De Novo Transcriptomic and Metabolomic Analyses Reveal the Ecological Adaptation of High-Altitude Bombus pyrosoma.

Yanjie Liu,Muhammad Naeem,Jiandong An,Zhiyong Zhou,Huiyue Zhao,Qihua Luo,Yadong Yang,Guangshuo Zhang

doi:10.3390/insects11090631

Abstract

Simple SummaryBumblebees are very important pollinators for many wild and agricultural flowers and play significant roles in natural and agricultural ecosystems. The distribution of bumblebees varies between the species; some species occupy narrow areas, while others have a varied distribution from low to high elevation. Bombus pyrosoma is one of the bumblebee species with a highly varied geomorphological distribution range in China. To answer why some bumblebee species have a varied distribution, we compared the transcriptomic and metabolomic data of B. pyrosoma from the low-altitude North China Plain and the high-altitude Tibet Plateau. The results showed that energy metabolism and innate immunity of the high-altitude B. pyrosoma had been enhanced in order to adapt to the extreme environment of hypoxia and low temperature, compared to the low-altitude bumblebees. This study highlights the ecological adaptation of bumblebees distributed from low- to high-altitude conditions.Bombus pyrosoma is one of the most abundant bumblebee species in China, with a distribution range of very varied geomorphology and vegetation, which makes it an ideal pollinator species for research into high-altitude adaptation. Here, we sequenced and assembled transcriptomes of B. pyrosoma from the low-altitude North China Plain and the high-altitude Tibet Plateau. Subsequent comparative analysis of de novo transcriptomes from the high- and low-altitude groups identified 675 common upregulated genes (DEGs) in the high-altitude B. pyrosoma. These genes were enriched in metabolic pathways and corresponded to enzyme activities involved in energy metabolism. Furthermore, according to joint analysis with comparative metabolomics, we suggest that the metabolism of coenzyme A (CoA) and the metabolism and transport of energy resources contribute to the adaptation of high-altitude B. pyrosoma. Meanwhile, we found many common upregulated genes enriched in the Toll and immune deficiency (Imd)signaling pathways that act as important immune defenses in insects, and hypoxia and cold temperatures could induce the upregulation of immune genes in insects. Therefore, we suppose that the Toll and Imd signaling pathways also participated in the high-altitude adaptation of B. pyrosoma. Like other organisms, we suggest that the high-altitude adaptation of B. pyrosoma is controlled by diverse mechanisms.

Highlights

The Tibet Plateau represents a classic high-altitude environment including hypoxia, cold temperatures and strong ultraviolet rays, which are very harmful to the survival and development of organisms
We suppose that B. pyrosoma has developed some strategies to adapt to different habitats, including varied climates and food sources. Compared to their low-altitude counterparts, B. pyrosoma that inhabit the Tibet Plateau must overcome hypoxic and cold environments and limited food sources to achieve survival and reproduction. With this hypothesis in mind, we examined the de novo transcriptome and metabolome of B. pyrosoma from the Tibet Plateau and the North China Plain to reveal some regulatory pathways or genes involved in the ecological adaptation of high-altitude B. pyrosoma
161,258,620 clean reads were generated from the first site of the low-altitude group (Lg), 173,756,628 clean reads were generated from the second site and 173,564,050 clean reads were generated from the third site

Summary

Introduction

The Tibet Plateau represents a classic high-altitude environment including hypoxia, cold temperatures and strong ultraviolet rays, which are very harmful to the survival and development of organisms. Several studies have examined different organisms, i.e., dogs, pikas, Tibetan horses, Tibetan chickens, snub-nosed monkeys and Drosophila, to understand their hypoxic adaptabilities [8,9,10,11,12,13]. These studies have confirmed that the high-altitude adaptations of various animals and insects share some common characteristics in terms of the metabolism of oxygen and production of energy, as in the case of Drosophila and high-altitude Homo sapiens, which share similar genes that respond to hypoxia [8]. The calcium signaling pathway is an important target of selection for hypoxic high-altitude adaptation in Tibetan chickens [11]

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