Functional carbohydrate-active enzymes acquired by horizontal gene transfer from plants in the whiteflyBemisia tabaci

Abstract

SummaryCarbohydrate-active enzymes (CAZymes) 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 CAZymes acquired by horizontal gene transfer (HGT) from bacteria or fungi in a number of phytophagous arthropods and plant-parasitic nematodes. Although the whiteflyBemisia tabaciis a major agricultural pest, knowledge of HGT-acquired CAZymes in this phloem-feeding insect of the Hemiptera order (subfamily Aleyrodinae) is still lacking. We performed a comprehensive and accurate detection of HGT candidates inB. tabaciand identified 136 HGT events, 14 of which corresponding to CAZymes. TheB. tabaciHGT-acquired CAZymes 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 (GH17) and 152 (GH152) acquired from plants are functional beta-glucanases with different substrate specificities, suggesting distinct roles. These two CAZymes are the first characterized GH17 and GH152 glucanases in a metazoan. We identified a lower number of HGT events in the related AleyrodinaeTrialeurodes vaporariorum, with only three HGT-acquired CAZymes, including one GH152 glucanase, suggesting a unique HGT event in the ancestor of the Aleyrodinae. A GH152 CAZyme acquired from plants was also identified in two plant cell-feeding insects of the Thysanoptera order, suggesting convergent acquisition and highlighting the importance of plant-acquired CAZymes in the biology of piercing-sucking insects.