The evolution of new enzyme function: lessons from xenobiotic metabolizing bacteria versus insecticide‐resistant insects

Abstract

Here, we compare the evolutionary routes by which bacteria and insects have evolved enzymatic processes for the degradation of four classes of synthetic chemical insecticide. For insects, the selective advantage of such degradative activities is survival on exposure to the insecticide, whereas for the bacteria the advantage is simply a matter of access to additional sources of nutrients. Nevertheless, bacteria have evolved highly efficient enzymes from a wide variety of enzyme families, whereas insects have relied upon generalist esterase-, cytochrome P450- and glutathione-S-transferase-dependent detoxification systems. Moreover, the mutant insect enzymes are less efficient kinetically and less diverged in sequence from their putative ancestors than their bacterial counterparts. This presumably reflects several advantages that bacteria have over insects in the acquisition of new enzymatic functions, such as a broad biochemical repertoire from which new functions can be evolved, large population sizes, high effective mutation rates, very short generation times and access to genetic diversity through horizontal gene transfer. Both the insect and bacterial systems support recent theory proposing that new biochemical functions often evolve from ‘promiscuous’ activities in existing enzymes, with subsequent mutations then enhancing those activities. Study of the insect enzymes will help in resistance management, while the bacterial enzymes are potential bioremediants of insecticide residues in a range of contaminated environments.

The classification of esterases: an important gene family involved in insecticide resistance - A review

“…The histidine residue's affinity to water molecules is an important part of the second step (Fig. 4) and enables the enzyme to return to its active state and release the acid molecule (Testa & Kramer 2007, Russell et al 2011). This hydrolysis step of the reaction is a common process among hydrolases and corresponds to a nucleophilic attack of water on the acylated enzyme and release of the acid moiety of the carboxylic ester and the free active enzyme (Ollis et al 1992, Sogorb & Vilanova 2002.…”

“…The main mechanisms described to date involve either point mutation in insecticide-targeted sites and/or more efficient detoxification mechanisms. The latter, also known as metabolic resistance mainly occurs due to an increase in the expression or activity of three major enzyme families: esterases (EST), glutathione-S-transferases and the cytochrome P450 superfamily of enzymes (Beaty & Marquadt 1996, Hemingway & Ranson 2000, Hemingway et al 2004, Li et al 2007, Russell et al 2011. Measuring the activity of these enzymes in natural populations is an important step in monitoring insecticide resistance mechanisms worldwide and should be conducted together with the surveillance of control efficacy to prevent significant changes in susceptibility to the insecticides being used (Brogdon 1989, Brogdon & McAllister 1998, Coleman & Hemingway 2007, Polson et al 2011.…”

Anti-insect potential of a lectin from the tuber, Dioscorea mangenotiana towards Eldana saccharina (Lepidoptera: Pyralidae)

“…Acid phosphatase activity increased during the normal development of E. saccharina larvae whereas alkaline phosphatase showed a continuous decrease after 72 h. But the treatment of the larvae with DML I resulted in significant decrease in the activities of the two enzymes (p < 0.05) when compared with the control (Figure 5B and C). The role of esterases in development of resistance and in sequestration of xenobiotics has been established (Russel et al, 2011). The increase in the plateau of esterase activity in the lectin -treated larvae suggest that esterases might be playing a significant role in detoxification of D. mangenotina -lectin I and the increase in activity could be attributed to positive feedback response (Kaur and Arora, 2009).…”

X-Ray Structure of the Amidase Domain of AtzF, the Allophanate Hydrolase from the Cyanuric Acid-Mineralizing Multienzyme Complex

“…Since atrazine was introduced in the 1950s, bacteria have evolved highly efficient catabolic pathways that allow the use of atrazine as a sole nitrogen and carbon source (7)(8)(9)(10). These pathways have provided valuable insights into the evolutionary processes that drive the establishment of new enzyme function and new catabolic pathways (11)(12)(13)(14)(15).…”