Abstract
Insects are major contributors to natural as well as to man-managed ecosystems and largely bear on human affairs, both positively and negatively. They have varied microbial communities that provide them with nutritional benefits, enhanced defenses, and improved stress resistance. This review centers on nutritional contributions of gut symbionts to their insect hosts. It explores the complex relationships between symbiont, host nutrition, and host life cycle, summarizing some of the important developments in symbiotic science. It particularly focuses on Tephritidae fruit flies that cause enormous agricultural damage. It exposes the present knowledge on the symbionts of the tephritids Ceratitis capitata (the Mediterranean fruit fly) and Bactrocera oleae (the Olive fly) and recapitulates recent advances in the improvement of the performance of mass-reared sterile males used in sterile insect technique to combat the medfly.
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References
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 32:402–407
Amiot M-J, Fleuriet A, Macheix J-J (1989) Accumulation of oleuropein derivatives during olive maturation. Phytochemistry 28:67–69
Anand AA, Vennison JS, Sankar GS, Prabhu IGD, Vasan TP, Raghuraman GT, Geffrey JC, Vendan ES (2010) Isolation and characterization of bacteria from the gut of Bombyx mori that degrade cellulose, xylan, pectin and starch and their impact on digestion. J Insect Sci 10:1–20
Appel HM (1994) The chewing herbivore gut lumen: physicochemical conditions and their impact on plant nutrients, allelochemicals and insect pathogens. In: Bernays EA (ed) Insect–plant interactions, vol 1. CRC Press, Boca Raton, pp 209–221
Baumann P, Moran NA, Baumann L (2006) Bacteriocyte-associated endosymbionts of insects. In: Dworkin M, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes: symbiotic associations, biotechnology, applied microbiology, vol 1. Springer, New York, pp 403–438
Behar A, Yuval B, Jurkevitch E (2005) Enterobacteria-mediated nitrogen fixation in natural populations of the fruit fly Ceratitis capitata. Mol Ecol 14:2637–2643
Behar A, Jurkevitch E, Yuval B (2008a) Bringing back the fruit into fruit fly-bacteria interactions. Mol Ecol 17:1375–1386
Behar A, Yuval B, Jurkevitch E (2008b) Gut bacterial communities in the Mediterranean fruit fly (Ceratitis capitata) and their impact on host longevity. J Insect Physiol 54:1377–1383
Ben Ami E, Yuval B, Jurkevitch E (2010) Manipulation of the microbiota of mass-reared Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae) improves sterile male sexual performance. ISME J 4:28–37
Ben Yosef M, Jurkevitch E, Yuval B (2008a) Effect of bacteria on nutritional status and reproductive success of the Mediterranean fruit fly Ceratitis capitata. Physiol Entomol 33:145–154
Ben Yosef M, Behar A, Jurkevitch E, Yuval B (2008b) Bacteria–diet interactions affect longevity in the medfly – Ceratitis capitata. J Appl Entomol 132:690–694
Ben Yosef M, Aharon Y, Jurkevitch E, Yuval B (2010) Give us the tools and we will do the job: symbiotic bacteria affect olive fly fitness in a diet dependent fashion. Proc R Soc B Biol Sci 277:1545–1552
Bignell DE, Egelton P (2000) Termites in ecosystems. In: Abe T, Bignel BE, Higashi M (eds) Termites: evolution, sociality, symbiosis, ecology. Kluwer Academic, Dordrecht, pp 363–388
Breznak J, Switzer J (1986) Acetate synthesis from H2 plus CO2 by termite gut microbes. Appl Environ Microbiol 52:623–630
Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8:218–230
Brownlie JC, Johnson KN (2009) Symbiont-mediated protection in insect hosts. Trends Microbiol 17:348–354
Brownlie JC, Cass BN, Riegler M, Witsenburg JJ, Iturbe-Ormaetxe I, McGraw EA, O’Neill SL (2009) Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Pathog 5:e1000368
Brune A (2006) Symbiotic associations between termites and prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 439–474
Burton M, Burton R (2002) International wildlife encyclopedia. Marshall Cavendish Corporation, Tarrytown
Bustamante RNC, Martius C (1998) Nutritional preferences of wood-feeding termites inhabiting floodplain forests of the Amazon River. Brazil Acta Amazonica 28:301–307
Capuzzo C, Firrao G, Mazzon L, Squartini A, Girolami V (2005) ‘Candidatus Erwinia dacicola’, a coevolved symbiotic bacterium of the olive fly Bactrocera oleae (Gmelin). Int J Syst Evol Microbiol 55:1641–1647
Cheng Q, Aksoy S (1999) Tissue tropism, transmission and expression of foreign genes in vivo in midgut symbionts of tsetse flies. Insect Mol Biol 8:125–132
Christenson LD, Foote RH (1960) Biology of fruit flies. Annu Rev Entomol 5:171–92
Dedeine F, Vavre F, Fleury F, Loppin B, Hochberg ME, Boulétreau M (2001) Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci USA 98:6247–6252
Douglas AE (2006) Phloem-sap feeding by animals: problems and solutions. J Exp Bot 57:747–754
Drew RAI, Yuval B (2000) The evolution of fruit fly feeding behavior. In: Aluja M, Norrbom A (eds) Fruit flies, phylogeny and evolution of behavior. CRC Press, Boca Raton, pp 731–749
Dunn AK, Stabb EV (2005) Culture-independent characterization of the microbiota of the ant lion Myrmeleon mobilis (Neuroptera: Myrmeleontidae). Appl Environ Microbiol 71:8784–8794
Duyck PF, David P, Quilici S (2004) A review of relationships between interspecific competition and invasions in fruit flies (Diptera: Tephritidae). Ecol Entomol 29:511–520
Egami I, Iiyama K, Zhang P, Chieda Y, Ino N, Hasegawa K, Lee JM, Kusakabe T, Yasunaga-Aoki C, Shimizu S (2009) Insecticidal bacterium isolated from an antlion larva from Munakata, Japan. J Appl Entomol 133:117–124
Estes AM, Hearn DJ, Bronstein JL, Pierson EA (2009) The olive fly endosymbiont, “Candidatus Erwinia dacicola,” switches from an intracellular existence to an extracellular existence during host insect development. Appl Environ Microbiol 75:7097–7106
Eutick ML, Veivers P, O’Brien RW, Slaytor M (1978) Dependence of the higher termite, Nasutitermes exitiosus and the lower termite, Coptotermes lacteus on their gut flora. J Insect Physiol 24:363–368
Evenhuis NL, Pape T, Pont AC, Thompson FC (2008) Database of World Diptera. http://www.diptera.org/biosys.htm
Fukatsu T, Hosokawa T (2009) Capsule-transmitted obligate gut bacterium of plataspid stinkbugs: a novel model system for insect symbiosis studies. In: Bourtzis K, Miller TA (eds) Insect symbiosis, vol 3. CRC Press, Boca Raton
Gallai N, Salles J-M, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821
Gavriel S, Jurkevitch E, Gazit Y, Yuval B (2011) Bacterially enriched diet improves sexual performance of sterile male Mediterranean fruit flies. J Appl Entomol. doi:10.1111/j.1439-0418.2010.01605.x
Gulian PJ, Cranston PS (2010) The insects: an outline of entomology. Wiley, London, pp. 565
Headrick DH, Goeden RD (1994) Reproductive behavior of California fruit flies and the classification and evolution of Tephritidae (Diptera) mating systems. Studia Dipterol 1:195–252
Hendrichs J, Franz G, Rendon P (1995) Increased effectiveness and applicability of the sterile insect technique through male-only releases for control of Mediterranean fruit flies during fruiting seasons. J Appl Entomol 119:371–377
Hongoh Y, Sharma VK, Prakash T, Noda S, Taylor TD, Kudo T, Sakaki Y, Toyoda A, Hattori M, Ohkuma M (2008a) Complete genome of the uncultured Termite Group 1 bacteria in a single host protist cell. Proc Natl Acad Sci 1–5:5555–5560
Hongoh Y, Sharma VK, Prakash T, Noda S, Taylor TD, Kudo T, Sakaki Y, Toyoda A, Hattori M, Ohkuma M (2008b) Genome of an endosymbiont coupling N2 fixation to cellulolysis within protist cells in termite gut. Science 322:1108–1109
Hosokawa T, Kikuchi Y, Nikoh N, Shimada M, Fukatsu T (2006) Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLoS Biol 4:e337
Hosokawa T, Koga R, Kikuchi Y, Meng XY, Fukatsu T (2010) Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci 107:769–774
Hoy MA, Jeyaprakash A (2005) Microbial diversity in the predatory mite Metaseiulus occidentalis (Acari: Phytoseiidae) and its prey, Tetranychus urticae (Acari: Tetranychidae). Biol Control 32:427–441
Hypsa V, Novakova E (2009) Inset symbionts and molecular phylogenetics. In: Bourtzis K, Miller TA (eds) Insect symbiosis, vol 3. CRC Press, Boca Raton
Ji R, Brune A (2001) Transformation and mineralization of 14C-labeled cellulose, peptidoglycan, and protein by the soil-feeding termite. Biol Fertil Soils 33:166–174
Ji R, Kappler A, Brune A (2000) Transformation and mineralization of synthetic 14C-labeled humic model compounds by soil-feeding termites. Soil Biol Biochem 32:1281–1291
Jurkevitch E (2011) Riding the Trojan horse: combating pest insects with their own symbionts. Microb Biotech. doi:10.1111/j.1751-7915.2011.00249
Kikuchi Y, Hosokawa T, Fukatsu T (2007) Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl Environ Microbiol 73:4308–4316
Kikuchi Y, Hosokawa T, Fukatsu T (2011) An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J 5:446–460
Kounatidis I, Crotti E, Sapountzis P, Sacchi L, Rizzi A, Chouaia B, Bandi C, Alma A, Daffonchio D, Mavragani-Tsipidou P, Bourtzis K (2009) Acetobacter tropicalis is a major symbiont of the olive fruit fly (Bactrocera oleae). Appl Environ Microbiol 75:3281–3288
Kuechler SM, Dettner K, Kehl S (2011) Characterization of an obligate intracellular bacterium in midgut epithelium of bulrush bug Chilacis typhae (Heteroptera, Lygaeidae, Artheneinae). Appl Environ Microbiol. doi:10.1128/AEM.02983-10
Lauzon CR, Sjogren RE, Prokopy RJ (2000) Enzymatic capabilities of bacteria associated with apple maggot flies: a postulated role in attraction. J Chem Ecol 26:953–967
Lauzon CR, McCombs SD, Potter SE, Peabody NC (2009) Establishment and vertical passage of Enterobacter (Pantoea) agglomerans and Klebsiella pneumoniae through all life stages of the Mediterranean fruit fly (Diptera: Tephritidae). Ann Entomol Soc Am 102:85–95
Lhocine N, Ribeiro PS, Buchon N, Wepf A, Wilson R, Tenev T, Lemaitre B, Gstaiger M, Meier P, Leulier F (2008) PIMS modulates immune tolerance by negatively regulating Drosophila innate immune signaling. Cell Host Microbe 4:147–158
Liu N, Yan X, Zhang M, Xie L, Wang Q, Huang Y, Zhou X, Wang S, Zhou Z (2011) Microbiome of fungus-growing termites: a new reservoir for lignocellulase genes. Appl Environ Microbiol 77:48–56
Maestro Duran R (1990) Relationship between the composition and ripening of the olive and the quality of the oil. Acta Hortic 290:441–451
Mazzon L, Piscedda A, Simonato M, Martinez-Sanudo I, Squartini A, Girolami V (2008) Presence of specific symbiotic bacteria in flies of the subfamily Tephritinae (Diptera Tephritidae) and their phylogenetic relationships: proposal of ‘Candidatus Stammerula tephritidis’. Int J Syst Evol Microbiol 58:1277–1287
Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190
Moya A, Pereto J, Gil R, Latorre A (2008) Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat Rev Genet 9:218–229
Nishiwaki H, Ito K, Shimomura M, Nakashima K, Matsuda K (2007) Insecticidal bacteria isolated from predatory larvae of the antlion species Myrmeleon bore (Neuroptera: Myrmeleontidae). J Invertebr Pathol 96:80–88
Ohkuma M, Noda S, Kudo T (1999) Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites. Appl Environ Microbiol 65:4926–4934
Ohkuma M (2003) Termite symbiotic systems: efficient bio-recycling of lignocellulose. Appl Microbiol Biotechnol 61:1–9
Ohkuma M (2008) Symbioses of flagellates and prokaryotes in the gut of lower termites. Trends Microbiol 16:345–352
Ohkuma M, Brune A (2006) Role of the termite microbiota in symbiotic digestion. In: Bignell DE, Voisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 439–476
Pais R, Lohs C, Wu Y, Wang J, Aksoy S (2008) The obligate mutualist Wigglesworthia glossinidia influences reproduction, digestion, and immunity processes of its host, the Tsetse fly. Appl Environ Microbiol 74:5965–5974
Pimentel D (2009) Pesticides and pest control. In: Peshin R, Dhawan AK (eds) Integrated pest management: innovation-development process, vol 1. Springer, Dordrecht
Ryan D, Robards K, Lavee S (1999) Accumulation of oleuropein derivatives during olive maturation. Int J Food Sci Technol 34:265–274
Ryu J-H, Kim S-H, Lee H-Y, Bai JY, Nam Y-D, Bae J-W, Lee DG, Shin SC, Ha E-M, Lee W-J (2008) Innate immune homeostasis by the homeobox gene Caudal and commensal-gut mutualism in Drosophila. Science 319:777–782
Sands WA (1969) The association of termites and fungi. In: Krishna K, Weesner FM (eds) Biology of termites. Academic, New York, pp 495–524
Sandström J, Pettersson J (1994) Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance. J Insect Physiol 40:947–955
Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E (2010) Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proceedings of the National Academy of Sciences. /cgi/doi/10.1073/pnas.1009906107
Stammer HJ (1929) Die bakteriensymbiose der trypetiden (Diptera). Zoomorphology 15:481–523
Tayasu I, Abe T, Eggleton P, Bignell DE (1997) Nitrogen and carbon isotope ratios in termites: an indicator of trophic habit along the gradient from wood-feeding to soil-feeding. Ecol Entomol 22:343–351
Toh H, Weiss BL, Perkin SAH, Yamashita A, Oshima K, Hattori M, Aksoy S (2006) Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res 16:149–156
Toju H, Hosokawa T, Koga R, Nikoh N, Meng XY, Kimura N, Fukatsu T (2010) “Candidatus Curculioniphilus buchneri,” a novel clade of bacterial endocellular symbionts from weevils of the genus Curculio. Appl Environ Microbiol 76:275–282
Tokuda G, Lo N, Watanabe H (2005) Marked variations in patterns of cellulase activity against crystalline- vs carboxymethyl-cellulose in the digestive systems of diverse, wood-feeding termites. Physiol Entomol 30:372–80
Vreysen MJ, Saleh KM, Ali MY, Abdulla AM, Zhu ZR, Juma KG, Dyck VA, Msangi AR, Mkonyi AR, Feldmann HU (2000) Glossina austeni (Diptera: Glossinidae) eradicated on the Island of Unguja, Zanzibar, using the sterile insect technique. J Econ Entomol 93:123–135
Warnecke F, Luginbuhl P, Ivanova N, Ghassemian M, Richardson T et al (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–565
Weeks AR, Turelli M, Harcombe WR, Reynolds KT, Hoffmann AA (2007) From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol 5:e114
White IM, Elson-Harris MM (1992) Fruit flies of economic significance: their identification and bionomics. CAB International, Wallingford
Wood TG, Thomas RJ (1989) The mutualistic association between Macrotermitinae and Termitomyces. In: Wilding N, Collins NM, Hammond PM, Webber JF (eds) Insect-fungus interaction. Academic, London, pp 69–92
Wu D, Daugherty SC, Van Aken SE, Pai GH, Watkins KL, Khouri H, Tallon LJ, Zaborsky JM, Dunbar HE, Tran PL, Moran NA, Eisen JA (2006) Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol 4:e188
Yeates DK, Wiegmann BM (2005) Phylogeny and evolution of Diptera: recent insight and new perspective. In: Yeates DK, Wiegmann BM (eds) The evolutionary biology of flies. Colombia University Press, New York, pp 14–44
Yoshida N, Oeda K, Watanabe E, Mikami T, Fukita Y, Nishimura K, Komai K, Matsuda K (2001) Protein function: chaperonin turned insect toxin. Nature 411:44–44
Zamora R, Alaiz M, Hidalgo FJ (2001) Influence of cultivar and fruit ripening on olive (Olea europaea) fruit protein content, composition, and antioxidant activity. J Agric Food Chem 49:4267–4270
Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735
Zinder DE, Dworkin M (2000) Morphological and physiological diversity. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 185–220
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Jurkevitch, E. (2012). Insect “Symbiology” Is Coming of Age, Bridging Between Bench and Field. In: Rosenberg, E., Gophna, U. (eds) Beneficial Microorganisms in Multicellular Life Forms. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-21680-0_2
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