Horizontal Gene Transfer and Gene Duplication of β-Fructofuranosidase Confer Lepidopteran Insects Metabolic Benefits

Abstract

Horizontal gene transfer (HGT) is a potentially critical source of material for ecological adaptation and the evolution of novel genetic traits. However, reports on post-transfer duplication in organism genomes are lacking, and the evolutionary advantages conferred on the recipient are generally poorly understood. Sucrase plays an important role in insect physiological growth and development. Here, we performed a comprehensive analysis of the evolution of insect β-fructofuranosidase transferred from bacteria via HGT. We found that post-transfer duplications of β-fructofuranosidase were widespread in Lepidoptera and sporadic occurrences of β-fructofuranosidase were found in Coleoptera and Hymenoptera. β-fructofuranosidase genes often undergo modifications, such as gene duplication, differential gene loss, and changes in mutation rates. Lepidopteran β-fructofuranosidase gene (SUC) clusters showed marked divergence in gene expression patterns and enzymatic properties in Bombyx mori (moth) and Papilio xuthus (butterfly). We generated SUC1 mutations in B. mori using CRISPR/Cas9 to thoroughly examine the physiological function of SUC. BmSUC1 mutant larvae were viable but displayed delayed growth and reduced sucrase activities that included susceptibility to the sugar mimic alkaloid found in high concentrations in mulberry. BmSUC1 served as a critical sucrase and supported metabolic homeostasis in the larval midgut and silk gland, suggesting that gene transfer of β-fructofuranosidase enhanced the digestive and metabolic adaptation of lepidopteran insects. These findings highlight not only the universal function of β-fructofuranosidase with a link to the maintenance of carbohydrate metabolism but also an underexplored function in the silk gland. This study expands our knowledge of post-transfer duplication and subsequent functional diversification in the adaptive evolution and lineage-specific adaptation of organisms.

BmSuc1 Affects Silk Properties by Acting on Sericin1 in Bombyx mori

“…The expression of BmSUC1 in the luminal of the silk gland is higher than that in the glandular ( Figure 2 D,F), and Guo et al also detected the presence of BmSUC1 protein in cocoon silk [ 23 ], indicating that silkworm BmSUC1 is synthesized in the glandular and secreted into the luminal to directly interact with silk protein to play its function. The findings of Dai et al suggest that BmSUC1 has a role in maintaining silk gland metabolic homeostasis [ 34 ]. Loss of BmSUC1 resulted in a disturbance of the silk secretion environment, resulting in a decrease in the secretion of sericin protein and a decrease in the content of sericin in the cocoons ( Figure 8 ).…”

Genome‐wide identification and comparative analysis of lipocalin families in Lepidoptera with an emphasis on Bombyx mori

“…Gene duplication is one of the primary driving forces of genome evolution and a significant mechanism for the establishment of new gene functions (Moore & Purugganan, 2003). Duplicate genes tend to diverge in regulatory and coding regions to produce novel regulatory profiles, novel peptides, or specialized subfunctions (Rogers et al ., 2014; Man & Gallagher, 2020; Dai et al ., 2021). In this study, we observed sequence and exon/intron size differences across 8 lipocalin groups.…”

Paving the Way for Gene Silencing in Lepidoptera: Integrated Sequencing Data Unveil the Rnai Core Machinery of Leucoptera Coffeella.

“…Among Lepidoptera, evidences of host-parasite interactions in moths reveal that sequences transmitted by endosymbiotic microorganisms can affect the host fitness, metabolism, reproduction, population dynamics, and genetic diversity [11]. Concerning feeding and host adaptation, digestive and metabolic benefits conferred by HGT to functional enhancement in favor of lepidopteran insects, such as b-fructofuranosidase [12] and cysteine synthase genes [13].…”