Expression, activity, and consequences of biochemical inhibition of alpha- and beta-glucosidases in different life stages of Culex quinquefasciatus

Authors: BURGESS, EDWIN - University Of Florida; Sanscrainte, Neil; TAYLOR, CAITLIN - University Of Florida; BUSS, LYLE - University Of Florida; Estep Iii, Alden

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/8/2023
Publication Date: 8/29/2023
Citation: Burgess, E.R., Sanscrainte, N.D., Taylor, C.E., Buss, L.A., Estep Iii, A.S. 2023. Expression, activity, and consequences of biochemical inhibition of alpha- and beta-glucosidases in different life stages of Culex quinquefasciatus. PLOS ONE. 18(8). https://doi.org/10.1371/journal.pone.0286609.
DOI: https://doi.org/10.1371/journal.pone.0286609

Interpretive Summary: Mosquitoes use digestive enzymes to digest blood and sugar meals that enable them to survive and reproduce. Sugar meals, typically from plants, are critical for key physiological processes in both male and female mosquitoes, whereas blood meals are taken only by females. Enzymes involved in sugar digestion have been the subject of study for decades but have been limited to a relatively narrow range of mosquito species. Here we describe the nature of alpha-glucosidases and the unexplored beta-glucosidases that may help Cx. quinquefasciatus mosquito larvae acquire nutrients from their aquatic environments. We also test several inhibitors of alpha-glucosidases and beta-glucosidases to determine if they may be potentially useful for mosquito control.

Technical Abstract: Mosquitoes utilize a plethora of digestive enzymes to meet the challenge of both requisite blood and sugar meals that enable them to survive and reproduce. Sugar meals, typically derived from plant sources, are critical for key physiological processes in both male and female mosquitoes, whereas blood meals are taken only by females to complete oogenesis. Enzymes involved in sugar digestion have been the subject of study for decades but have been limited to a relatively narrow range of mosquito species. The southern house mosquito, Culex quinquefasciatus, is of public health importance and seldom considered in these types of studies outside of topics related to Bacillus sphaericus, a biocontrol agent that requires interaction with a specific gut-associated '-glucosidase. Here we sought to describe the nature of alpha-glucosidases and the unexplored beta-glucosidases that may aid Cx. quinquefasciatus larvae in acquiring nutrients from cellulosic sources in their aquatic environments. Consistent with our hypothesis, we found both alpha- and beta-glucosidase activity in larvae. Interestingly, '-glucosidase activity all but disappeared at the pupal stage and remained suppressed in adults, while '-glucosidase activity remained in the pupal stage and then exceeded larval activity by approximately 1.5-fold. Expression of putative alpha- and beta-glucosidase genes chosen did not generally follow the trends seen in enzyme activities. When the '-glucosidase inhibitor acarbose was administered to adults, mortality was seen especially in males but also in females after two days of exposure and key energetic storage molecules, glycogen and lipids, were significantly lower than controls. In contrast, administering the beta-glucosidase inhibitor conduritol beta-epoxide to larvae did not produce mortality even at the highest soluble concentration. Here we provide insights into the importance of alpha- and beta-glucosidases on the survival of Cx. quinquefasciatus in their three mobile life stages.