Functional Carbohydrate-Active Enzymes Acquired by Horizontal Gene Transfer from Plants in the Whitefly Bemisia tabaci.

Abstract

Carbohydrate-active enzymes involved in the degradation of plant cell walls and/or the assimilation of plant carbohydrates for energy uptake are widely distributed in microorganisms. In contrast, they are less frequent in animals, although there are exceptions, including examples of carbohydrate-active enzymes acquired by horizontal gene transfer from bacteria or fungi in several of phytophagous arthropods and plant-parasitic nematodes. Although the whitefly Bemisia tabaci is a major agricultural pest, knowledge of horizontal gene transfer-acquired carbohydrate-active enzymes in this phloem-feeding insect of the Hemiptera order (subfamily Aleyrodinae) is still lacking. We performed a comprehensive and accurate detection of horizontal gene transfer candidates in B. tabaci and identified 136 horizontal gene transfer events, 14 of which corresponding to carbohydrate-active enzymes. The B. tabaci horizontal gene transfer-acquired carbohydrate-active enzymes were not only of bacterial or fungal origin, but some were also acquired from plants. Biochemical analysis revealed that members of the glycoside hydrolase families 17 and 152 acquired from plants are functional beta-glucanases with different substrate specificities, suggesting distinct roles. These two carbohydrate-active enzymes are the first characterized glycoside hydrolase families 17 and 152 glucanases in an animal. We identified a lower number of horizontal gene transfer events in the related Aleyrodinae Trialeurodes vaporariorum, with only three horizontal gene transfer-acquired carbohydrate-active enzymes, including a glycoside hydrolase family 152 glucanase, with phylogenetic analysis suggesting a unique horizontal gene transfer event in the ancestor of the Aleyrodinae. Another glycoside hydrolase family 152 carbohydrate-active enzyme, most likely independently acquired from plants, was also identified in two plant cell-feeding insects of the Thysanoptera order, highlighting the importance of plant-acquired carbohydrate-active enzymes in the biology of piercing-sucking insects.