Skip to main content

Advertisement

SpringerLink
Log in

Longevity-modulating effects of symbiosis: insights from Drosophila–Wolbachia interaction

  • Review Article
  • Published:
Biogerontology Aims and scope Submit manuscript

Abstract

Microbial communities are known to significantly affect various fitness components and survival of their insect hosts, including Drosophila. The composition of symbiotic microbiota has been shown to change with the host’s aging. It is unclear whether these changes are caused by the aging process or, vice versa, they affect the host’s aging and longevity. Recent findings indicate that fitness and lifespan of Drosophila are affected by endosymbiotic bacteria Wolbachia. These effects, however, are inconsistent and have been reported both to extend and shorten longevity. The main molecular pathways underlying the lifespan-modulating effects of Wolbachia remain unclear, however insulin/insulin-like growth factor, immune deficiency, ecdysteroid synthesis and signaling and c-Jun N-terminal kinase pathways as well as heat shock protein synthesis and autophagy have been proposed to play a role. Here we revise the current evidence that elucidates the impact of Wolbachia endosymbionts on the aging processes in Drosophila.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Aggarwal K, Silverman N (2008) Positive and negative regulation of the Drosophila immune response. Bmb Rep 41:267–277

    Article  CAS  PubMed  Google Scholar 

  • Alexandrov ID, Alexandrova MV, Goryacheva II et al (2007) Removing endosymbiotic Wolbachia specifically decreases life span of females and competitiveness in a laboratory strain of Drosophila melanogaster. Russ J Genet+ 43(10):1147–1152

    Article  CAS  Google Scholar 

  • Anagnostou C, Dorsch M, Rohlfs M (2010) Influence of dietary yeasts on Drosophila melanogaster life-history traits. Entomol Exp Appl 136(1):1–11

    Article  Google Scholar 

  • Araújo A (2012) Are all mth-like genes involved in life span determination? Master thesis, Universidade do Porto

  • Ashburner M, Ball CA, Blake JA et al (2000) Gene Ontology: tool for the unification of biology. Nat Genet 25(1):25–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Attrill H, Falls K, Goodman JL et al (2015) FlyBase: establishing a Gene Group resource for Drosophila melanogaster. Nucleic Acids Res. doi:10.1093/nar/gkv1046

    PubMed  PubMed Central  Google Scholar 

  • Ballard JWO (2004) Sequential evolution of a symbiont inferred from the host: Wolbachia and Drosophila simulans. Mol Biol Evol 21(3):428–442

    Article  CAS  PubMed  Google Scholar 

  • Biagi E, Candela M, Franceschi C, Brigidi P (2011) The aging gut microbiota: new perspectives. Ageing Res Rev 10(4):428–429

    Article  PubMed  Google Scholar 

  • Biteau B, Karpac J, Supoyo S et al (2010) Life span extension by preserving proliferative homeostasis in Drosophila. PLoS Genet 6(10):e1001159

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bourtzis K, Nirgianaki A, Markakis G, Savakis C (1996) Wolbachia infection and cytoplasmic incompatibility in Drosophila species. Genetics 144(3):1063–1073

    CAS  PubMed  PubMed Central  Google Scholar 

  • Boyle L, O’Neill SL, Robertson HM, Karr TL (1993) Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260(5115):1796–1799

    Article  CAS  PubMed  Google Scholar 

  • Brandt A, Vilcinskas A (2013) The fruit fly Drosophila melanogaster as a model for aging research. In: Vilcinskas A (ed) Yellow biotechnology I. Springer, Berlin, Heidelberg, pp 63–77

  • Brennan LJ, Haukedal JA, Earle JC et al (2012) Disruption of redox homeostasis leads to oxidative DNA damage in spermatocytes of Wolbachia-infected Drosophila simulans. Insect Mol Biol 21(5):510–520

    Article  CAS  PubMed  Google Scholar 

  • Broderick NA, Lemaitre B (2012) Gut-associated microbes of Drosophila melanogaster. Gut Microbes 3(4):307–321

    Article  PubMed  PubMed Central  Google Scholar 

  • Brogiolo W, Stocker H, Ikeya T et al (2001) An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr Biol 11(4):213–221

    Article  CAS  PubMed  Google Scholar 

  • Broughton S, Partridge L (2009) Insulin/IGF-like signalling, the central nervous system and aging. Biochem J 418:1–12

    Article  CAS  PubMed  Google Scholar 

  • Broughton SJ, Piper MDW, Ikeya T et al (2005) Longer life span, altered metabolism and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc Natl Acad Sci USA 102:3105–3110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown AN, Lloyd VK (2015) Evidence for horizontal transfer of Wolbachia by a Drosophila mite. Exp Appl Acarol 66(3):301–311

    Article  PubMed  Google Scholar 

  • Brownlie JC, Cass BN, Riegler M et al (2009) Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Pathog 5:e1000368. doi:10.1371/journal.ppat.1000368

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brummel T, Ching A, Seroude L et al (2004) Drosophila lifespan enhancement by exogenous bacteria. Proc Natl Acad Sci USA 101:12974–12979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buchon N, Broderick NA, Lemaitre B (2013) Gut homeostasis in a microbial world: insights from Drosophila melanogaster. Nat Rev Microbiol 11(9):615–626

    Article  CAS  PubMed  Google Scholar 

  • Carrington LB, Leslie J, Weeks AR, Hoffmann AA (2009) The popcorn Wolbachia infection of Drosophila melanogaster: can selection alter Wolbachia longevity effects? Evolution 63(10):2648–2657

    Article  PubMed  Google Scholar 

  • Caturegli P, Asanovich KM, Walls JJ et al (2000) ankA: an Ehrlichia phagocytophila group gene encoding a cytoplasmic protein antigen with ankyrin repeats. Infect Immun 68(9):5277–5283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chandler JA, Lang JM, Bhatnagar S et al (2011) Bacterial communities of diverse Drosophila species: ecological context of a host–microbe model system. PLoS Genet 7(9):e1002272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Che M, Wang R, Li X, Wang HY, Zheng XF (2015) Expanding roles of superoxide dismutases in cell regulation and cancer. Drug Discov Today. doi:10.1016/j.drudis.2015.10.001

    PubMed  Google Scholar 

  • Cheng J, Palva AM, de Vos WM, Satokari R (2013) Contribution of the intestinal microbiota to human health: from birth to 100 years of age. In between pathogenicity and commensalism. Curr Top Microbiol Immunol 358:323–346

    CAS  PubMed  Google Scholar 

  • Chrostek E, Teixeira L (2015) Mutualism breakdown by amplification of Wolbachia genes. PLoS Biol. doi:10.1371/journal.pbio.1002065

    PubMed  PubMed Central  Google Scholar 

  • Chrostek E, Marialva MSP, Esteves SS et al (2013) Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: a phenotypic and phylogenomic analysis. PLoS Genet. doi:10.1371/journal.pgen.1003896

    PubMed  PubMed Central  Google Scholar 

  • Clancy DJ, Gems D, Harshman LG et al (2001) Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292(5514):104–106

    Article  CAS  PubMed  Google Scholar 

  • Combe BE, Defaye A, Bozonnet N et al (2014) Drosophila microbiota modulates host metabolic gene expression via IMD/NF-κB signaling. PLoS One 9(4):e94729

    Article  PubMed Central  CAS  Google Scholar 

  • Corby-Harris V, Pontaroli AC, Shimkets LJ et al (2007) Geographical distribution and diversity of bacteria associated with natural populations of Drosophila melanogaster. Appl Environ Microb 73(11):3470–3479

    Article  CAS  Google Scholar 

  • Costello EK, Stagaman K, Dethlefsen L et al (2012) The application of ecological theory toward an understanding of the human microbiome. Science 336(6086):1255–1262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cvejic S, Zhu Z, Felice SJ et al (2004) The endogenous ligand Stunted of the GPCR Methuselah extends life span in Drosophila. Nat Cell Biol 6(6):540–546

    Article  CAS  PubMed  Google Scholar 

  • Darby AC, Armstrong SD, Bah GS et al (2012) Analysis of gene expression from the Wolbachia genome of a filarial nematode supports both metabolic and defensive roles within the symbiosis. Genome Res 22(12):2467–2477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Bary A (1879) Die Erscheinungen der Symbiose. Trübner, Strassbourg

    Google Scholar 

  • Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92

    Article  CAS  PubMed  Google Scholar 

  • Dobson SL, Bourtzis K, Braig HR et al (1999) Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochem Molec Biol 29(2):153–160

    Article  CAS  Google Scholar 

  • Douglas AE, Werren JH (2016) Holes in the hologenome: why host-microbe symbioses are not holobionts. mBio 7(2):e02099-15

    Article  PubMed  PubMed Central  Google Scholar 

  • Dyer KA, Jaenike J (2004) Evolutionarily stable infection by a male-killing endosymbiont in Drosophila innubila molecular evidence from the host and parasite genomes. Genetics 168(3):1443–1455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eleftherianos I, Castillo JC (2012) Molecular mechanisms of aging and immune system regulation in Drosophila. Int J Mol Sci 13(8):9826–9844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eleftherianos I, Atri J, Accetta J, Castillo JC (2013) Endosymbiotic bacteria in insects: guardians of the immune system? Front Physiol 4:46

    Article  PubMed  PubMed Central  Google Scholar 

  • Engel P, Moran NA (2013) The gut microbiota of insects–diversity in structure and function. FEMS Microbiol Rev 37(5):699–735

    Article  CAS  PubMed  Google Scholar 

  • Erkosar B, Storelli G, Defaye A, Leulier F (2013) Host-intestinal microbiota mutualism:“learning on the fly”. Cell Host Microbe 13(1):8–14

    Article  CAS  PubMed  Google Scholar 

  • Fast EM, Toomey ME, Panaram K et al (2011) Wolbachia enhance Drosophila stem cell proliferation and target the germline stem cell niche. Science 334(6058):990–992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng Y, Yao Z, Klionsky DJ (2015) How to control self-digestion: transcriptional, post-transcriptional, and post-translational regulation of autophagy. Trends Cell Biol 25(6):354–363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Filomeni G, De Zio D, Cecconi F (2015) Oxidative stress and autophagy: the clash between damage and metabolic needs. Cell Death Differ 22(3):377–388

    Article  CAS  PubMed  Google Scholar 

  • Fleming JE, Reveillaud I, Niedzwiecki A (1992) Role of oxidative stress in Drosophila aging. Mutat Res 275(3):267–279

    Article  CAS  PubMed  Google Scholar 

  • Foster J, Ganatra M, Kamal I et al (2005) The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol 3:0599–0614

    Article  CAS  Google Scholar 

  • Frankel S, Rogina B (2012) Indy mutants: live long and prosper. Genet Aging 3:13

    Google Scholar 

  • Fry AJ, Rand DM (2002) Wolbachia interactions that determine Drosophila melanogaster survival. Evolution 56:1976–1981

    Article  PubMed  Google Scholar 

  • Fry AJ, Palmer MR, Rand DM (2004) Variable fitness effects of Wolbachia infection in Drosophila melanogaster. Heredity 93:379–389

    Article  CAS  PubMed  Google Scholar 

  • Fukai T, Ushio-Fukai M (2011) Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid Redox Signal 15(6):1583–1606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Futerman PH, Layen SJ, Kotzen ML et al (2006) Fitness effects and transmission routes of a microsporidian parasite infecting Drosophila and its parasitoids. Parasitology 132(04):479–492

    Article  CAS  PubMed  Google Scholar 

  • Gelino S, Hansen M (2012) Autophagy-an emerging anti-aging mechanism? J Clin Exp Pathol S 4:006. doi:10.4172/2161-0681.S4-006

    Google Scholar 

  • Giannakou ME, Goss M, Jünger MA et al (2004) Long-lived Drosophila with overexpressed dFOXO in adult fat body. Science 305(5682):361–361

    Article  CAS  PubMed  Google Scholar 

  • Gilbert SF (2014) Symbiosis as the way of eukaryotic life: the dependent co-origination of the body. J Biosci 39(2):201–209

    Article  PubMed  Google Scholar 

  • Gilbert SF (2016) Chapter twenty-two-developmental plasticity and developmental symbiosis: the return of eco-devo. Curr Top Dev Biol 116:415–433

    Article  PubMed  Google Scholar 

  • Giordano R, O’Neill SL, Robertson HM (1995) Wolbachia infections and the expression of cytoplasmic incompatibility in Drosophila sechellia and D. mauritiana. Genetics 140(4):1307–1317

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gonda RL, Garlena RA, Stronach B (2012) Drosophila heat shock response requires the JNK pathway and phosphorylation of mixed lineage kinase at a conserved serine-proline motif. PLoS One 7(7):e42369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grönke S, Clarke DF, Broughton S et al (2010) Molecular evolution and functional characterization of Drosophila insulin-like peptides. PLoS Genet 6(2):e1000857

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gupta D (2008) Peptidoglycan recognition proteins-maintaining immune homeostasis and normal development. Cell Host Microbe 3:273–274

    Article  CAS  PubMed  Google Scholar 

  • Haselkorn TS (2010) The Spiroplasma heritable bacterial endosymbiont of Drosophila. Fly 4(1):80–87

    Article  CAS  PubMed  Google Scholar 

  • Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322(5902):702–702

    Article  CAS  PubMed  Google Scholar 

  • Heintz C, Mair W (2014) You are what you host: microbiome modulation of the aging process cell 156(3):408–411

    CAS  PubMed  Google Scholar 

  • Helfand S, Rogina B (2003) Molecular genetics of aging in the fly: is this the end of the beginning? BioEssays 25:134–141

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann AA (1988) Partial cytoplasmic incompatibility between two Australian populations of Drosophila melanogaster. Entomol Exp Appl 48(1):61–67

    Article  Google Scholar 

  • Hoffmann AA, Turelli M, Simmons GM (1986) Unidirectional incompatibility between populations of Drosophila simulans. Evolution 692–701

  • Hughes DP, Pierce NE, Boomsma JJ (2008) Social insect symbionts: evolution in homeostatic fortresses. Trends Ecol Evol 23(12):672–677

    Article  PubMed  Google Scholar 

  • Hurst GD, Johnson AP, vd 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 

  • Ikeya T, Broughton S, Alic N et al (2009) The endosymbiont Wolbachia increases insulin/IGF-like signalling in Drosophila. Proc R Soc Lond B Biol Sci 276:3799–3807

    Article  CAS  Google Scholar 

  • Jaenike J (2007) Spontaneous emergence of a new Wolbachia phenotype. Evolution 61(9):2244–2252

    Article  PubMed  Google Scholar 

  • Johnson KN (2015) Bacteria and antiviral immunity in insects. Curr Opin Insect Sci 8:97–103

    Article  Google Scholar 

  • Junnila RK, List EO, Berryman DE et al (2013) The GH/IGF-1 axis in ageing and longevity. Nat Rev Endocrinol 9(6):366–376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaneko T, Yano T, Aggarwal K et al (2006) PGRP-LC and PGRP-LE have essential yet distinct functions in the Drosophila immune response to monomeric DAP-type peptidoglycan. Nat Immunol 7:715–723

    Article  CAS  PubMed  Google Scholar 

  • Karpac J, Jasper H (2009) Insulin and JNK: optimizing metabolic homeostasis and lifespan. Trends Endocrinol Metab 20(3):100–106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karunanithi S, Brown IR (2015) Heat shock response and homeostatic plasticity. Frontiers in cellular neuroscience 9:68

    Article  PubMed  PubMed Central  Google Scholar 

  • Keebaugh ES, Schlenke TA (2014) Insights from natural host–parasite interactions: the Drosophila model. Dev Comp Immunol 42(1):111–123

    Article  PubMed  Google Scholar 

  • Kikuchi Y (2009) Endosymbiotic bacteria in insects: their diversity and culturability. Microbes Environ 24(3):195–204

    Article  PubMed  Google Scholar 

  • Kriesner P, Hoffmann AA, Lee SF et al (2013) Rapid sequential spread of two Wolbachia variants in Drosophila simulans. PLoS Pathog 9(9):e1003607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Landis GN, Tower J (2005) Superoxide dismutase evolution and life span regulation. Mech Ageing Dev 126(3):365–379

    Article  CAS  PubMed  Google Scholar 

  • Lemaitre B, Hoffmann J (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25:697–743

    Article  CAS  PubMed  Google Scholar 

  • Libert S, Chao Y, Chu X, Pletcher SD (2006) Trade-offs between longevity and pathogen resistance in Drosophila melanogaster are mediated by NFkappaB signaling. Aging Cell 5(6):533–543

    Article  CAS  PubMed  Google Scholar 

  • Libert S, Chao Y, Zwiener J, Pletcher SD (2008) Realized immune response is enhanced in long-lived puc and chico mutants but is unaffected by dietary restriction. Mol Immunol 45(3):810–817

    Article  CAS  PubMed  Google Scholar 

  • Lin YJ, Seroude L, Benzer S (1998) Extended life-span and stress resistance in the Drosophila mutant methuselah. Science 282(5390):943–946

    Article  CAS  PubMed  Google Scholar 

  • Madeo F, Tavernarakis N, Kroemer G (2010) Can autophagy promote longevity? Nat Cell Biol 12(9):842–846

    Article  CAS  PubMed  Google Scholar 

  • Madeo F, Zimmermann A, Maiuri MC, Kroemer G (2015) Essential role for autophagy in life span extension. J Clin Invest 125(1):85–93

    Article  PubMed  PubMed Central  Google Scholar 

  • Maillet F, Bischoff V, Vignal C et al (2008) The Drosophila peptidoglycan recognition protein PGRP-LF Blocks PGRP-LC and IMD/JNK pathway activation. Cell Host Microbe 3(5):293–303

    Article  CAS  PubMed  Google Scholar 

  • Markov AV, Lazebny OE, Goryacheva II et al (2009) Symbiotic bacteria affect mating choice in Drosophila melanogaster. Anim Behav 77(5):1011–1017

    Article  Google Scholar 

  • Martin BD, Schwab E (2012) Symbiosis:“Living together” in chaos. Stud Hist Biol 4(4):7–25

    Google Scholar 

  • Martinez J, Ok S, Smith S et al (2015) Should symbionts be nice or selfish? Antiviral effects of Wolbachia are costly but reproductive parasitism is not. PLoS Pathog 11:5021–5021

    Article  CAS  Google Scholar 

  • Martinez-Lopez N, Athonvarangkul D, Singh R (2015) Autophagy and aging. Adv Exp Med Biol 847:73–87

    Article  PubMed  PubMed Central  Google Scholar 

  • Masui S, Sasaki T, Ishikawa H (2000) Genes for the type IV secretion system in an intracellular symbiont, Wolbachia, a causative agent of various sexual alterations in arthropods. J Bacteriol 182(22):6529–6531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mateos M, Castrezana SJ, Nankivell BJ et al (2006) Heritable endosymbionts of Drosophila. Genetics 174(1):363–376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McFall-Ngai M, Hadfield MG, Bosch TC et al (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA 110(9):3229–3236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mercot H, Llorente B, Jacques M et al (1995) Variability within the Seychelles cytoplasmic incompatibility system in Drosophila simulans. Genetics 141(3):1015–1023

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miller WJ, Ehrman L, Schneider D (2010) Infectious speciation revisited: impact of symbiont-depletion on female fitness and mating behavior of Drosophila paulistorum. PLoS Pathog 6(12):e1001214

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Min KT, Benzer S (1997) Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc Natl Acad Sci USA 94(20):10792–10796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moore MN, Shaw JP, Ferrar Adams DR, Viarengo A (2015) Anti-oxidative cellular protection effect of fasting-induced autophagy as a mechanism for hormesis. Mar Environ Res 107:35–44

    Article  CAS  PubMed  Google Scholar 

  • Morrow G, Samson M, Michaud S, Tanguay RM (2004) Overexpression of the small mitochondrial Hsp22 extends Drosophila life span and increases resistance to oxidative stress. The FASEB J 18(3):598–599

    CAS  PubMed  Google Scholar 

  • Myllymaki H, Valanne S, Ramet M (2014) The Drosophila imd signaling pathway. J Immunol 192:3455–3462

    Article  PubMed  CAS  Google Scholar 

  • Nässel DR, Liu Yiting, Luo Jiangnan (2015) Insulin/IGF signaling and its regulation in Drosophila. Gen Comp Endocrinol. doi:10.1016/j.ygcen.2014.11.021

    PubMed  Google Scholar 

  • Negri I (2011) Wolbachia as an “infectious” extrinsic factor manipulating host signaling pathways. Front Endocrinol 2:115–115

    Google Scholar 

  • Negri I, Pellecchia M (2012) Sex steroids in insects and the role of the endosymbiont Wolbachia: a new perspective. In: Raghvendra KD (ed) Sex hormones, InTech publisher, p 353–374

  • Negri I, Pellecchia M, Grève P et al (2010) Sex and stripping: the key to the intimate relationship between Wolbachia and host. Commun Integr Biol 3(2):110–115

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Brien LE, Soliman SS, Li X, Bilder D (2011) Altered modes of stem cell division drive adaptive intestinal growth. Cell 147:603–614

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Olsen K, Reynolds KT, Hoffmann AA (2001) A field cage test of the effects of the endosymbiont Wolbachia on Drosophila melanogaster. Heredity 86(6):731–737

    Article  CAS  PubMed  Google Scholar 

  • O’Neill SL, Karr TL (1990) Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature 348(6297):178–180

    Article  PubMed  Google Scholar 

  • Orme MH, Leevers SJ (2005) Flies on steroids: the interplay between ecdysone and insulin signaling. Cell Metab 2(5):277–278

    Article  CAS  PubMed  Google Scholar 

  • Osborne SE, San Leong Y, O’Neill SL, Johnson KN (2009) Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog 5(11):e1000656

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ottaviani E, Ventura N, Mandrioli M et al (2011) Gut microbiota as a candidate for life span extension: an ecological/evolutionary perspective targeted on living organisms as metaorganisms. Biogerontology 12(6):599–609

    Article  CAS  PubMed  Google Scholar 

  • Paaby AB, Schmidt PS (2008) Functional significance of allelic variation at methuselah, an aging gene in Drosophila. PLoS One 3(4):e1987

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Paaby AB, Schmidt PS (2009) Dissecting the genetics of longevity in Drosophila melanogaster. Fly 3(1):29–38

    Article  CAS  PubMed  Google Scholar 

  • Paik D, Jang YG, Lee YE et al (2012) Misexpression screen delineates novel genes controlling Drosophila life span. Mech Ageing Dev 133(5):234–245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Papafotiou G, Oehler S, Savakis C, Bourtzis K (2011) Regulation of Wolbachia ankyrin domain encoding genes in Drosophila gonads. Res Microbiol 162(8):764–772

    Article  CAS  PubMed  Google Scholar 

  • Partridge L, Brüning JC (2008) Forkhead transcription factors and ageing. Oncogene 27(16):2351–2363

    Article  CAS  PubMed  Google Scholar 

  • Petrosyan A, Gonçalves ÓF, Hsieh IH, Saberi K (2014) Improved functional abilities of the life-extended Drosophila mutant Methuselah are reversed at old age to below control levels. Age 36(1):213–221

    Article  PubMed  Google Scholar 

  • Pletcher SD, Macdonald SJ, Marguerie R et al (2002) Genome-wide transcript profiles in aging and calorically restricted Drosophila melanogaster. Curr Biol 12(9):712–723

    Article  CAS  PubMed  Google Scholar 

  • Ponton F, Wilson K, Holmes A et al (2015) Macronutrients mediate the functional relationship between Drosophila and Wolbachia. P R Soc Lond B Biol Sci. doi:10.1098/rspb.2014.2029

    Google Scholar 

  • Ren C, Webster P, Finkel SE, Tower J (2007) Increased internal and external bacterial load during Drosophila aging without life-span trade-off. Cell Metab 6:144–152

    Article  CAS  PubMed  Google Scholar 

  • Ridley EV, Wong AC, Douglas AE (2013) Microbe-dependent and nonspecific effects of procedures to eliminate the resident microbiota from Drosophila melanogaster. Appl Environ Microb 79(10):3209–3214

    Article  CAS  Google Scholar 

  • Ristow M, Schmeisser K (2014) Mitohormesis: promoting health and lifespan by increased levels of reactive oxygen species (ROS). Dose Response 12(2):288–341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rogers RP, Rogina B (2015) The role of INDY in metabolism, health and longevity. Front Genet. doi:10.3389/fgene.2015.00204

    PubMed  PubMed Central  Google Scholar 

  • Rogina B, Helfand SL (2013) Indy mutations and Drosophila longevity. Front Genet. doi:10.3389/fgene.2013.00047

    PubMed  PubMed Central  Google Scholar 

  • Rosenberg E, Zilber-Rosenberg I (2016) Microbes drive evolution of animals and plants: the hologenome concept. mBio 7(2):e01395–15

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosenberg E, Sharon G, Zilber-Rosenberg I (2009) The hologenome theory of evolution contains Lamarckian aspects within a Darwinian framework. Environ Microbiol 11(12):2959–2962

    Article  PubMed  Google Scholar 

  • Royet J, Dziarski R (2007) Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences. Nat Rev Microbiol 5(4):264–277

    Article  CAS  PubMed  Google Scholar 

  • Russell JA, Dubilier N, Rudgers JA (2014) Nature’s microbiome: introduction. Mol Ecol 23(6):1225–1237

    Article  PubMed  Google Scholar 

  • Sadagurski M, White MF (2013) Integrating metabolism and longevity through insulin and IGF1 signaling. Endocrinol Metab Clin North Am 42(1):127–148

    Article  PubMed  Google Scholar 

  • Saffo MB (1992) Coming to terms with a field: words and concepts in symbiosis. Symbiosis 14(1–3):17–31

    Google Scholar 

  • Serbus LR, White PM, Silva JP et al (2015) The impact of host diet on Wolbachia titer in Drosophila. PLoS Pathog 11(3):e1004777

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Serga SV, Kozeretskaya IA (2013) The puzzle of Wolbachia spreading out through natural populations of Drosophila melanogaster. Zh Obshch Biol 74(2):99–111

    CAS  PubMed  Google Scholar 

  • Serga S, Maistrenko O, Rozhok A et al (2014) Fecundity as one of possible factors contributing to the dominance of the wMel genotype of Wolbachia in natural populations of Drosophila melanogaster. Symbiosis 63(1):11–17. doi:10.1007/s13199-014-0283-1

    Article  Google Scholar 

  • Seroude L, Brummel T, Kapahi P, Benzer S (2002) Spatio-temporal analysis of gene expression during aging in Drosophila melanogaster. Aging Cell 1(1):47–56

    Article  CAS  PubMed  Google Scholar 

  • Sharon G, Segal D, Ringo JM et al (2010) Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci USA 107(46):20051–20056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheeley SL, McAllister BF (2009) Mobile male-killer: similar Wolbachia strains kill males of divergent Drosophila hosts. Heredity 102(3):286–292

    Article  CAS  PubMed  Google Scholar 

  • Shin SC, Kim SH, You H et al (2011) Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334(6056):670–674

    Article  CAS  PubMed  Google Scholar 

  • Simon AF, Shih C, Mack A, Benzer S (2003) Steroid control of longevity in Drosophila melanogaster. Science 299(5611):1407–1410

    Article  CAS  PubMed  Google Scholar 

  • Simonsen A, Cumming RC, Brech A et al (2008) Promoting basal levels of autophagy in the nervous system enhances longevity and oxidant resistance in adult Drosophila. Autophagy 4(2):176

    Article  CAS  PubMed  Google Scholar 

  • Simpson SJ, Raubenheimer D (2012) The nature of nutrition: a unifying framework from animal adaptation to human obesity. Princeton University Press, Princeton

    Google Scholar 

  • Siozios S, Ioannidis P, Klasson L et al (2013) The diversity and evolution of Wolbachia ankyrin repeat domain genes. PLoS One 8(2):e55390. doi:10.1371/journal.pone.0055390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slack C, Giannakou ME, Foley A et al (2011) dFOXO-independent effects of reduced insulin-like signaling in Drosophila. Aging Cell 10(5):735–748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Starr DJ, Cline TW (2002) A host-parasite interaction rescues Drosophila oogenesis defects. Nature 418(6893):76–79

    Article  CAS  PubMed  Google Scholar 

  • Staubach F, Baines JF, Künzel S et al (2013) Host species and environmental effects on bacterial communities associated with Drosophila in the laboratory and in the natural environment. PLoS One 8(8):e70749. doi:10.1371/journal.pone.0070749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Storelli G, Defaye A, Erkosar B et al (2011) Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through Tor-dependent nutrient sensing. Cell Metab 14(3):403–414

    Article  CAS  PubMed  Google Scholar 

  • Szumiel I (2012) Radiation hormesis: autophagy and other cellular mechanisms. Int J Radiat Biol 88(9):619–628

    Article  CAS  PubMed  Google Scholar 

  • Tatar M, Khazaeli AA, Curtsinger JW (1997) Chaperoning extended life. Nature 390(6655):30–30

    Article  CAS  PubMed  Google Scholar 

  • Teixeira L, Ferreira Á, Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6(12):e1000002

    Article  PubMed Central  CAS  Google Scholar 

  • Toivonen JM, Walker GA, Martinez-Diaz P et al (2007) No influence of Indy on life span in Drosophila after correction for genetic and cytoplasmic background effects. PLoS Genet 3(6):e95. doi:10.1371/journal.pgen.0030095

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tower J (2011) Heat shock proteins and Drosophila aging. Exp Geront 46(5):355–362

    Article  CAS  Google Scholar 

  • Unckless RL, Jaenike J (2012) Maintenance of a male-killing Wolbachia in Drosophila innubila by male-killing dependent and male-killing independent mechanisms. Evolution 66(3):678–689

    Article  PubMed  Google Scholar 

  • Versace E, Nolte V, Pandey RV et al (2014) Experimental evolution reveals habitat-specific fitness dynamics among Wolbachia clades in Drosophila melanogaster. Mol Ecol 23(4):802–814

    Article  PubMed  PubMed Central  Google Scholar 

  • Vogel C, Marcotte EM (2012) Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat Rev Genet 13(4):227–232

    CAS  PubMed  PubMed Central  Google Scholar 

  • Voronin D, Cook DA, Steven A, Taylor MJ (2012) Autophagy regulates Wolbachia populations across diverse symbiotic associations. Proc Natl Acad Sci USA 109(25):E1638–E1646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang MC, Bohmann D, Jasper H (2003) JNK signaling confers tolerance to oxidative stress and extends life span in Drosophila. Dev Cell 5(5):811–816

    Article  CAS  PubMed  Google Scholar 

  • Wang MC, Bohmann D, Jasper H (2005) JNK extends life span and limits growth by antagonizing cellular and organism-wide responses to insulin signaling. Cell 121(1):115–125

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Zhou C, He Z (2012) Wolbachia infection decreased the resistance of Drosophila to lead. PLoS One 7(3):e32643. doi:10.1371/journal.pone.0032643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Karpac J, Jasper H (2014) Promoting longevity by maintaining metabolic and proliferative homeostasis. J Exp Biol 217(1):109–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weinert LA, Araujo-Jnr EV, Ahmed MZ et al (2015) The incidence of bacterial endosymbionts in terrestrial arthropods. Proc R Soc Lond B Biol Sci. doi:10.1098/rspb.2015.0249

    Google Scholar 

  • Werren JH (1997) Biology of Wolbachia. Annu Rev Entomol 42(1):587–609

    Article  CAS  PubMed  Google Scholar 

  • Werren JH, Jaenike J (1995) Wolbachia and cytoplasmic incompatibility in mycophagous Drosophila and their relatives. Heredity 75(3):320–326

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wong CN, Ng P, Douglas AE (2011) Low-diversity bacterial community in the gut of the fruitfly Drosophila melanogaster. Environ Microbiol 13:1889–1900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong AC, Chaston JM, Douglas AE (2013) The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis. ISME J 7(10):1922–1932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong ZS, Brownlie JC, Johnson KN (2015) Oxidative stress correlates with Wolbachia-mediated antiviral protection in Wolbachia–Drosophila associations. Appl Environ Microb 81:3001–3005

    Article  CAS  Google Scholar 

  • Wu M, Sun LV, Vamathevan J et al (2004) Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2:0327–0341

    Article  CAS  Google Scholar 

  • Wu H, Wang MC, Bohmann D (2009) JNK protects Drosophila from oxidative stress by trancriptionally activating autophagy. Mech Dev 126(8):624–637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xi Z, Gavotte L, Xie Y, Dobson SL (2008) Genome-wide analysis of the interaction between the endosymbiotic bacterium Wolbachia and its Drosophila host. BMC Genom 9(1):1

    Article  CAS  Google Scholar 

  • Yamada R, Floate KD, Riegler M, O’Neill SL (2007) Male development time influences the strength of Wolbachia-induced cytoplasmic incompatibility expression in Drosophila melanogaster. Genetics 177(2):801–808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zapata HJ, Quagliarello VJ (2015) The microbiota and microbiome in aging: potential implications in health and age-related diseases. J Am Geriatr Soc 63:776–781

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng Y, Wang JL, Liu C et al (2011) Differentially expressed profiles in the larval testes of Wolbachia infected and uninfected Drosophila. BMC Genom 12(1):595

    Article  CAS  Google Scholar 

  • Zhu CT, Chang C, Reenan RA, Helfand SL (2014) Indy gene variation in natural populations confers fitness advantage and life span extension through transposon insertion. Aging (Albany NY) 6(1):58

    Article  CAS  Google Scholar 

  • Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32(5):723–735

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Zhiyong Xi and Dr. Stephen Dobson from the Department of Entomology of the University of Kentucky for providing valuable information about genes that change expression under Wolbachia infection in the Drosophila S2 cell line. The authors acknowledge Dr. Elena Pasyukova from Institute of Molecular Genetics of the Russian Academy of Sciences for a critical review of manuscript draft. The authors thank Dr. Andrii Rozhok from the Department of Biochemistry and Molecular Genetics of University of Colorado School of Medicine for critical comments and for editing grammar in the manuscript.

Author information

Authors and Affiliations

  1. Department of Veterinary and Microbiological Sciences, North Dakota State University, PO BOX 6050, Fargo, ND, 58108-6050, USA

    Oleksandr M. Maistrenko

  2. Taras Shevchenko National University of Kyiv, Kiev, Ukraine

    Svitlana V. Serga & Iryna A. Kozeretska

  3. Laboratory of Epigenetics, D.F. Chebotarev State Institute of Gerontology NAMS of Ukraine, Kiev, Ukraine

    Alexander M. Vaiserman

Authors
  1. Oleksandr M. Maistrenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Svitlana V. Serga
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexander M. Vaiserman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Iryna A. Kozeretska
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Oleksandr M. Maistrenko.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maistrenko, O.M., Serga, S.V., Vaiserman, A.M. et al. Longevity-modulating effects of symbiosis: insights from Drosophila–Wolbachia interaction. Biogerontology 17, 785–803 (2016). https://doi.org/10.1007/s10522-016-9653-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10522-016-9653-9

Keywords

Search

Navigation