Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

How multi-partner endosymbioses function

Nature Reviews Microbiology volume 14, pages 731–743 (2016)Cite this article

Subjects

Key Points

  • Multi-partner endosymbioses have evolved independently in several lineages of the plant sap-feeding insects of the order Hemiptera. Many of these endosymbionts have much-reduced genomes as a result of relaxed selection and genomic decay.

  • In multi-partner endosymbioses, the production of essential amino acids is often partitioned between the different endosymbionts, such that each endosymbiont mediates the biosynthesis of a subset of essential amino acids or a subset of the reactions in the biosynthetic pathway of a single essential amino acid.

  • The essential amino acid biosynthetic pathways that are partitioned between primary endosymbionts and more recently acquired endosymbionts are energetically costly, which suggests that the capacity for energy production may be limiting in primary endosymbionts, possibly as a result of genomic decay.

  • Rather than partition nutrient biosynthesis, the benefit to the host of some multi-partner endosymbioses relates to the acquisition of additional functions. In these examples, one endosymbiont specializes in providing a nutritional benefit, whereas the other endosymbiont provides a non-nutritional benefit, such as protection from natural enemies.

  • The phylogenetic distribution of the various endosymbiont taxa that colonize Hemiptera indicates that multi-partner endosymbioses have generally evolved through the sequential acquisition of different microorganisms, together with the occasional replacement of one or more endosymbionts by different taxa.

  • The absence of endosymbionts in, for example, some insect pollinators and vertebrates, including humans, may provide an opportunity to identify symbiosis-related molecular functions that can be targeted as novel pest control strategies.

Abstract

Various animals are associated with specific endosymbiotic microorganisms that provide the host with essential nutrients or confer protection against natural enemies. Genomic analyses of the many endosymbioses that are found in plant sap-feeding hemipteran insects have revealed independent acquisitions — and occasional replacements — of endosymbionts, such that many of these endosymbioses involve two or more microbial partners. In this Review, I discuss how partitioning of the genetic capacity for metabolic function between different endosymbionts has sustained nutritional function in multi-partner endosymbioses, and how the phenotypic traits of these endosymbionts can be shaped by co-evolutionary interactions with both co-occurring microbial taxa and the host, which often operate over long evolutionary timescales.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Interactions among the partners in multi-partner endosymbioses.
Figure 2: The microbial taxa in hemipteran endosymbioses
Figure 3: Essential amino acid biosynthesis pathways shared between endosymbionts.
Figure 4: Evolutionary dynamics of multi-partner endosymbioses.

Similar content being viewed by others

References

  1. McFall-Ngai, M. et al. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl Acad. Sci. USA 110, 3229–3236 (2013).

    CAS  PubMed  Google Scholar 

  2. The Human Microbiome Consortium. Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214 (2012).

  3. Sender, R., Fuchs, S. & Milo, R. Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell 164, 337–340 (2016).

    CAS  PubMed  Google Scholar 

  4. Lloyd-Price, J., Abu-Ali, G. & Huttenhower, C. The healthy human microbiome. Genome Med. 8, 51 (2016).

    PubMed  PubMed Central  Google Scholar 

  5. Douglas, A. E. The Symbiotic Habit (Princeton Univ. Press, 2010).

    Google Scholar 

  6. Douglas, A. E. Multiorganismal insects: diversity and function of resident microorganisms. Annu. Rev. Entomol. 60, 17–34 (2015).

    CAS  PubMed  Google Scholar 

  7. Kerney, R. et al. Intracellular invasion of green algae in a salamander host. Proc. Natl Acad. Sci. USA 108, 6497–6502 (2011).

    CAS  PubMed  Google Scholar 

  8. Moulder, J. W. The cell as an extreme environment. Proc. R. Soc. Lond. B Biol. Sci. 204, 199–210 (1979).

    CAS  PubMed  Google Scholar 

  9. Peterson, L. W. & Artis, D. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat. Rev. Immunol. 14, 141–153 (2014).

    CAS  PubMed  Google Scholar 

  10. Ray, K., Marteyn, B., Sansonetti, P. J. & Tang, C. M. Life on the inside: the intracellular lifestyle of cytosolic bacteria. Nat. Rev. Microbiol. 7, 333–340 (2009).

    CAS  PubMed  Google Scholar 

  11. McCutcheon, J. P. & Moran, N. A. Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10, 13–26 (2012).

    CAS  Google Scholar 

  12. Buchner, P. Endosymbioses of Animals with Plant Microorganisms (John Wiley and Sons, 1965).

    Google Scholar 

  13. Nakabachi, A. et al. Defensive bacteriome symbiont with a drastically reduced genome. Curr. Biol. 23, 1478–1484 (2013). This study demonstrates that a bacterium that can synthesize a polyketide with predicted defensive function has evolved into an endosymbiont that has a very small genome and is absolutely dependent on its insect host, complementing the nutritional function of the primary symbiont.

    CAS  PubMed  Google Scholar 

  14. Bennett, G. M. & Moran, N. A. Small, smaller, smallest: the origins and evolution of ancient dual symbioses in a phloem-feeding insect. Genome Biol. Evol. 5, 1675–1688 (2013).

    PubMed  PubMed Central  Google Scholar 

  15. Toenshoff, E. R., Gruber, D. & Horn, M. Co-evolution and symbiont replacement shaped the symbiosis between adelgids (Hemiptera: Adelgidae) and their bacterial symbionts. Environ. Microbiol. 14, 1284–1295 (2012).

    CAS  PubMed  Google Scholar 

  16. Toenshoff, E. R., Szabo, G., Gruber, D. & Horn, M. The pine bark adelgid, Pineus strobi, contains two novel bacteriocyte-associated gammaproteobacterial symbionts. Appl. Environ. Microbiol. 80, 878–885 (2014).

    PubMed  PubMed Central  Google Scholar 

  17. Gottlieb, Y. et al. Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Appl. Environ. Microbiol. 72, 3646–3652 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. McCutcheon, J. P. & von Dohlen, C. D. An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr. Biol. 21, 1366–1372 (2011). The article provides the first description of a nested endosymbiosis, in which the genomes of the two endosymbionts encode different genes of certain EAA biosynthetic pathways.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Koga, R., Nikoh, N., Matsuura, Y., Meng, X. Y. & Fukatsu, T. Mealybugs with distinct endosymbiotic systems living on the same host plant. FEMS Microbiol. Ecol. 83, 93–100 (2013).

    CAS  PubMed  Google Scholar 

  20. Husnik, F. & McCutcheon, J. P. Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis. Proc. Natl Acad. Sci. USA 113, E5416–E5424 (2016).

    CAS  PubMed  Google Scholar 

  21. Watanabe, K., Yukuhiro, F., Matsuura, Y., Fukatsu, T. & Noda, H. Intrasperm vertical symbiont transmission. Proc. Natl Acad. Sci. USA 111, 7433–7437 (2014).

    CAS  PubMed  Google Scholar 

  22. De Vooght, L., Caljon, G., Van Hees, J. & Van Den Abbeele, J. Paternal transmission of a secondary symbiont during mating in the viviparous tsetse fly. Mol. Biol. Evol. 32, 1977–1980 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Oliver, T. A., Smith, A. H. & Russell, J. A. Defensive symbiosis in the real world — advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct. Ecol. 28, 341–355 (2014).

    Google Scholar 

  24. Moran, N. A., Russell, J. A., Koga, R. & Fukatsu, T. Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Appl. Environ. Microbiol. 71, 3302–3310 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Skaljac, M., Zanic, K., Ban, S. G., Kontsedalov, S. & Ghanim, M. Co-infection and localization of secondary symbionts in two whitefly species. BMC Microbiol. 10, 142 (2010).

    PubMed  PubMed Central  Google Scholar 

  26. Caspi-Fluger, A. et al. Rickettsia 'in' and 'out': two different localization patterns of a bacterial symbiont in the same insect species. PLoS ONE 6, e21096 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Koga, R., Tsuchida, T. & Fukatsu, T. Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc. Biol. Sci. 270, 2543–2550 (2003).

    PubMed  PubMed Central  Google Scholar 

  28. Darby, A. C., Chandler, S. M., Welburn, S. C. & Douglas, A. E. Aphid-symbiotic bacteria cultured in insect cell lines. Appl. Environ. Microbiol. 71, 4833–4839 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Oliver, K. M., Moran, N. A. & Hunter, M. S. Costs and benefits of a superinfection of facultative symbionts in aphids. Proc. Biol. Sci. 273, 1273–1280 (2006).

    PubMed  PubMed Central  Google Scholar 

  30. Chandler, S. M., Wilkinson, T. L. & Douglas, A. E. Impact of plant nutrients on the relationship between a herbivorous insect and its symbiotic bacteria. Proc. Biol. Sci. 275, 565–570 (2008).

    CAS  PubMed  Google Scholar 

  31. Oliver, K. M., Degnan, P. H., Burke, G. R. & Moran, N. A. Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu. Rev. Entomol. 55, 247–266 (2010).

    CAS  PubMed  Google Scholar 

  32. Caspi-Fluger, A. et al. Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proc. Biol. Sci. 279, 1791–1796 (2012). A very thorough study of horizontal transmission of a secondary symbiont that provides empirical evidence for one route contributing to the lack of congruence between the phylogenies of aphids and their secondary symbionts.

    CAS  PubMed  Google Scholar 

  33. Oliver, K. M., Campos, J., Moran, N. A. & Hunter, M. S. Population dynamics of defensive symbionts in aphids. Proc. Biol. Sci. 275, 293–299 (2008).

    PubMed  Google Scholar 

  34. Douglas, A. E., François, C. L. M. J. & Minto, L. B. Facultative 'secondary' bacterial symbionts and the nutrition of the pea aphid, Acyrthosiphon pisum. Physiol. Entomol. 31, 262–269 (2006).

    CAS  Google Scholar 

  35. Rothacher, L., Ferrer-Suay, M. & Vorburger, C. Bacterial endosymbionts protect aphids in the field and alter parasitoid community composition. Ecology 97, 1712–1723 (2016). An important study that demonstrates the significance of secondary symbionts to protection against natural enemies under field conditions, which complements many laboratory studies.

    PubMed  Google Scholar 

  36. Hansen, A. K. & Moran, N. A. The impact of microbial symbionts on host plant utilization by herbivorous insects. Mol. Ecol. 23, 1473–1496 (2014).

    PubMed  Google Scholar 

  37. Gerardo, N. M. & Parker, B. J. Mechanisms of symbiont-conferred protection against natural enemies: an ecological and evolutionary framework. Curr. Opin. Insect Sci. 4, 8–14 (2014).

    PubMed  Google Scholar 

  38. Oliver, K. M., Degnan, P. H., Hunter, M. S. & Moran, N. A. Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325, 992–994 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Laughton, A. M., Garcia, J. R. & Gerardo, N. M. Condition-dependent alteration of cellular immunity by secondary symbionts in the pea aphid, Acyrthosiphon pisum. J. Insect Physiol. 86, 17–24 (2016).

    CAS  PubMed  Google Scholar 

  40. Caragata, E. P. et al. Dietary cholesterol modulates pathogen blocking by Wolbachia. PLoS Pathog. 9, e1003459 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Hufbauer, R. A. & Via, S. Evolution of an aphid–parasitoid interaction: variation in resistance to parasitism among aphid populations specialized on different plants. Evolution 53, 1435–1445 (1999).

    PubMed  Google Scholar 

  42. Burke, G., Fiehn, O. & Moran, N. Effects of facultative symbionts and heat stress on the metabolome of pea aphids. ISME J. 4, 242–252 (2010).

    PubMed  Google Scholar 

  43. Dunbar, H. E., Wilson, A. C., Ferguson, N. R. & Moran, N. A. Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS Biol. 5, e96 (2007).

    PubMed  PubMed Central  Google Scholar 

  44. Ramsey, J. S. et al. Metabolic interplay between the Asian citrus psyllid and its Profftella symbiont: an Achilles' heel of the citrus greening insect vector. PLoS ONE 10, e0140826 (2015).

    PubMed  PubMed Central  Google Scholar 

  45. Sloan, D. B. & Moran, N. A. Genome reduction and co-evolution between the primary and secondary bacterial symbionts of psyllids. Mol. Biol. Evol. 29, 3781–3792 (2012). This study provides a clear-cut demonstration of how the acquisition of different secondary symbionts in various psyllid lineages has led to the evolution of different patterns of partitioning of EAA biosynthesis reactions, which highlights ongoing evolutionary changes in multi-partner endosymbioses.

    CAS  PubMed  PubMed Central  Google Scholar 

  46. McCutcheon, J. P., McDonald, B. R. & Moran, N. A. Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc. Natl Acad. Sci. USA 106, 15394–15399 (2009).

    CAS  PubMed  Google Scholar 

  47. McCutcheon, J. P. & Moran, N. A. Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution. Genome Biol. Evol. 2, 708–718 (2010).

    PubMed  PubMed Central  Google Scholar 

  48. Lamelas, A., Gosalbes, M. J., Moya, A. & Latorre, A. New clues about the evolutionary history of metabolic losses in bacterial endosymbionts, provided by the genome of Buchnera aphidicola from the aphid Cinara tujafilina. Appl. Environ. Microbiol. 77, 4446–4454 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Van Leuven, J. T., Meister, R. C., Simon, C. & McCutcheon, J. P. Sympatric speciation in a bacterial endosymbiont results in two genomes with the functionality of one. Cell 158, 1270–1280 (2014). The study provides the first report of within-lineage partitioning of function in endosymbiotic bacteria, which was identified in the companion symbiont ' Ca . Hodgkinia cicadicola' in a cicada species.

    CAS  PubMed  Google Scholar 

  50. Campbell, M. A. et al. Genome expansion via lineage splitting and genome reduction in the cicada endosymbiont Hodgkinia. Proc. Natl Acad. Sci. USA 112, 10192–10199 (2015).

    CAS  PubMed  Google Scholar 

  51. Husnik, F. et al. Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153, 1567–1578 (2013).

    CAS  PubMed  Google Scholar 

  52. Matsuura, Y. et al. Huge symbiotic organs in giant scale insects of the genus Drosicha (Coccoidea: Monophlebidae) harbor flavobacterial and enterobacterial endosymbionts. Zoolog. Sci. 26, 448–456 (2009).

    CAS  PubMed  Google Scholar 

  53. Dhami, M. K., Turner, A. P., Deines, P., Beggs, J. R. & Taylor, M. W. Ultrastructural and molecular characterization of a bacterial symbiosis in the ecologically important scale insect family Coelostomidiidae. FEMS Microbiol. Ecol. 81, 537–546 (2012).

    CAS  PubMed  Google Scholar 

  54. Koga, R., Bennett, G. M., Cryan, J. R. & Moran, N. A. Evolutionary replacement of obligate symbionts in an ancient and diverse insect lineage. Environ. Microbiol. 15, 2073–2081 (2013).

    PubMed  Google Scholar 

  55. Sloan, D. B. & Moran, N. A. The evolution of genomic instability in the obligate endosymbionts of whiteflies. Genome Biol. Evol. 5, 783–793 (2013).

    PubMed  PubMed Central  Google Scholar 

  56. Wernegreen, J. J. Mutualism meltdown in insects: bacteria constrain thermal adaptation. Curr. Opin. Microbiol. 15, 255–262 (2012).

    PubMed  PubMed Central  Google Scholar 

  57. Bennett, G. M. & Moran, N. A. Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole. Proc. Natl Acad. Sci. USA 112, 10169–10176 (2015).

    CAS  PubMed  Google Scholar 

  58. Gomez-Valero, L. et al. Coexistence of Wolbachia with Buchnera aphidicola and a secondary symbiont in the aphid Cinara cedri. J. Bacteriol. 186, 6626–6633 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Douglas, A. E. Molecular dissection of nutrient exchange at the insect–microbial interface. Curr. Opin. Insect Sci. 4, 23–28 (2014).

    PubMed  Google Scholar 

  60. Douglas, A. E. Symbiotic microorganisms: untapped resources for insect pest control. Trends Biotechnol. 25, 338–342 (2007).

    CAS  PubMed  Google Scholar 

  61. Mitri, S. & Foster, K. R. The genotypic view of social interactions in microbial communities. Annu. Rev. Genet. 47, 247–273 (2013).

    CAS  PubMed  Google Scholar 

  62. West, S. A., Diggle, S. P., Buckling, A., Gardner, A. & Griffin, A. S. The social lives of microbes. Annu. Rev. Ecol. Evol. Syst. 38, 53–77 (2007).

    Google Scholar 

  63. Rakoff-Nahoum, S., Foster, K. R. & Comstock, L. E. The evolution of cooperation within the gut microbiota. Nature 533, 255–259 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Cryan, J. R. & Urban, J. M. Higher-level phylogeny of the insect order Hemiptera: is Auchenorrhyncha really paraphyletic? Syst. Entomol. 37, 7–21 (2012).

    Google Scholar 

  65. von Dohlen, C. D. & Moran, N. A. Molecular phylogeny of the Homoptera: a paraphyletic taxon. J. Mol. Evol. 41, 211–223 (1995).

    CAS  PubMed  Google Scholar 

  66. Bourgoin, T. & Campbell, B. C. Inferring a phylogeny for Hemiptera: falling into the 'autapomorphic trap'. Denisia 4, 67–82 (2002).

    Google Scholar 

  67. Kikuchi, Y., Meng, X. Y. & Fukatsu, T. Gut symbiotic bacteria of the genus Burkholderia in the broad-headed bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera: Alydidae). Appl. Environ. Microbiol. 71, 4035–4043 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Nikoh, N., Hosokawa, T., Oshima, K., Hattori, M. & Fukatsu, T. Reductive evolution of bacterial genome in insect gut environment. Genome Biol. Evol. 3, 702–714 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Matsuura, Y. et al. Bacterial symbionts of a devastating coffee plant pest, the stinkbug Antestiopsis thunbergii (Hemiptera: Pentatomidae). Appl. Environ. Microbiol. 80, 3769–3775 (2014).

    PubMed  PubMed Central  Google Scholar 

  70. Nakabachi, A. & Ishikawa, H. Provision of riboflavin to the host aphid, Acyrthosiphon pisum, by endosymbiotic bacteria, Buchnera. J. Insect Physiol. 45, 1–6 (1999).

    CAS  PubMed  Google Scholar 

  71. Fan, H. W. et al. Genomic analysis of an ascomycete fungus from the rice planthopper reveals how it adapts to an endosymbiotic lifestyle. Genome Biol. Evol. 7, 2623–2634 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Noda, H. & Koizumi, Y. Sterol biosynthesis by symbiotes: cytochrome P450 sterol C-22 desaturase genes from yeast-like symbiotes of rice planthoppers and anobiid beetles. Insect Biochem. Mol. Biol. 33, 649–658 (2003).

    CAS  PubMed  Google Scholar 

  73. Moran, N. A. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc. Natl Acad. Sci. USA 93, 2873–2878 (1996).

    CAS  PubMed  Google Scholar 

  74. Fares, M. A., Moya, A. & Barrio, E. GroEL and the maintenance of bacterial endosymbiosis. Trends Genet. 20, 413–416 (2004).

    CAS  PubMed  Google Scholar 

  75. Price, D. R. et al. Aphid amino acid transporter regulates glutamine supply to intracellular bacterial symbionts. Proc. Natl Acad. Sci. USA 111, 320–325 (2014).

    CAS  PubMed  Google Scholar 

  76. Duncan, R. P., Feng, H., Nguyen, D. M. & Wilson, A. C. Gene family expansions in aphids maintained by endosymbiotic and nonsymbiotic traits. Genome Biol. Evol. 8, 753–764 (2016).

    PubMed  PubMed Central  Google Scholar 

  77. Cocucci, E. & Meldolesi, J. Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol. 25, 364–372 (2015).

    CAS  PubMed  Google Scholar 

  78. Pande, S. et al. Metabolic cross-feeding via intercellular nanotubes among bacteria. Nat. Commun. 6, 6238 (2015).

    CAS  PubMed  Google Scholar 

  79. Russell, C. W., Bouvaine, S., Newell, P. D. & Douglas, A. E. Shared metabolic pathways in a coevolved insect–bacterial symbiosis. Appl. Environ. Microbiol. 79, 6117–6123 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Kaleta, C., Schauble, S., Rinas, U. & Schuster, S. Metabolic costs of amino acid and protein production in Escherichia coli. Biotechnol. J. 8, 1105–1114 (2013).

    CAS  PubMed  Google Scholar 

  81. Poliakov, A. et al. Large-scale label-free quantitative proteomics of the pea aphid–Buchnera symbiosis. Mol. Cell. Proteomics 10, M110 007039 (2011).

    PubMed  PubMed Central  Google Scholar 

  82. Luan, J. B. et al. Metabolic coevolution in the bacterial symbiosis of whiteflies and related plant sap-feeding insects. Genome Biol. Evol. 7, 2635–2647 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Work in the author's laboratory is financially supported by the US National Science Foundation (NSF; grant IOS-1354743) and the Sarkaria Institute of Insect Physiology and Toxicology.

Author information

Authors and Affiliations

  1. Department of Entomology and Department of Molecular Biology and Genetics, Cornell University, Ithaca, 14853, New York, USA

    Angela E. Douglas

Authors
  1. Angela E. Douglas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Angela E. Douglas.

Ethics declarations

Competing interests

The author declares no competing financial interests.

Supplementary information

Supplementary information S1 (table)

Multi-partner symbioses in Hemipteran insects (PDF 173 kb)

PowerPoint slides

Glossary

Endosymbionts

Microorganisms that are localized to the internal organs, often within cells, of animals.

Essential amino acids

(EAAs). Ten of the 20 amino acids that constitute proteins, but which cannot be synthesized by animals (some animals, but not hemipteran insects, have limited capacity to synthesize one essential amino acid, arginine).

Stylet

Mouthparts of hemipteran insects, in which the mandibles and maxillae are modified to pierce into plant or animal tissues and take up liquid food.

Primary symbionts

Endosymbionts that are required by an insect host and that are invariably vertically transmitted to the insect offspring.

Bacteriocyte

A specialized insect cell that houses and maintains intracellular endosymbionts.

Transovarial transmission

Vertical transmission of endosymbiotic microorganisms by transfer to the offspring insect through the ovaries of the reproductive female.

Companion symbionts

Endosymbionts that co-occur with the primary symbiont 'Candidatus Sulcia muelleri' in the suborder Auchenorrhyncha. Companion symbionts are generally required by the insect and are vertically transmitted (similarly to primary symbionts). The identity of the companion symbionts varies among different auchenorrhynchan lineages.

Secondary symbionts

Endosymbionts that co-occur with the primary symbiont in the suborder Sternorrhyncha. Some secondary symbionts are required by the insect, but many are facultative for the insect and show patterns of mixed vertical and horizontal transmission.

Syncytium

A cell that contains several nuclei that are generated either through rounds of nuclear division without cytokinesis or through the fusion of multiple cells.

Haemolymph

A blood-like fluid in insects.

Nested endosymbiosis

Symbiosis in which the cells of one endosymbiont are localized within a cell of a second endosymbiont.

Parasitoid

An insect that develops within a single insect host of a different species, which it kills before emerging as an adult.

Encapsulation

An innate immune response of an insect by which a parasite is enclosed within many layers of haemocytes and killed, often by the cytotoxic products of the haemocytes.

Epistatic interactions

Interactions between genes: the phenotypic effect of one gene is influenced by another gene.

Polyketide

A group of complex aromatic secondary metabolites, which includes macrolides, polyenes and tetracyclines.

Genomic decay

The accumulation of deleterious mutations and gene loss by genetic drift in organisms that have a small effective population size.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Douglas, A. How multi-partner endosymbioses function. Nat Rev Microbiol 14, 731–743 (2016). https://doi.org/10.1038/nrmicro.2016.151

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro.2016.151

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing