Symbiotic microorganisms: untapped resources for insect pest control Angela E. Douglas TRENDS in Biotechnology Vol.25 No.8 Opinion

objectives Two approaches have particular potential: 1- The disruption of microbial symbionts required by insect pests. 1- The disruption of microbial symbionts required by insect pests. 2- Manipulation of microorganisms with major impacts on insect traits contributing to their pest status (e.g. capacity to vector diseases, natural enemy resistance)

The effectiveness of control methods in 20 th century Rapid and effective methods to control insect pests represent one of the many scientific achievements of the twentieth century. This has been achieved principally through chemical insecticides, with other approaches, including biological control agents and sterile-insect technique, valuable for certain pest species and contexts

Defect of pest control strategies However, the ‘ many strategies ’ in our insect pest control arsenal are not enough. Why? (i) An increasing recognition of the limitations of current approaches through pest resistance, and public and regulatory concerns over environmental and human health impacts, (ii) Novel pest scenarios (both ‘ new pests ’ and (ii) Novel pest scenarios (both ‘ new pests ’ and ‘ old pests in new places ’ ), as a result of burgeoning and Increasingly mobile human populations and climate change

Core of the problem Until recently, symbiotic microorganisms have been far more important to many insects than to most biologists, for the simple reason that most entomologists are not expert in microbiology

Perspective (Opinion or Shifting ) Douglas said that “ I believe that the science is now poised to shift from an exclusive focus on fundamental research towards application ”

Current approach Current approach A further control strategy based on the reproductive distortion of insect populations by the bacterium Wolbachia has been considered widely in the recent literature HM What is Wolbachia?

The diversity of insect – microbial symbioses Importantly, very few of these microorganisms are ‘ professional ’ pathogens. Most are harmless or beneficial to the insect, or only deleterious under specific circumstances

Only deleterious under specific circumstances When the Bt toxin is ingested by gypsy moth caterpillars, it disrupts the insect gut wall. This allows otherwise harmless bacteria in the gut lumen of the insect to gain access to the body tissues, where they proliferate, rapidly causing septicaemia and insect death. In other words, each of the gut microbiota and Bt toxin is harmless on its own, and pathogenicity is caused by their co-occurrence HM How was the gypsy moth entered USA?

Disruption of microbial symbioses required by insect pest The mycetocyte symbioses include various pest taxa, including planthoppers, aphids, tsetse flies and lice, with the common trait that they feed on grossly unbalanced or inadequate diets (blood, plant sap, wood, etc.)

This symbiosis-based strategy is suitable for situations requiring the suppression of insect pest populations over a period of days to weeks but not immediate insect death. Antibiotics

Two complementary approaches are needed: to identify specific targets, and to screen for symbiosis-active compounds.

Compounds active against mycetocyte symbioses The search for compounds active against mycetocyte symbioses has barely started. A probable source is the plant kingdom, for such compounds would provide defense against phytophagous insects with mycetocyte symbionts.

Compounds active against mycetocyte symbioses This yielded certain labiate plants that selectively depressed the performance of aphids containing the usual complement of Buchnera bacteria.

Compounds active against mycetocyte symbioses there might be overlap in the underlying molecular mechanisms through convergence, leading to the availability of single compounds (or classes of compounds) active against a range of insect pests of agricultural, medical and veterinary importance

Symbiont-mediated manipulation of insect traits The purpose of this strategy is not to eradicate the pest but to eliminate the harmful effects of the pest It is particularly relevant to insect vectors of disease. If only we could engineer vector- incompetent insects!

Symbiont-mediated manipulation of insect traits To date, most progress has been made by introducing traits to symbiotic microorganisms by genetic manipulation. This approach was originally termed paratransgenesis, defined formally as the modification of the insect phenotype by genetic transformation of its associated microorganisms(s), and it is also referred to as ‘ symbiont-based control ’ and ‘ symbiotic control ’. This approach is particularly suitable for microbial symbionts that can be cultured and transformed readily.