Insect interactions with beneficial microorganisms

Insects are metabolically impoverished.  They cannot synthesize the 9 essential amino acids, various coenzymes (e.g. B vitamins) and sterols.  Many insects can subsist on nutritionally-poor diets because they possess symbiotic microorganisms that provide these crucial nutrients.  Symbiotic insects include plant sap feeders (e.g. aphids, whitefly, planthoppers, leafhoppers), blood feeders (e.g. anopluran lice, bed-bugs, tsetse fly) and the cockroaches and various beetles.  The symbioses in insect pests are potential targets for novel pest management strategies.

We are studying the nutritional interactions of insects with intracellular bacteria and gut microorganisms.

1. Nutritional Interactions in the Aphid Symbiosis

The dominant symbiotic bacterium in most aphids is the γ-proteobacterium Buchnera aphidicola.  The aphid-Buchnera association has persisted for at least 160 million years and it is obligate for both partners.


We have shown that the symbiotic bacteria Buchnera aphidicola provide their aphid hosts with essential amino acids.

Figure. Buchnera-derived essential amino acids supporting the growth of two-to-seven-day-old pea aphid larvae.
[Gündüz and Douglas 2009. Proceedings of the Royal Society of London B 276, 987-991.]

 

We have found that the contribution of Buchnera to aphid nutrition varies among aphid clones. We are sequencing the genomes of the Buchnera in the different aphid clones as a first route to investigate the basis for this variation.
Figure.
Our study of 5 pea aphid clones and 8 black bean aphid clones confirm that these aphids are independent of a dietary supply of most essential amino acids (which are provided by the symbiotic bacteria Buchnera) but up to four essential amino acids is not supplied at a sufficient rate by Buchnera to sustain optimal growth (shown as black circles). [Wilkinson and Douglas 2003. Entomologia Experimentalis et Applicata 106, 103-111; M.J. Searle and Douglas, unpublished]

To further study the nutritional contribution of Buchnera to their aphid host, we have reconstructed the metabolic network of Buchnera APS from the pea aphid.

 

  We have used flux balance analysis (FBA) to investigate the function of the Buchnera metabolic network in silico. By FBA, flux through metabolism is optimized to the desired output (e.g. biomass production) assuming that fluxes producing and consuming a metabolite are equal. We have shown that the amount of each essential amino acid produced by Buchnera in silico varies with the supply of key carbon and nitrogen substrates from the host.

Figure. Calculated export of essential amino acids by Buchnera under two models with limiting supply of either carbon or nitrogen substrates. Equal export under the two models is shown as a dashed line. [Thomas et al. 2009 BMC Systems Biology 3,24]

This in silico analysis illustrates how in principle the aphid host might control essential amino acid production by its Buchnera symbionts.  We are currently seeking to test these models experimentally.

We have found that  the plant range of the black bean aphid Aphis fabae is influenced by additional symbiotic bacteria that occur in some aphids and are collectively known as secondary symbionts. Aphis fabae performs relatively poorly on the red dead nettle Lamium purpureum, and its poor performance is exacerbated by secondary symbionts.

Figure. Relative growth rate (RGR) of 16 clones of Aphis fabae bearing Buchnera only (circles) or Buchnera plus secondary symbionts [either Hamiltonella defensa (squares) or Regiella insecticola (triangles)]. Equal performance on the two plants is shown as a dashed line.  Supplementary experiments involving clones either cured of their secondary symbionts or experimentally infected with secondary symbionts confirmed that it is these bacteria and not the aphid genotype that determines aphid performance on Lamium purpureum.[Chandler et al. 2008 Proceedings of the Royal Society of London B 275, 565-570]

The negative impact of secondary symbionts on aphids reared on L. purpureum is correlated with a ten-fold increase in the abundance of the bacteria.  The effect may be a response to the low phloem nitrogen of L. purpureum because aphids maintained on low-nitrogen diets also perform poorly and have elevated titers of secondary bacteria.

2. Insect Interactions with Gut Microorganisms

The guts of most insects bear nonpathogenic microorganisms.  We have recently initiated a program of research on the relationship between insects and their gut microbiota.  We are investigating the impacts of eliminating the microorganisms on insect fitness and nutrition, and the two-way interaction between microbial function and gene expression of the insect host.  We are working principally with Drosophila melanogaster.
We are also exploring the impact of the antibiotic tetracycline on insect fitness in collaboration with Oxitec Ltd. The results are immediately relevant to the vigor of tetracycline-treated insects used by the RIDL ® technology for producing genetically sterile insects.

If you are interested in this - or any other - aspect of our research, do contact us.