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

Abstract

Carbohydrate-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 several of phytophagous arthropods and plant-parasitic nematodes. Although the whitefly Bemisia tabaci is 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 in B. tabaci and identified 136 HGT events, 14 of which corresponding to CAZymes. The B. tabaci HGT-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 an animal. We identified a lower number of HGT events in the related Aleyrodinae Trialeurodes vaporariorum, with only three HGT-acquired CAZymes, including a GH152 glucanase, with phylogenetic analysis suggesting a unique HGT event in the ancestor of the Aleyrodinae. Another GH152 CAZyme, 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 CAZymes in the biology of piercing-sucking insects. Significance statementCarbohydrate-active enzymes (CAZymes) are crucial for sugar metabolism. Those involved in plant cell wall degradation are usually absent from animal genomes. In this study, we explored CAZyme repertoires in the genomes of several insects: the phloem-feeding whitefly Bemisia tabaci, a major agricultural pest, and the related greenhouse whitefly Trialeurodes vaporariorum, as well as two Thysanoptera species that feed on plant cell contents. We identified several cases of CAZymes acquired from plant via horizontal gene transfer in the genome of these insects. Notably, we showed that two B. tabaci CAZymes of plant origin function as glucanases with distinct substrate specificities, potentially helping the insect to overcome plant defenses. Overall, these findings enhance our understanding of how the ability to feed on plants evolved in insects.