Abstract
The microorganisms forming symbioses with insects play an important role in nutrition, development and evolution of their hosts. They make it possible for their hosts to use poorly digestible nutrients, to resist the biotic and abiotic stresses, and to regulate the metamorphosis. The microsymbionts of insects may be facultative (genetically specialized for symbiosis but retaining the capacity for autonomous existence; they are usually located extracellularly, in the gut, hemolymph, or salivary glands of the host) or obligatory (incapable of autonomous existence due to the loss of large parts of their genomes; they are usually located inside specialized host cells). The intracellular symbionts (endocytobionts) are capable of vertical transmission during the host reproduction, which determines the loss of many housekeeping genes, including the genes for replication, transcription and translation. In some obligatory symbionts, amplification of genes performing the functions useful for the hosts, such as the synthesis of essential amino acids, was found. These symbionts exhibit increased rates of accumulation of mutations, including non-synonymous nucleotide substitutions, reflecting suppression of the purifying selection and activation of genetic drift stimulating the genome reduction. Transfer of some genes from endocytobionts to the nuclear chromosomes of insects enables them to implement the novel metabolic functions, including assimilation of rare nutrients. The obligatory intracellular insect symbionts may be used as models to reconstruct the early stages of evolution of cellular organelles, which involve reduction of essential genes and the loss of genetic individuality of the symbionts, i.e., the ability for self-maintenance and expression of their residual genomes. Genetic analysis of insect microsymbionts extends the opportunities for their practical application associated with biological control of harmful insects (herbivorous, bloodsucking) and stimulation of the beneficial ones (honey collectors, pollinators, antagonists of pests).
Similar content being viewed by others
References
Acuña, R., Padilla, B.E., Flórez-Ramos, C.P., Rubio, J.D., Herrera, J.C., Benavides, P., Lee, S.-J., Yeats, T.H., Egan, A.N., Doyle, J.J., and Rose, J.K.C., Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee, Proc. Natl. Acad. Sci. U. S. A., 2012, vol. 109, pp. 4197–4202.
Afrikyan, E.K., Kinosyan, M.A., Okasov, A.K., and Kazanchyan, N.L., Specifics of the insect enthomopathogenic microbiota, Dokl. NAS of Armenia, 2014, vol. 114, no. 2, pp. 156–163.
Andongma, A.A., Wan, L., Dong, Y.C., Li, P., Desneux, N., White, J.A., and Niu, C.-Y., Pyrosequencing reveals a shift in symbiotic bacteria populations across life stages of Bactrocera dorsalis, Sci. Rep., 2015, vol. 5, no. 9470. doi 10.1038/srep09470
Baba, T., Ara, T., Okumura, Y., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K.A., Tomita, M., Wanner, B.L., and Mori, H., Construction of Escherichia coli K-12 in-frame, single-gene knock-out mutants—the Keio collection, Mol. Syst. Biol., 2006, vol. 2, no. 1. doi 10.1038/msb4100050
Bodył, A., Mackiewicz, P., and Gagat, P., Organelle evolution: Paulinella breaks a paradigm, Curr. Biol., 2012, vol. 22, pp. 304–305.
Brewin, N.J., Plant cell wall remodeling in the Rhizobiumlegume symbiosis, Crit. Rev. Plant Sci., 2004, vol. 23, pp. 1–24.
Broderick, N.A. and Lemaitre, B., Gut-associated microbes of Drosophila melanogaster, Gut Microbes., 2012, vol. 3, pp. 307–321.
Broderick, N.A., Raffa, K.F., and Handelsman, J., Midgut bacteria required for Bacillus thuringiensis insecticidal activity, Proc. Natl. Acad. Sci. U. S. A., 2006, vol. 103, pp. 15196–15199.
Caldera, E.J., Poulsen, M., Suen, G., and Currie, C.R., Insect symbioses: a case study of past, present, and future of fungus-growing ant research, Environ. Entomol., 2009, vol. 38, pp. 78–92.
Capuzzo, C., Firrao, G., Mazzon, L., Squartini, A., and Girolami, V., ‘Candidatus Erwinia dacicola’, a coevolved symbiotic bacterium of the olive fly Bactrocera oleae (Gmelin), Int. J. Syst. Evol. Microbiol., 2005, vol. 55, pp. 1641–1647.
Charles, H., Balmand, S., Lamelas, A., Cottret, L., Pérez-Brocal, V., Burdin, B., Latorre, A., Febvay, G., Colella, S., Calevro, F., and Rahbé, Y., A genomic reappraisal of symbiotic function in the aphid/Buchnera symbiosis: reduced transporter sets and variable membrane organizations, PLoS One, 2011, vol. 6. e29096. doi 10.1371/journal.pone.0029096
Clark, B.W., Phillips, T.A., and Coats, J.R., Environmental fate and effects of Bacillus thuringiensis (Bt) proteins from transgenic crops: a review, J. Agric. Food Chem., 2005, vol. 53, pp. 4643–4653.
Cordaux, R., Bouchon, D., and Grève, P., The impact of endosymbionts on the evolution of host sex-determination mechanisms, Trends Genet., 2011, vol. 27, pp. 332–341.
Douglas, A.E., Lessons from studying insect symbioses, Cell Host and Microbe, 2011, vol. 10, pp. 359–366.
Douglas, A.E., The molecular basis of bacterial–insect symbiosis, J. Mol. Biol., 2014, vol. 426, pp. 3830–3837.
Dowd, P.F., Insect fungal symbionts: a promising source of detoxifying enzymes, J. Industr. Microbiol., 1992, vol. 9, pp. 149–161.
Felsenstein, J., The evolutionary advantage of recombination, Genetics, 1974, vol. 78, pp. 737–756.
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., et al., The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode, PLoS Biol., 2005, vol. 3, no. 4. e121.
Gil, R., Sabater-Munoz, B., Latorre, A., Silva, F.J., and Moya, A., Extreme genome reduction in Buchnera spp.: toward the minimal genome needed for symbiotic life, Proc. Natl. Acad. Sci. U. S. A., 2002, vol. 99, pp. 4454–4458.
Gonzalez, J.M., Brown, B.J., and Carlton, B.C., Transfer of Bacillus thuringiensis plasmids coding for delta endotoxin among strains of B. thuringiensis and B. cereus, Proc. Natl. Acad. Sci. U. S. A., 1982, vol. 79, pp. 6951–6955.
Gosalbes, M.J., Lamelas, A., Moya, A., and Latorre, A., The striking case of tryptophan provision in the cedar aphid Cinara cedri, J. Bacteriol., 2008, vol. 190, pp. 6026–6029.
Gross, J. and Bhattacharya, D., Mitochondrial and plastid evolution in eukaryotes: an outsiders’ perspective, Nat. Rev. Genet., 2009, vol. 10, pp. 495–505.
Gunduz E.A., Douglas A.E. Symbiotic bacteria enable insect to use a nutritionally inadequate diet, Proc. R. Soc. B. 2009, vol. 276, pp. 987–991.
Gupta, A.K., Nayduch, D., Verma, P., Shah, B., Ghate, H.V., Patole, M.S., and Shouche, Y.S., Phylogenetic characterization of bacteria in the gut of house flies (Musca domestica L.), FEMS Microbiol. Ecol., 2012, vol. 79, pp. 581–593.
Hackstein, J.H.P., van Hoek, A.H.A.M., Leunissen, J.A.M., and Huynen, M., Anaerobic ciliates and their methanogenic endosymbionts, in Symbiosis: Mechanisms and Model Systems, Seckbach, J., Ed., Dordrecht: Kluwer Acad. Publ., 2002, pp. 257–270.
Hotopp, D.J.C., Clark, M.E., Oliveira, D.C., Foster, J.M., Fischer, P., Muñoz Torres, M.C., Giebel, J.D., Kumar, N., Ishmael, N., Wang, S., Ingram, J., Nene, R.V., Shepard, J., Tomkins, J., Richards, S., et al., Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes, Science, 2007, vol. 317, pp. 1753–1756.
Husnik, F., Nikoh, N., Koga, R., Ross, L., Duncan, R.P., Fujie, M., Tanaka, M., Satoh, N., Bachtrog, D., Wilson, A.C., von Dohlen, C.D., Fukatsu, T., and McCutcheon, J.P., Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis, Cell, 2013, vol. 153, pp. 1567–1578.
Janson, E.M., Stireman, J.O., Singer, M.S., and Abbot, P., Phytophagous insect-microbe mutualisms and adaptive evolutionary diversification, Evolution, 2008, vol. 62, pp. 997–1012.
Kandybin, N.V., Patyka, T.I., Ermolova, V.P., and Patyka, V.F., Mikrobiokontrol’ chislennosti nasekomykh i ego dominanta Bacillus thuringiensis (Microbiocontrol of Insect Abundance and Its Dominant, Bacillus thuringiensis), S.-Pb., Pushkin: Inform. Center Plant Protection, 2009.
Keeling, P.J., Jeffrey, D. and Palmer, J.D., Horizontal gene transfer in eukaryotic evolution, Nature Rev. Genet., 2008, vol. 9, pp. 605–618.
Kikuchi, Y., Hosokawa, T., and Fukatsu, T., Insectmicrobe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation, Appl. Environ. Microbiol., 2007, vol. 73, pp. 4308–4316.
Kim, J.K., Son, W.D., Kim, C.-H., Cho, J.H., Marchetti, R., Silipo, A., Sturiale, L., Park, H.Y., Huh, Y.R., Nakayama, H., Fukatsu, T., Molinaro, A., and Lee, B.L., Insect gut symbiont’s susceptibility to host antimicrobial peptides caused by alteration of bacterial cell envelope, J. Biol. Chem., 2015, vol. 290, pp. 21042–21053.
Koga, R., Tsuchida, T., and Fukatsu, T., Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid, Proc. Roy. Soc. Lond. B, 2003, vol. 270, pp. 2543–2550.
Latorre, A., Gill, R., Silva, F.J., and Moya, A., Chromosomal stasis versus plasmid plasticity in aphid endosymbiont Buchnera aphidicola, Heredity, 2005, vol. 95, pp. 339–347.
Lilburn, T.G., Kim, K.S., Ostrom, N.E., Byzek, K.R., Leadbetter, J.R., and Breznak, J.A., Nitrogen fixation by symbiotic and free-living spirochetes, Science, 2001, vol. 292, pp. 2495–2498.
Lithgow, T. and Schneider, A., Evolution of macromolecular import pathways in mitochondria, hy-drogenosomes and mitosomes, Phil. Trans. R. Soc. B, 2010, vol. 365, pp. 799–817.
Liu, L., Huang, X., Zhang, R., Jiang, L., and Qiao, G., Phylogenetic congruence between Mollitrichosiphum (Aphididae: Greenideinae) and Buchnera indicates insect-bacteria parallel evolution, Syst. Entomol., 2013, vol. 38, pp. 81–92.
Luan, J.-B., Chen, W., Hasegawa, D.K., Simmons, A.M., Wintermantel, W.M., Ling, K.-S., Fei, Z., Liu, S.-S., and Douglas, A.E., Metabolic coevolution in the bacterial symbiosis of whiteflies and related plant sap-feeding insects, Genome Biol. Evol., 2015, vol. 7, pp. 2635–2647.
Manzano-Marín, A. and Latorre, A., The genome of Serratia symbiotica from the aphid Cinara tujafilina zooms in on the process of accommodation to a cooperative intracellular life, Genome Biol. Evol., 2014, vol. 6, pp. 1683–1698.
Mehdiabadi, N.J. and Schultz, T.R., Natural history and phylogeny of the fungus-farming ants (Hymenoptera: Formicidae: Myrmicinae: Attini), Myrmecol. News, 2009, vol. 13, pp. 37–55.
Minard, G., Mavingui, P., and Moro, C.V., Diversity and function of bacterial microbiota in the mosquito holobiont, Parasites and Vectors, 2013, vol. 6, no. 146. doi 10.1186/1756-3305-6-146
Moran, N.A., Accelerated evolution and Muller’s ratchet endosymbiotic bacteria, Proc. Natl. Acad. Sci. U. S. A., 1996, vol. 93, pp. 2873–2878.
Moran, N.A., Degnan, P.H., Santos, S.R., Dunbar, H.E., and Ochman, H., The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes, Proc. Natl. Acad. Sci. U. S. A., 2005, vol. 102, pp. 16919–16926.
Moran, N.A., McCutcheon, J.P., and Nakabachi, A., Genomics and evolution of heritable bacterial symbionts, Annu. Rev. Genet., 2008, vol. 42, pp. 165–190.
Mueller, U.G., Gerardo, N.M., Aanen, D.K., Six, D.L., and Schultz, T.R., The evolution of agriculture in insects, Annu. Rev. Ecol. Evol. System., 2005, vol. 36, pp. 563–595.
Nakabachi, A., Yamashita, A., Toh, H., Ishikawa, H., Dunbar, H.E., Moran, N.A., and Hattori, M., The 160-kilobase genome of the bacterial endosymbiont Carsonella, Science, 2006, vol. 314, pp. 267–270.
Nikoh, N., Hosokawa, T., and Moriyama, M., Evolutionary origin of insect-Wolbachia nutritional mutualism, Proc. Natl. Acad. Sci. U. S. A., 2014, vol. 111, pp. 10257–10262.
Nikoh, N., Hosokawa, T., Oshima, K., Hattori, M., and Fukatsu, T., Reductive evolution of bacterial genome in insect gut environment, Genome Biol. Evol., 2011, vol. 3, pp. 702–714. doi 10.1093/gbe/evr064
Nikoh, N., McCutcheon, J.P., Kudo, T., Miyagishima, S., and Moran, N.A., Bacterial genes in the aphid genome: absence of functional gene transfer from Buchnera to its host, PLoS Genet., 2010, vol. 6, no. 2. e1000827. doi 10.1371/journal.pgen.1000827
Nikoh, N., Tanaka, K., Shibata, F., Kondo, N., Hizume,M., Shimada, M., and Fukatsu, T., Wolbachia genome integrated in an insect chromosome: evolution and fate of laterally transferred endosymbiont genes, Genome Res., 2008, vol. 18, pp. 272–280.
Ohkuma, M., Maeda, Y., Johjima, T., and Kudo, T., Lignin degradation and roles of white rot fungi: study on an efficient symbiotic system in fungus-growing termites and its application to bioremediation, RIKEN Rev., 2001, no. 42, pp. 39–42.
Poulsen, M., Cafaro, M.J., Erhardt, D.P., Little, A.E.F., Gerardo, N.M., Tebbets, B., Klein, B.S., and Currie, C.R., Variation in Pseudonocardia antibiotic defense helps govern parasite-induced morbidity in Acromyrmex leaf-cutting ants, Environ. Microbiol. Rep., 2010, vol. 2, pp. 534–540.
Prado, S.S. and Almeida, R.P.P., Role of symbiotic gut bacteria in the development of Acrosternum hilare and Murgantia histrionica, Entomol. Exper. Applic., 2009, vol. 132, pp. 21–29.
Provorov, N.A. and Vorobyev, N.I., Evolution of host-beneficial traits in nitrogen-fixing bacteria: modeling and construction of systems for interspecies altruism, Appl. Biochem. Microbiol., 2015, vol. 51, no. 4, pp. 381–387.
Ricci, I., Valzano, M., Ulissi, U., Epis, S., Cappelli, A., and Favia, G., Symbiotic control of mosquito borne disease, Pathogens Global Health, 2012, vol. 106, pp. 380–385.
Richards, A.M., Von Dwingelo, J.E., Price, C.T., and Kwaik, Y.A., Cellular microbiology and molecular ecology of Legionella–amoeba interaction, Virulence, 2013, vol. 4, pp. 307–314.
Rio, R.V.M., Symula, R.E., Wang, J., Lohs, C., Wu, Y., Snyder, A.K., Bjornson, R.D., Oshima, K., Biehl, B.S., Perna, N.T., Hattori, M., and Akso, S., Insight into the transmission biology and species-specific functional capabilities of tsetse (Diptera: Glossinidae) obligate symbiont Wigglesworthia, MBio, 2012, vol. 3, no. 1. e00240–11. doi 10.1128/mBio.00240-11
Sanchez-Contreras, M. and Vlasido, I., The diversity of insect-bacteria interactions and its applications for disease control, Biotechnol. Gen. Engin. Rev., 2008, vol. 25, pp. 203–244.
Sorokan’, A.V., Rumyantsev, S.D., Ben’kovskaya, G.V., and Maksimov, I.V., Ecological role of microsymbionts in the interactions of plants and phytophagous insects, Usp. Sovr. Biol., 2017, vol. 134, no. 5, pp. 135–150.
Steinhaus, E.A., Insect Microbiology, Ithaca: Comstock, 1947.
Suh, S.-O., Noda, H., and Blackwell, M., Insect symbiosis: derivation of yeast-like endosymbionts within en entomopathogenic filamentous lineage, Mol. Biol. Evol., 2001, vol. 18, pp. 995–1000.
Tikhonovich, I.A. and Provorov, N.A., Development of symbiogenetic approaches for studying variation and heredity of superspecies systems, Russ. J. Genet., 2012, vol. 48, pp. 357–368.
van der Vlugt-Bergmans, C.J.B. and van der Werf, M.J., Genetic and biochemical characterization of a novel monoterpene ε-lactone hydrolase from Rhodococcus erythropolis DCL14, Appl. Environ. Microbiol., 2001, vol. 67, pp. 733–741.
van Ham, R.C., Kamerbeek, J., Palacios, C., Rausell, C., Abascal, F., Bastolla, U., Fernandez, J.M., Jimenez, L., Postigo, M., Silva, F.J., Tamames, J., Viguera, E., Latorre, A., Valencia, A., Moran, F., and Moya, A., Reductive genome evolution in Buchnera aphidicola, Proc. Natl. Acad. Sci. U. S. A., 2003, vol. 100, pp. 581–586.
van Ham, R.C., Martinez-Torres, D., Moya, A., and Latorre, A., Plasmid-encoded anthranilate synthase (TrpEG) in Buchnera aphidicola from aphids of the family Pemphigidae, Appl. Environ. Microbiol., 1999, vol. 65, pp. 117–125.
van Hoek, A.H.A.M., Akhmanova, A.S., Huynen, M.A., and Hackstein, J.H.P., A mitochondrial ancestry of the hydrogenosomes of Nyctotherus ovalis, Mol. Biol. Evol., 2000, vol. 17, pp. 202–206.
van Hoek, A.H.A.M., van Alen, T.A., Sprakel, V.S.A., Leunissen, J.A.M., Brigge, T., Vogels, G.D., and Hackstein, J.H.P., Multiple acquisition of methanogenic archaeal symbionts by anaerobic ciliates, Mol. Biol. Evol., 2000, vol. 17, pp. 251–258.
Vasquez, A., Forsgren, E., Fries, I., Paxton, R.J., Flaberg, E., Szekely, L., and Olofsson, T.C., Symbionts as major modulators of insect health: lactic acid bacteria and honeybees, PLoS One, 2012, vol. 7, no. 3. e33188. doi 10.1371/journal.pone.0033188
Viñuelas, J., Febvay, G., Duport, G., Colella, S., Fayard, J.-M., Charles, H., Rahbé, Y., and Calevro, F., Multimodal dynamic response of the Buchnera aphidicola pLeu plasmid to variations in leucine demand of its host, the pea aphid Acyrthosiphon pisum, Mol. Microbiol., 2011, vol. 81, pp. 1271–1285.
Wernegreen, J.J. and Moran, N.A., Evidence for genetic drift in endosymbionts (Buchnera): analyses of proteincoding genes, Mol. Biol. Evol., 1999, vol. 16, pp. 83–97.
Woolfit, M., Iturbe-Ormaetxe, I., McGraw, E.A., and O’Neill, S.L., An ancient horizontal gene transfer between mosquito and the endosymbiotic bacterium Wolbachia pipientis, Mol. Biol. Evol., 2009, vol. 26, pp. 367–374.
Zakharov, I.A., Intracellular symbionts as a factor in insect evolution, Usp. Sovr. Biol., 2014, vol. 134, no. 5, pp. 435–446.
Zilber-Rosenberg, I. and Rosenberg, E., Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution, FEMS Microbiol. Rev., 2008, vol. 32, pp. 723–735.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © N.A. Provorov, O.P. Onishchuk, 2018, published in Mikrobiologiya, 2018, Vol. 87, No. 2, pp. 99–113.
Rights and permissions
About this article
Cite this article
Provorov, N.A., Onishchuk, O.P. Microbial Symbionts of Insects: Genetic Organization, Adaptive Role, and Evolution. Microbiology 87, 151–163 (2018). https://doi.org/10.1134/S002626171802011X
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S002626171802011X