Abstract

As one of the most detrimental citrus pests worldwide, the citrus red mite, Panonychus citri (McGregor), shows extraordinary fecundity, polyphagia, and acaricide resistance, which may be influenced by microbes as other arthropod pests. However, the community structure and physiological function of microbes in P. citri are still largely unknown. Here, the high-throughput sequencing of 16S rDNA amplicons was employed to identify and compare the profile of bacterial communities across the larva, protonymph, deutonymph, and adult stages of P. citri. We observed a dominance of phylums Proteobacteria and Firmicutes, and classes α-, γ-, β-Proteobacteria and Bacilli in the bacterial communities across the host lifespan. Based on the dynamic analysis of the bacterial community structure, a significant shift pattern between the immature (larva, protonymph, and deutonymph) and adult stages was observed. Accordingly, among the major families (and corresponding genera), although the relative abundances of Pseudomonadaceae (Pseudomonas), Moraxellaceae (Acinetobacter), and Sphingobacteriaceae (Sphingobacterium) were consistent in larva to deutonymph stages, they were significantly increased to 30.18 ± 8.76% (30.16 ± 8.75%), 20.78 ± 10.86% (18.80 ± 10.84%), and 11.71 ± 5.49% (11.68 ± 5.48%), respectively, in adult stage, which implied the important function of these bacteria on the adults’ physiology. Actually, the functional prediction of bacterial communities and Spearman correlation analysis further confirm that these bacteria had positively correlations with the pathway of “lipid metabolism” (including eight sublevel pathways) and “metabolism of cofactors and vitamins” (including five sublevel pathways), which all only increased in adult stages. In addition, the bacterial communities were eliminated by using broad-spectrum antibiotics, streptomycin, which significantly suppressed the survival and oviposition of P. citri. Overall, we not only confirmed the physiological effects of bacteria community on the vitality and fecundity of adult hosts, but also revealed the shift pattern of bacterial community structures across the life stages and demonstrated the co-enhancements of specific bacterial groups and bacterial functions in nutritional metabolism in P. citri. This study sheds light on basic information about the mutualism between spider mites and bacteria, which may be useful in shaping the next generation of control strategies for spider mite pests, especially P. citri.

Highlights

  • Many arthropods harbor diverse microbial communities in their digestive systems or intracellular/intercellular niches for symbiotic systems (Dillon and Dillon, 2004)

  • To control the significant variation of microbiota associated with the outdoor environment, P. citri were collected from the sweet orange orchard (N 30◦ 28 26, E 114◦ 21 5 ), Huazhong Agricultural University, Hubei Wuhan, China, and reared for at least 15 populations in indoor condition as follow: the citrus red mites were kept on fresh leaves of Citrus maxima (Burm.) Merr., which were placed ventral-side up and surrounded by wet cotton sliver, and placed on 5 mm layer of distilled water-saturated sponge; leaf disks were renewed weekly; the temperature and moisture were controlled at 26 ± 1◦C and 60 ± 5% Relative Humidity (RH), respectively and the photoperiod was 14 h:10 h

  • The rarefaction curves showed that the accumulation of operational taxonomic units (OTUs) tended toward saturation in the numbers of reads, which indicated that the samples were sufficient to reveal the bacterial communities (Supplementary Figure S1B)

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Summary

Introduction

Many arthropods harbor diverse microbial communities in their digestive systems or intracellular/intercellular niches for symbiotic systems (Dillon and Dillon, 2004). Many of these microbiota play important roles in interactions with their hosts for improved physiology, life history traits, environmental adaptability, reproduction, and are even essential for the host’s survival (Engel and Moran, 2013; Kwong and Moran, 2016). The diversity and structure of microbial communities in some important pests have been identified (Engel and Moran, 2013). In some insect vectors of specific diseases (e.g., mosquito borne disease), Wolbachia have been successfully used in the biological control of these diseases (Pan et al, 2012)

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