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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

    Book  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bordenstein SR, Bordenstein SR (2011) Temperature affects the tripartite interactions between bacteriophage WO, Wolbachia, and cytoplasmic incompatibility. PLoS One 6(12), e29106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bordenstein SR, Reznikoff WS (2005) Mobile DNA in obligate intracellular bacteria. Nat Rev Microbiol 3(9):688–699. doi:10.1038/nrmicro1233

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Brady CM, White JA (2013) Cowpea aphid (Aphis craccivora) associated with different host plants has different facultative endosymbionts. Ecol Entomol 38(4):433–437

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Calendar R, Abedon ST (2005) The bacteriophages, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen DQ, Purcell AH (1997) Occurrence and transmission of facultative endosymbionts in aphids. Curr Microbiol 34(4):220–225

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cloutier C, Douglas AE (2003) Impact of a parasitoid on the bacterial symbiosis of its aphid host. Entomol Exp Appl 109(1):13–19

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Digilio MC, Isidoro N, Tremblay E, Pennacchio F (2000) Host castration by Aphidius ervi venom proteins. J Insect Physiol 46(6):1041–1050

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Douglas AE (1989) Mycetocyte symbiosis in insects. Biol Rev 64(4):409–434. doi:10.1111/j.1469-185X.1989.tb00682.x

    Article  CAS  PubMed  Google Scholar 

  • Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37

    Article  CAS  PubMed  Google Scholar 

  • Duron O (2014) Arsenophonus insect symbionts are commonly infected with APSE, a bacteriophage involved in protective symbiosis. FEMS Microbiol Ecol 90(1):184–194

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hamilton PT, Perlman SJ (2013) Host defense via symbiosis in Drosophila. Plos Pathog 9(12). doi:10.1371/journal.ppat.1003808

    Google Scholar 

  • Hansen AK, Vorburger C, Moran NA (2012) Genomic basis of endosymbiont-conferred protection against an insect parasitoid. Genome Res 22(1):106–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hatfull GF (2008) Bacteriophage genomics. Curr Opin Microbiol 11(5):447–453. doi:10.1016/j.mib.2008.09.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He XZ (2008) Reproductive behavior of Aphidius ervi Haliday (Hymenoptera: Aphidiidae). Massey University Dissertation, Palmerston North, New Zealand

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Horvath P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327(5962):167–170. doi:10.1126/science.1179555

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Jaenike J (2012) Population genetics of beneficial heritable symbionts. Trends Ecol Evol 27(4):226–232. doi:10.1016/j.tree.2011.10.005

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lawrence PO (1990) Serosal cells of Biosteres longicaudatus (Hymenoptera, Braconidae) – ultrastructure and release of polypeptides. Arch Insect Biochem 13(3–4):199–216

    Article  CAS  Google Scholar 

  • Lenski RE (1988) Dynamics of interactions between bacteria and virulent bacteriophage. Adv Microb Ecol 10:1–44

    Article  CAS  Google Scholar 

  • Lin L, Bitner R, Edlin G (1977) Increased reproductive fitness of Escherichia coli Lambda-lysogens. J Virol 21(2):554–559

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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)

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Martinez AJ, Kim KL, Harmon JP, Oliver KM (2016) Specificity of multi-modal aphid defenses against two rival parasitoids. PLoS One

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • McCutcheon JP, Moran NA (2012) Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10(1):13–26. doi:10.1038/Nrmicro2670

    CAS  Google Scholar 

  • McDaniel L, Houchin LA, Williamson SJ, Paul JH (2002) Plankton blooms – Lysogeny in marine Synechococcus. Nature 415(6871):496. doi:10.1038/415496a

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montllor CB, Maxmen A, Purcell AH (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27(2):189–195

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Moran NA, Wernegreen JJ (2000) Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol Evol 15(8):321–326

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Nováková E, Hypša V, Moran NA (2009) Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiol 9(1):143

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ptashne M (2004) A genetic switch: phage lambda revisited, vol 3. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roossinck MJ (2011) The good viruses: viral mutualistic symbioses. Nat Rev Microbiol 9(2):99–108. doi:10.1038/Nrmicro2491

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Scarborough CL, Ferrari J, Godfray HCJ (2005) Aphid protected from pathogen by endosymbiont. Science 310(5755):1781. doi:10.1126/science.1120180

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Strand MR (2010) Polydnaviruses. In: Asagari S, Johnson K (eds) Insect virology. Caister Scientific Press, Norfolk, pp 171–197

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Tsuchida T, Koga R, Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science 303(5666):1989–1989

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28(2):127–181. doi:10.1016/j.femsre.2003.08.001

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wernegreen JJ (2002) Genome evolution in bacterial endosymbionts of insects. Nat Rev Genet 3(11):850–861. doi:10.1038/nrg931

    Article  CAS  PubMed  Google Scholar 

  • Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6(10):741–751. doi:10.1038/nrmicro1969

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Williams HTP (2013) Phage-induced diversification improves host evolvability. BMC Evol Biol 13(1):17

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Google Scholar