Journal of Chemical Ecology

, Volume 39, Issue 7, pp 952–961 | Cite as

Microbial Brokers of Insect-Plant Interactions Revisited

Review Article

Abstract

Recent advances in sequencing methods have transformed the field of microbial ecology, making it possible to determine the composition and functional capabilities of uncultured microorganisms. These technologies have been instrumental in the recognition that resident microorganisms can have profound effects on the phenotype and fitness of their animal hosts by modulating the animal signaling networks that regulate growth, development, behavior, etc. Against this backdrop, this review assesses the impact of microorganisms on insect-plant interactions, in the context of the hypothesis that microorganisms are biochemical brokers of plant utilization by insects. There is now overwhelming evidence for a microbial role in insect utilization of certain plant diets with an extremely low or unbalanced nutrient content. Specifically, microorganisms enable insect utilization of plant sap by synthesizing essential amino acids. They also can broker insect utilization of plant products of extremely high lignocellulose content, by enzymatic breakdown of complex plant polysaccharides, nitrogen fixation, and sterol synthesis. However, the experimental evidence for microbial-mediated detoxification of plant allelochemicals is limited. The significance of microorganisms as brokers of plant utilization by insects is predicted to vary, possibly widely, as a result of potentially complex interactions between the composition of the microbiota and the diet and insect developmental age or genotype. For every insect species feeding on plant material, the role of resident microbiota as biochemical brokers of plant utilization is a testable hypothesis.

Keywords

Insect-plant interactions Microbial brokers Microbiota Symbiosis 

Notes

Acknowledgments

This work was supported by NSF grant BIO 1241099, AFRI grant NYW-2011-04650 and the Sarkaria Institute for Insect Physiology and Toxicology.

References

  1. Abo-Khatwa N (1978) Cellulase of fungus-growing termites: a new hypothesis of its origin. Experientia 34:559–560CrossRefGoogle Scholar
  2. Adams AS, Aylward FO, Adams SM, Erbilgin N, Aukema BH, Currie CR, Suen G, Raffa KF (2013) Mountain pine beetles colonizing historical and naive host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. Appl Environ Microbiol. [Epub ahead of print]Google Scholar
  3. Aharon Y, Pasternak Z, Ben Yosef M, Behar A, Lauzon C, Yuval B, Jurkevitch E (2013) Phylogenetic, metabolic, and taxonomic diversities shape mediterranean fruit fly microbiotas during ontogeny. Appl Environ Microbiol 79:303–313PubMedCrossRefGoogle Scholar
  4. Akman Gunduz E, Douglas AE (2009) Symbiotic bacteria enable insect to use a nutritionally inadequate diet. Proc Roy Soc Lond B 276:987–991CrossRefGoogle Scholar
  5. Ali JG, Alborn HT, Stelinski LL (2011) Constitutive and induced subterranean plant volatiles attract both entomopathogenic and plant parasitic nematodes. J Ecol 99:26–35CrossRefGoogle Scholar
  6. Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Revs 59:143–169Google Scholar
  7. Asano Y, Hiramoto T, Nishino R, aiba Y, Kimura T, Yoshihara K, Koga Y, Sudo N (2012) Critical role of gut microbiota in the production of biologically active, free catecholamines in the gut lumen of mice. Amer J Physiol Gastrointest Liver Physiol 303:G1288–G1295CrossRefGoogle Scholar
  8. Bansal R, Hulbert S, Schemerhorn B, Reese JC, Whitworth RJ, Stuart JJ, Chen MS (2011) Hessian fly-associated bacteria: transmission, essentiality, and composition. PLoS One 6:e23170PubMedCrossRefGoogle Scholar
  9. Behar A, Yuval B, Jurkevitch E (2005) Enterobacteria-mediated nitrogen fixation in natural populations of the fruit fly Ceratitis capitata. Mol Ecol 14:2637–2643PubMedCrossRefGoogle Scholar
  10. Behmer ST, Nes WD (2003) Insect sterol nutrition and physiology: a global overview. Adv Insect Physiol 31:1–72CrossRefGoogle Scholar
  11. Behmer ST, Grebenok RJ, Douglas AE (2011) Plant sterols and host plant suitability for a phloem-feeding insect. Funct Ecol 25:484–491CrossRefGoogle Scholar
  12. Berenbaum M (1980) Adaptive significance of midgut pH in larval Lepidoptera. Amer Nat 115:138–146CrossRefGoogle Scholar
  13. Brodbeck BV, Mizell RF, Andersen PC (1993) Physiological and behavioural adaptations of three species of leafhoppers in response to the dilute nutrient content of xylem sap. J Insect Physiol 39:73–81CrossRefGoogle Scholar
  14. Buchner P (1965) Endosymbioses of animals with plant microorganisms. John Wiley & Sons, ChichesterGoogle Scholar
  15. Bugg TD, Ahmad M, Hardiman EM, Singh R (2011) The emerging role for bacteria in lignin degradation and bio-product formation. Curr Opin Biotechnol 22:394–400PubMedCrossRefGoogle Scholar
  16. Calderon-Cortes N, Quesada M, Watanabe H, Cano-Camacho H, Oyama K (2012) Endogenous plant cell wall digestion: a key mechanism in insect evolution. Annu Revs Ecol Evol Syst 43:45–71CrossRefGoogle Scholar
  17. Carini P, Steindler L, Beszteri S, Giovannoni SJ (2013) Nutrient requirements for growth of the extreme oligotroph ‘Candidatus Pelagibacter ubique’ HTCC1062 on a defined medium. ISME J 7:592–602PubMedCrossRefGoogle Scholar
  18. Cazemir AE, Op Den Camp HJM, Hackstein JHP, Vogels GD (1997) Fibre digestion in arthropods. Comp Biochem Physiol A Physiol 118:101–109CrossRefGoogle Scholar
  19. Chaston JM, Douglas AE (2012) Making the most of “omics” for symbiosis research. Biol Bull 223:21–29PubMedGoogle Scholar
  20. Christensen H, Fogel ML (2011) Feeding ecology and evidence for amino acid synthesis in the periodical cicada (Magicicada). J Insect Physiol 57:211–219PubMedCrossRefGoogle Scholar
  21. De Fine Licht HH, Schiott M, Rogowska-Wrzesinska A, Nygaard S, Roepstorff P, Boomsma JJ (2013) Laccase detoxification mediates the nutritional alliance between leaf-cutting ants and fungus-garden symbionts. Proc Natl Acad Sci USA 110:583–587PubMedCrossRefGoogle Scholar
  22. Despres L, David JP, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22:298–307PubMedCrossRefGoogle Scholar
  23. Dong S, Pang K, Bai X, Yu X, Hao P (2011) Identification of two species of yeast-like symbiotes in the brown planthopper, Nilaparvata lugens. Curr Microbiol 62:1133–1138PubMedCrossRefGoogle Scholar
  24. Douglas AE (1989) Mycetocyte symbiosis in insects. Biol Rev Camb Philos Soc 64:409–434PubMedCrossRefGoogle Scholar
  25. Douglas AE (1992) In: Menken SBJ, Visser JH, Harrewijn P (eds) Microbial brokers of insect-plant interactions. Proceedings of the 8th international insect-plant interactions. Kluwer Academic Publishers, Dordrecht, pp 329–336Google Scholar
  26. Douglas AE (2003) The nutritional physiology of aphids. Adv Insect Physiol 31:73–140CrossRefGoogle Scholar
  27. Douglas AE (2009) The microbial dimension in insect nutritional ecology. Funct Ecol 23:38–47CrossRefGoogle Scholar
  28. Douglas AE, Minto LB, Wilkinson TL (2001) Quantifying nutrient production by the microbial symbionts in an aphid. J Exp Biol 204:349–358PubMedGoogle Scholar
  29. Febvay G, Rahbe Y, Rynkiewicz M, Guillaud J, Bonnot G (1999) Fate of dietary sucrose and neosynthesis of amino acids in the pea aphid, Acyrthosiphon pisum, reared on different diets. J Exp Biol 202:2639–2652PubMedGoogle Scholar
  30. Gilbert HJ (2010) The biochemistry and structural biology of plant cell wall deconstruction. Plant Physiol 153:444–455PubMedCrossRefGoogle Scholar
  31. Goodman AL, Kallstrom G, Faith JJ, Reyes A, Moore A, Dantas G, Gordon JI (2011) Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice. Proc Natl Acad Sci USA 108:6252–6257PubMedCrossRefGoogle Scholar
  32. Hatcher PE (1995) Three-way interactions between plant pathogenic fungi, herbivorous insects and their host plants. Biol Rev Camb Philos Soc 70:639–694CrossRefGoogle Scholar
  33. Herrera CM, Pellmyr O (2002) Plant-animal interactions. Blackwell Publishing, Oxford, UK, p 313Google Scholar
  34. Hess M, Sczyrba A, Egan R, Kim TW, Chokhawala H, Schroth G, Luo S, Clark DS, Chen F, Zhang T et al (2011) Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331:463–467PubMedCrossRefGoogle Scholar
  35. Human Microbiome Project Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214CrossRefGoogle Scholar
  36. Ingwell LL, Eigenbrode SD, Bosque-Perez NA (2012) Plant viruses alter insect behavior to enhance their spread. Sci Rep 2:578PubMedCrossRefGoogle Scholar
  37. Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  38. Koch A (1960) Intracellular symbiosis in insects. Annu Rev Microbiol 14:121–140PubMedCrossRefGoogle Scholar
  39. Lasken RS (2013) Single-cell sequencing in its prime. Nat Biotechnol 31:211–212PubMedCrossRefGoogle Scholar
  40. Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Prome JC, Denarie J (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344:781–784PubMedCrossRefGoogle Scholar
  41. Loman NJ, Constantinidou C, Chan JZ, Halachev M, Sergeant M, Penn CW, Robinson ER, Pallen MJ (2012) High-throughput bacterial genome sequencing: an embarrassment of choice, a world of opportunity. Nature Rev Microbiol 10:599–606CrossRefGoogle Scholar
  42. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556PubMedCrossRefGoogle Scholar
  43. Lukjancenko O, Wassenaar TD, Ussery DW (2010) Comparison of 61 sequenced Escherichia coli genomes. Microb Ecol 60:708–720PubMedCrossRefGoogle Scholar
  44. Macdonald SJ, Lin GG, Russell CW, Thomas GH, Douglas AE (2012) The central role of the host cell in symbiotic nitrogen metabolism. Proc Roy Soc Lond B 279:2965–2973CrossRefGoogle Scholar
  45. Mandel MJ, Wollenberg MS, Stabb EV, Visick KL, Ruby EG (2009) A single regulatory gene is sufficient to alter bacterial host range. Nature 458:215–218PubMedCrossRefGoogle Scholar
  46. Martin MM, Martin JS (1978) Cellulose digestion in midgut of fungus-growing termite Macrotermes natalensis: role of acquired enzymes. Science 199:1453–1455PubMedCrossRefGoogle Scholar
  47. McCutcheon JP, Moran NA (2007) Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc Natl Acad Sci USA 104:19392–19397PubMedCrossRefGoogle Scholar
  48. McCutcheon JP, Moran NA (2010) Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution. Genome Biol Evol 2:708–718PubMedGoogle Scholar
  49. McCutcheon JP, Moran NA (2012) Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10:13–26Google Scholar
  50. Mccutcheon JP, Mcdonald BR, Moran NA (2009a) Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc Natl Acad Sci U S A 106:15394–15399CrossRefGoogle Scholar
  51. McCutcheon JP, McDonald BR, Moran NA (2009b) Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial symbiont. PLoS Genet 5:e1000565PubMedCrossRefGoogle Scholar
  52. Mcfall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-Loso T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF et al (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA 110:3229–3236PubMedCrossRefGoogle Scholar
  53. Moran NA (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci USA 104:8627–8633PubMedCrossRefGoogle Scholar
  54. Musat N, Foster R, Vagner T, Adam B, Kuypers MM (2012) Detecting metabolic activities in single cells, with emphasis on nanoSIMS. FEMS Microbiol Rev 36:486–511PubMedCrossRefGoogle Scholar
  55. Nakabachi A, Ishikawa H (1999) Provision of riboflavin to the host aphid, Acyrthosiphon pisum, by endosymbiotic bacteria, Buchnera. J Insect Physiol 45:1–6PubMedCrossRefGoogle Scholar
  56. Nikoh N, Hosokawa T, Oshima K, Hattori M, Fukatsu T (2011) Reductive evolution of bacterial genome in insect gut environment. Genome Biol Evol 3:702–714PubMedCrossRefGoogle Scholar
  57. Noda H, Koizumi Y (2003) Sterol biosynthesis by symbiotes: cytochrome P450 sterol C-22 desaturase genes from yeastlike symbiotes of rice planthoppers and anobiid beetles. Insect Biochem Mol Biol 33:649–658PubMedCrossRefGoogle Scholar
  58. Norris DM, Baker JM, Chu HM (1969) Symbiotic interrelationships between microbes and ambrosia beetles. III. Ergosterol as the source of sterol to the insect. Ann Entomol Soc Am 62:413–414Google Scholar
  59. 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 65:4926–4934PubMedGoogle Scholar
  60. Oppert C, Klingeman WE, Willis JD, Oppert B, Jurat-Fuentes JL (2010) Prospecting for cellulolytic activity in insect digestive fluids. Comp Biochem Physiol B Biochem Mol Biol 155:145–154PubMedCrossRefGoogle Scholar
  61. Palin R, Geitmann A (2012) The role of pectin in plant morphogenesis. Biosystems 109:397–402PubMedCrossRefGoogle Scholar
  62. Pamp SJ, Harrington ED, Quake SR, Relman DA, Blainey PC (2012) Single-cell sequencing provides clues about the host interactions of segmented filamentous bacteria (SFB). Genome Res 22:1107–1119PubMedCrossRefGoogle Scholar
  63. Pant NC, Fraenkel G (1954) Studies of the symbiotic yeasts of the two insect species, Lasioderma serricorne F. and Stegobium paniceum. Biol Bull 107:420–430CrossRefGoogle Scholar
  64. Pauly M, Keegstra K (2010) Plant cell wall polymers as precursors for biofuels. Curr Op Plant Biol 13:305–312CrossRefGoogle Scholar
  65. Pernice M, Meibom A, van den Heuvel A, Kopp C, Domart-Coulon I, Hoegh-Guldberg O, Dove S (2012) A single-cell view of ammonium assimilation in coral-dinoflagellate symbiosis. ISME J 6:1314–1324PubMedCrossRefGoogle Scholar
  66. Pettolino FA, Walsh C, Fincher GB, Bacic A (2012) Determining the polysaccharide composition of plant cell walls. Nature Protoc 7:1590–1607CrossRefGoogle Scholar
  67. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T et al (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65PubMedCrossRefGoogle Scholar
  68. Rasko DA, Rosovitz MJ, Myers GSA, Mogodin EF, Fricke WF, Gajer P, Crabtree J, Sebaihia M, Thomson NR, Chaudhuri R et al (2008) The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bac 190:6881–6893CrossRefGoogle Scholar
  69. Renesto P, Crapoulet N, Ogata H, La Scola B, Vestris G, Claverie JM, Raoult D (2003) Genome-based design of a cell-free culture medium for Tropheryma whipplei. Lancet 362:447–449PubMedCrossRefGoogle Scholar
  70. Ridley EV, Wong AC, Westmiller S, Douglas AE (2012) Impact of the resident microbiota on the nutritional phenotype of Drosophila melanogaster. PLoS One 7:e36765PubMedCrossRefGoogle Scholar
  71. Russell JA, Moreau CS, Goldman-Huertas B, Fujiwara M, Lohman DJ, Pierce NE (2009) Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc Natl Acad Sci USA 106:21236–21241PubMedCrossRefGoogle Scholar
  72. Ryu JH, Kim SH, Lee HY, Bai JY, Nam YD, Bae JW, Lee DG, Shin SC, Ha EM, Lee WJ (2008) Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science 319:777–782PubMedCrossRefGoogle Scholar
  73. Schoonhoven LM, Van Loon JJA, Dicke M (2005) Insect-plant biology, 2nd edn. Chapman & Hall, London, p 409Google Scholar
  74. Shi W, Xie S, Chen X, Sun S, Zhou X, Liu L, Geo P, Kyrpides NC, No E-G, Yuan JS (2013) Comparative genomic analysis of the microbiome of herbivorous insects revealse eco-environmental adaptations: biotechnology applications. PLoS Genet 9:e1003131PubMedCrossRefGoogle Scholar
  75. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS Nature 407:81–86CrossRefGoogle Scholar
  76. Shin SC, Kim S-H, You H, Kim B, Kim AC, Lee K-A, Yoon J-H, Ryu J-H, Lee W-J (2011) Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334:670–674PubMedCrossRefGoogle Scholar
  77. Singh S, Eldin C, Kowalczewska M, Raoult D (2013) Axenic culture of fastidious and intracellular bacteria. Trends Microbiol 21:92–99PubMedCrossRefGoogle Scholar
  78. Slaytor M (1992) Cellulose digestion in termites and cockroaches: what role do symbionts play? Compar Biochem Physiol 103B:775–784Google Scholar
  79. Sloan DB, Moran NA (2012) Endosymbiotic bacteria as a source of carotenoids in whiteflies. Biol Lett 8:986–989PubMedCrossRefGoogle Scholar
  80. Smith K, Mckoy KD, Macpherson AJ (2007) Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Sem Immunol 19:59–69CrossRefGoogle Scholar
  81. Southwood TRE (1985) Interactions of plants and animals: pattern and process. Oikos 44:5–11CrossRefGoogle Scholar
  82. Stecher B, Maier L, Hardt WD (2013) ‘Blooming’ in the gut: how dysbiosis might contribute to pathogen evolution. Nat Rev Microbiol 11:277–284PubMedCrossRefGoogle Scholar
  83. Storelli G, Defaye A, Erkosar B, Hols P, Royet J, Leulier F (2011) Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab 14:403–414PubMedCrossRefGoogle Scholar
  84. Stout MJ, Thaler JS, Thomma BP (2006) Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annu Rev Entomol 51:663–689PubMedCrossRefGoogle Scholar
  85. Tack AJM, Gripenberg S, Roslin T (2012) Cross-kingdom interactions matter: fungal-mediated interactions structure an insect community on oak. Ecol Lett 15:177–185PubMedCrossRefGoogle Scholar
  86. Temperton B, Giovannoni SJ (2012) Metagenomics: microbial diversity through a scratched lens. Curr Opin Microbiol 15:605–612PubMedCrossRefGoogle Scholar
  87. Thompson BM, Grebenok RJ, Behmer ST, Gruner DS (2013) Microbial symbionts shape the sterol profile of the xylem-feeding woodwasp, Sirex noctilio. J Chem Ecol 39:129–139PubMedCrossRefGoogle Scholar
  88. Warnecke F, Luginbuhl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT, Cayouette M, McHardy AC, Djordjevic G, Aboushadi N et al (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–565PubMedCrossRefGoogle Scholar
  89. Watanabe H, Tokuda G (2010) Cellulolytic systems in insects. Annu Rev Entomol 55:609–632PubMedCrossRefGoogle Scholar
  90. Zaneveld JRR, Parfrey LW, van Treuren W, Lozupone C, Clemente JC, Knights D, Stombaugh J, Kuczynski J, Knight R (2011) Combined phylogenetic and genomic approaches for the high-throughput study of microbial habitat adaptation. Trends Microbiol 19:472–482PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of Entomology and Department of Molecular Biology and GeneticsCornell UniversityIthacaUSA

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