Instant Insecticide Resistance by Symbiosis

Contributed by: Zhenguo Lin

In the first half of the 20^th century, chemical pesticides began to be widely used to control a variety of pest species. In her 1962 groundbreaking book Silent Spring, Rachel Carson argued that insects are building up resistance to pesticides. Sadly, as Carson foretold, cases of resistance surfaced within two to 20 years after the introduction of every kind of new insecticide.

It is generally believed that the development of pesticide resistance is generated by changes of genetic information in the pest's genomes and it takes many generations for the pesticide resistant genes to spread in the population. However, some short cuts of acquiring pesticide resistance actually exist. As discussed in my previous blog, it is found that European house mice stole a rodenticide resistant gene through hybridization with Algerian mice (1). In a recent PNAS paper (2) , Kikuchi et al. found an unexpected mechanism of rapid acquisition of insecticide resistance from bacterial symbionts in bean bugs and stinky bugs, which are major pests in agriculture.

Fenitrothion is an organophosphate insecticide that acts as an inhibitor of cholinesterase, so that the nerve function is damaged in insects, humans, and many other animals. Fenitrothion has been heavily used to kill a wide range of pests. However, it has been found that repeated application of fenitrothion leads to rapid increase of fenitrothion-degrading microbes, including some species in the bacterial genus of Burkholderia. These bacteria are able to breakdown feritrothion into products that can be used as their carbon source.

Burkholderia are able to inhabit prosperously in the midgut of the bean bugs as symbionts. The infected bean bugs tend to grow bigger than uninfected bugs, showing mutual benefits of symbiosis.  Kikuchi et al. infected the bean bugs with six different Burkholderia species (strains): three of them are fenitrothion-degrading and the others are non-degrading (Figure 1) . They found that the bean bug infected with fenitrothion-degrading Burkholderia has much higher survival rates than those bugs infected with non-degrading Burkholderia, because the degraded fenitrothion is almost non-toxic to bugs. This study indicates that the insects can become resistant to fenitrothion instantly after they swallow these fenitrothion-degrading bacteria.

Interestingly, unlike many other insects, the offspring of bean bugs does not inherit Burkholderia from their mothers. The bean bugs need to pick the Burkholderia symbionts from surrounding soils each generation before reaching the adult stage. This seems to be inefficient, but it reduces the possibility that the fenitrothion-degrading bacteria become so dependent on their hosts that they lose their chemical-detoxifying genes. In addition, the authors found that the resistant Burkholderia species can increase rapidly in soil after treated with fenitrothion even though these bacteria are very rare in natural environments. The fenitrothion-degrading species rapidly become the most dominant group (>80%) in the Burkholderia population after merely one month of fenitrothion treatment. Therefore, bean bugs can easily acquire pesticide resistance because the resistance may have already developed in the bacterial population even before the arrival of insects. In addition, considering that the highly diversified enzymatic functions of bacteria are able to detoxify many different pesticide, the acquisition of instant pesticide resistances from these bacterial symbionts will definitely bring new challenges for the efficiency of insecticides.

Figure 1.

Insecticide resistance of R. pedestris infected with fenitrothion-degrading Burkholderia strains. (A and B) Survival of third instar nymphs of R. pedestris infected with the fenitrothion-degrading and nondegrading Burkholderia strains when reared on fenitrothion-coated soybean seeds. Results under the host genetic background TKS-1 (A) and TKA-7 (B) are shown. Mean and SE of 10 replicates are indicated at each data point. Each asterisk indicates that survival rate of the insects infected with the fenitrothion-degrading Burkholderiastrain is significantly higher than survival rate of the insects infected with the allied nondegrading strain (likelihood ratio test; P < 0.01). (Cand D) Resistance of Burkholderia-infected R. pedestris to percutaneous application (C) and oral administration (D) of fenitrothion. Third instar nymphs, which were infected either with the fenitrothion-degrading Burkholderia strain (SFA1) or with the nondegrading Burkholderia strain (RPE67), were administrated with 30 pmol of fenitrothion, and their survival was inspected 24 h later. On each of the columns is shown number of surviving insects/total number of treated insects. Statistically significant differences in the survival rates are shown (Fisher’s exact probability test). (2)

References

1. Song, Y.,  Endepols, S.,  Klemann, N., Richter, D.,  Matuschka, F.R., Shih, C.H., Nachman, M.W., and Kohn, M.H. 2011. Adaptive introgression of anticoagulant rodent poison resistance by hybridization between Old World mice. Current Biology 21:1296-1301

2. Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T. 2012. Symbiont-mediated insecticide resistance. Proc Natl Acad Sci USA 109:8618–8622

3. 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