Characterization of the gut microbiota of invasive Agrilus mali Matsumara (Coleoptera: Buprestidae) using high-throughput sequencing: uncovering plant cell-wall degrading bacteria

Abstract

The genus Agrilus comprises diverse exotic and agriculturally important wood-boring insects that have evolved efficient digestive systems. Agrilus mali Matsumara, an invasive insect, is causing extensive mortality to endangered wild apple trees in Tianshan. In this study, we present an in-depth characterization of the gut microbiota of A. mali based on high-throughput sequencing of the 16S rRNA gene and report the presence of lignocellulose-degrading bacteria. Thirty-nine operational taxonomic units (OTUs) were characterized from the larval gut. OTUs represented 6 phyla, 10 classes, 16 orders, 20 families, and 20 genera. The majority of bacterial OTUs belonged to the order Enterobacteriales which was the most abundant taxa in the larval gut. Cultivable bacteria revealed 9 OTUs that all belonged to Gammaproteobacteria. Subsequently, we examined the breakdown of plant cell-wall compounds by bacterial isolates. Among the isolates, the highest efficiency was observed in Pantoea sp., which was able to synthesize four out of the six enzymes (cellulase, cellobiase, β-xylanase, and β-gluconase) responsible for plant-cell wall degradation. One isolate identified as Pseudomonas orientalis exhibited lignin peroxidase activity. Our study provides the first characterization of the gut microbial diversity of A. mali larvae and shows that some cultivable bacteria play a significant role in the digestive tracts of larvae by providing nutritional needs.

Comparison of gut bacterial communities and their associations with host diets in four fruit borers

“…We can hypothesize that this family was present in all of the insects mainly because the metabolic versatility could be able to help the insects adapt their different environments. The highest relative abundance genus in the Enterobacteriaceae was Pantoea , which was responsible for plant cell wall degradation . Apart from fruit borers, Pantoea was observed in other species, such as Agrilus mali 52 and Ceratitis capitate .…”

“…The highest relative abundance genus in the Enterobacteriaceae was Pantoea, which was responsible for plant cell wall degradation. 52 Apart from fruit borers, Pantoea was observed in other species, such as Agrilus mali 52 and Ceratitis capitate. 53 The genus of Pantoea was present across the different lepidopteran species, suggesting the importance of Pantoea in the fitness of moth pests.…”

Gut Bacteria in the Holometabola: A Review of Obligate and Facultative Symbionts

“…The presence of two instances of co-speciation and three instances of symbiosis with an obligate symbiont ( Toju et al 2013 ) in weevils suggests a broader necessity for obligate symbionts among the plant-feeding beetles. Further survey and functional assessment of symbionts in successful phytophagous beetle lineages that primarily harbor facultative gut bacteria including the Buprestidae ( Vasanthakumar et al 2008 , Bozorov et al 2019 ) and Cerambycidae ( Ayayee et al 2014 , Ayayee et al 2016 , Mohammed et al 2018 ) will be necessary to assess the evolution of dependence on obligate bacteria compared with facultatives. The widespread strategy of harboring cellulolytic bacteria in the Scarabaeoidea whose larvae feed primarily on living and dead plant tissue ( Egert et al 2003 , 2005 ; Arias-Cordero et al 2012 ; Ceja-Navarro et al 2014 ; Zhang et al 2018 ; Chouaia et al 2019 ) further emphasizes the need to look more precisely at host biology.…”

Thirst or Malnutrition: The Impacts of Invasive Insect Agrilus mali on the Physiological Status of Wild Apple Trees

“…Originating from northeastern Asia, A. mali is distributed across Korea, Mongolia, China and Russia [7]. In China, A. mali causes damage to domestic apple in the orchards of Qinghai, Gansu and Shanxi Provinces.…”