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

Tohir A Bozorov,Bakhtiyor A Rasulov,Daoyuan Zhang

doi:10.1038/s41598-019-41368-x

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.

Highlights

The genus Agrilus comprises diverse exotic and agriculturally important wood-boring insects that have evolved efficient digestive systems
We explored the diversity of the microbial community that colonizes the larval gut of the invasive wood-borer A. mali to elucidate the digestive process of larvae for plant cell-wall component breakdown
Our results demonstrated that the gut bacterial community of A. mali larvae is relatively complex

Summary

Introduction

The genus Agrilus comprises diverse exotic and agriculturally important wood-boring insects that have evolved efficient digestive systems. 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. Many wood-boring beetles have become significant forest pests that cause extensive mortality of economically important trees Exploration of their feeding capabilities is essential for developing pest management programs[15,16,17]. Little is known about wood-boring larvae feeding behaviour, digestive tracts, gut microbiota, diversity and the symbiotic interactions with insects that develop within the stem phloem and cambium tissues. Larvae harbour diverse microbial communities, and exploring the role of the gut microbiota helps in understanding insect digestion of plant cell-wall compounds. A symbiotic interaction between gut microbiota and insects likely aids in the digestion of plant cell-wall polymers and provides nutritional supplements for the hosts

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