Breitbart M (2011) Broad surveys of DNA viral diversity obtained through viral metagenomics of mosquitoes. PLoS One 6(6), e20579
Noda H, Koizumi Y, Zhang Q, Deng KJ (2001) Infection density of Wolbachia and incompatibility level in two planthopper species, Laodelphax striatellus and Sogatella furcifera. Insect Biochem Mol 31(6–7):727–737
Nováková E, Hypša V, Moran NA (2009) Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiol 9(1):143
Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405(6784):299–304. doi:10.1038/35012500
Ohara M, Oswald E, Sugai M (2004) Cytolethal distending toxin: a bacterial bullet targeted to nucleus. J Biochem 136(4):409–413. doi:10.1093/jb/mvh154
Okuda T, Kadonookuda K (1995) Perilitus coccinellae teratocyte olypeptide – evidence for production of a teratocyte-specific 540 kda protein. J Insect Physiol 41(9):819–825
Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA 100(4):1803–1807. doi:10.1073/pnas.0335320100
Oliver KM, Moran NA, Hunter MS (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci USA 102(36):12795–12800. doi:10.1073/pnas.0506131102
Oliver KM, Moran NA, Hunter MS (2006) Costs and benefits of a superinfection of facultative symbionts in aphids. Proc R Soc B Biol Sci 273(1591):1273–1280. doi:10.1098/rspb.2005.3436
Oliver KM, Campos J, Moran NA, Hunter MS (2008) Population dynamics of defensive symbionts in aphids. Proc R Soc B Biol Sci 275(1632):293–299. doi:10.1098/rspb.2007.1192
Oliver KM, Degnan PH, Hunter MS, Moran NA (2009) Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325(5943):992–994. doi:10.1126/science.1174463
Oliver KM, Degnan PH, Burke GR, Moran NA (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55:247–266. doi:10.1146/annurev-ento-112408-085305
Oliver KM, Smith AH, Russell JA (2013) Defensive symbiosis in the real world–advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct Ecol 28(2):341–355. doi:10.1111/1365-2435.12133
Pantastico-Caldas M, Duncan KE, Istock CA, Bell JA (1992) Population-dynamics of bacteriophage and Bacillus subtilis in soil. Ecology 73(5):1888–1902. doi:10.2307/1940040
Peccoud J, Ollivier A, Plantegenest M, Simon JC (2009) A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. Proc Natl Acad Sci USA 106(18):7495–7500. doi:10.1073/pnas.0811117106
Plague GR, Dale C, Moran NA (2003) Low and homogeneous copy number of plasmid-borne symbiont genes affecting host nutrition in Buchnera aphidicola of the aphid Uroleucon ambrosiae. Mol Ecol 12(4):1095–1100. doi:10.1046/j.1365-294X.2003.01782.x
Pontes MH, Dale C (2006) Culture and manipulation of insect facultative symbionts. Trends Microbiol 14(9):406–412. doi:10.1016/j.tim.2006.07.004
Ptashne M (2004) A genetic switch: phage lambda revisited, vol 3. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
Rabinovitch A, Aviram I, Zaritsky A (2003) Bacterial debris – an ecological mechanism for coexistence of bacteria and their viruses. J Theor Biol 224(3):377–383. doi:10.1016/S0022-5193(03)00174-7
Rahbe Y, Digilio MC, Febvay G, Guillaud J, Fanti P, Pennacchio F (2002) Metabolic and symbiotic interactions in amino acid pools of the pea aphid, Acyrthosiphon pisum, parasitized by the braconid Aphidius ervi. J Insect Physiol 48(5):507–516
Rankin DJ, Rocha EPC, Brown SP (2011) What traits are carried on mobile genetic elements, and why? Heredity 106(1):1–10. doi:10.1038/Hdy.2010.24
Roossinck MJ (2011) The good viruses: viral mutualistic symbioses. Nat Rev Microbiol 9(2):99–108. doi:10.1038/Nrmicro2491
Russell JA, Moran NA (2005) Horizontal transfer of bacterial symbionts: heritability and fitness effects in a novel aphid host. Appl Environ Microbiol 71(12):7987–7994. doi:10.1128/Aem.71.12.7987-7994.2005
Russell JA, Moran NA (2006) Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc R Soc B Biol Sci 273(1586):603–610. doi:10.1098/rspb.2005.3348
Russell JA, Weldon S, Smith AH, Kim KL, Hu Y, Łukasik P, Doll S, Anastopoulos I, Novin M, Oliver KM (2013) Uncovering symbiont-driven genetic diversity across North American pea aphids. Mol Ecol 22(7):2045–2059. doi:10.1111/mec.12211
Sandstrom JP, Russell JA, White JP, Moran NA (2001) Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol Ecol 10(1):217–228
Saridaki A, Sapountzis P, Harris HL, Batista PD, Biliske JA, Pavlikaki H, Oehler S, Savakis C, Braig HR, Bourtzis K (2011) Wolbachia prophage DNA adenine methyltransferase genes in different Drosophila-Wolbachia associations. PLoS One 6(5), e19708
Sauer C, Stackebrandt E, Gadau J, Holldobler 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 50:1877–1886
Scarborough CL, Ferrari J, Godfray HCJ (2005) Aphid protected from pathogen by endosymbiont. Science 310(5755):1781. doi:10.1126/science.1120180
Schmid M, Sieber R, Zimmermann YS, Vorburger C (2012) Development, specificity and sublethal effects of symbiont-conferred resistance to parasitoids in aphids. Funct Ecol 26(1):207–215. doi:10.1111/j.1365-2435.2011.01904.x
Stern A, Mick E, Tirosh I, Sagy O, Sorek R (2012) CRISPR targeting reveals a reservoir of common phages associated with the human gut microbiome. Genome Res 22(10):1985–1994. doi:10.1101/gr.138297.112
Stouthamer R, Breeuwer JAJ, Hurst GDD (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53:71–102. doi:10.1146/annurev.micro.53.1.71
Strand MR (2010) Polydnaviruses. In: Asagari S, Johnson K (eds) Insect virology. Caister Scientific Press, Norfolk, pp 171–197
Strive T, Wright J, Kovaliski J, Botti G, Capucci L (2010) The non-pathogenic Australian lagovirus RCV-A1 causes a prolonged infection and elicits partial cross-protection to rabbit haemorrhagic disease virus. Virology 398(1):125–134. doi:10.1016/j.virol.2009.11.045
Susskind MM (1980) A new gene of bacteriophage-P22 which regulates synthesis of anti-repressor. J Mol Biol 138(4):685–713. doi:10.1016/0022-2836(80)90060-1
Susskind MM, Botstein D, Wright A (1974) Superinfection exclusion by P22 prophage in lysogens of Salmonella typhimurium. 3. Failure of superinfecting phage DNA to enter siea + lysogens. Virology 62(2):350–366. doi:10.1016/0042-6822(74)90398-5
Tamas I, Klasson L, Canback B, Naslund AK, Eriksson AS, Wernegreen JJ, Sandstrom JP, Moran NA, Andersson SGE (2002) 50 million years of genomic stasis in endosymbiotic bacteria. Science 296(5577):2376–2379
Tanaka K, Furukawa S, Nikoh N, Sasaki T, Fukatsu T (2009) Complete WO phage sequences reveal their dynamic evolutionary trajectories and putative functional elements required for integration into the Wolbachia genome. Appl Environ Microbiol 75(17):5676–5686. doi:10.1128/Aem.01172-09
Thao ML, Moran NA, Abbot P, Brennan EB, Burckhardt DH, Baumann P (2000) Cospeciation of psyllids and their primary prokaryotic endosymbionts. Appl Environ Microbiol 66(7):2898–2905. doi:10.1128/Aem.66.7.2898-2905.2000
Tillmann HL, Heiken H, Knapik-Botor A, Heringlake S, Ockenga J, Wilber JC, Goergen B, Detmer J, McMorrow M, Stoll M, Schmidt RE, Manns MP (2001) Infection with GB virus C and reduced mortality among HIV-infected patients. N Engl J Med 345(10):715–724. doi:10.1056/NEJMoa010398
Tsuchida T, Koga R, Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science 303(5666):1989–1989
van der Wilk F, Dullemans AM, Verbeek M, van den Heuvel JFJM (1999) Isolation and characterization of APSE-1, a bacteriophage infecting the secondary endosymbiont of Acyrthosiphon pisum. Virology 262(1):104–113
van Ham RCHJ, Kamerbeek J, Palacios C, Rausell C, Abascal F, Bastolla U, Fernandez JM, Jimenez L, Postigo M, Silva FJ, Tamames J, Viguera E, Latorre A, Valencia A, Moran F, Moya A (2003) Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci USA 100(2):581–586. doi:10.1073/pnas.0235981100
Vautrin E, Vavre F (2009) Interactions between vertically transmitted symbionts: cooperation or conflict? Trends Microbiol 17(3):95–99. doi:10.1016/j.tim.2008.12.002
Vautrin E, Genieys S, Charles S, Vavre F (2008) Do vertically transmitted symbionts co-existing in a single host compete or cooperate? A modelling approach. J Evol Biol 21(1):145–161. doi:10.1111/j.1420-9101.2007.01460.x
Via S, Bouck AC, Skillman S (2000) Reproductive isolation between divergent races of pea aphids on two hosts. II. Selection against migrants and hybrids in the parental environments. Evolution 54(5):1626–1637
Vinson SB, Mourad AK, Sebesta DK (1994) Sources of possible host regulatory factors in Cardiochiles nigriceps (Hymenoptera, Braconidae). Arch Insect Biochem 26(2–3):197–209
Wagner SM, Martinez AJ, Ruan YM, Kim KL, Lenhart PA, Dehnel AC, Oliver KM, White JA (2015) Facultative endosymbionts mediate dietary breadth in a polyphagous herbivore. Funct Ecol. doi:10.1111/1365-2435.12459
Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28(2):127–181. doi:10.1016/j.femsre.2003.08.001
Weldon S (2015) Matryoshka mutualisms: developing the bacteriophage APSE-Hamiltonella defensa-Acyrthosiphon pisum system as a model for tripartite symbioses. University of Georgia Dissertation, Athens, GA
Weldon SR, Strand MR, Oliver KM (2013) Phage loss and the breakdown of a defensive symbiosis in aphids. Proc R Soc B Biol Sci 280(1751):20122103. doi:10.1098/rspb.2012.2103
Wernegreen JJ (2002) Genome evolution in bacterial endosymbionts of insects. Nat Rev Genet 3(11):850–861. doi:10.1038/nrg931
Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6(10):741–751. doi:10.1038/nrmicro1969
Wilkes TE, Darby AC, Choi JH, Colbourne JK, Werren JH, Hurst GDD (2010) The draft genome sequence of Arsenophonus nasoniae, son-killer bacterium of Nasonia vitripennis, reveals genes associated with virulence and symbiosis. Insect Mol Biol 19(1):59–73
Williams HTP (2013) Phage-induced diversification improves host evolvability. BMC Evol Biol 13(1):17
Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R, Brownlie JC, McGraw EA, Martin W, Esser C, Ahmadinejad N, Wiegand C, Madupu R, Beanan MJ, Brinkac LM, Daugherty SC, Durkin AS, Kolonay JF, Nelson WC, Mohamoud Y, Lee P, Berry K, Young MB, Utterback T, Weidman J, Nierman WC, Paulsen IT, Nelson KE, Tettelin H, O’Neill SL, Eisen JA (2004) Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2(3):327–341. doi:10.1371/journal.pbio.0020069
Xie JL, Vilchez I, Mateos M (2010) Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS One 5(8):e12149. doi:10.1371/journal.pone.0012149
Zug R, Hammerstein P (2012) Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. Plos One 7(6). Doi:10.1371/journal.pone.0038544