The effect of white grub (Maladera Verticalis) larvae feeding on rhizosphere microbial characterization of aerobic rice (Oryza sativa L.) in Puer City, Yunnan Province, China

Abstract

Background: Rhizosphere microorganisms are vital in plants' growth and development and these beneficial microbes are recruited to the root-zone soil when experiencing various environmental stresses. However, the effect of white grub (Maladera verticalis) larvae feeding on the structure and function of rhizosphere microbial communities of aerobic rice (Oryza sativa L.) is unclear.

Results: In this study, we compared physicochemical properties, enzyme activities, and microbial communities using 18 samples under healthy and M. verticalis larvae-feeding aerobic rice rhizosphere soils at the Yunnan of China. 16 S rRNA and ITS amplicons were sequenced using Illumina high throughput sequencing. M. verticalis larvae feeding on aerobic rice can influence rhizosphere soil physicochemical properties and enzyme activities, which also change rhizosphere microbial communities. The healthy and M. verticalis larvae-feeding aerobic rice rhizosphere soil microorganisms had distinct genus signatures, such as possible_genus_04 and Knoellia genera in healthy aerobic rice rhizosphere soils and norank_f__SC - I-84 and norank_f__Roseiflexaceae genera in M. verticalis larvae-feeding aerobic rice rhizosphere soils. The pathway of the metabolism of terpenoids and polyketides and carbohydrate metabolism in rhizosphere bacteria were significantly decreased after M. verticalis larvae feeding. Fungal parasite-wood saprotroph and fungal parasites were significantly decreased after M. verticalis larvae feeding, and plant pathogen-wood saprotroph and animal pathogen-undefined saprotroph were increased after larvae feeding. Additionally, the relative abundance of Bradyrhizobium and Talaromyces genera gradually increased with the elevation of the larvae density. Bacterial and fungal communities significantly correlated with soil physicochemical properties and enzyme activities, respectively.

Conclusions: Based on the results we provide new insight for understanding the adaptation of aerobic rice to M. verticalis larvae feeding via regulating the rhizosphere environment, which would allow us to facilitate translation to more effective measures.

Keywords: Maladera Verticalis; Oryza sativa; Aerobic rice; Enzyme activities; Physicochemical properties; Rhizosphere microorganisms; White grub.

Fig. 1

An image of a white grub (Maladera verticalis larvae) in the field, which harms aerobic rice roots

Fig. 2

The diversity and composition of rhizosphere bacteria after M. verticalis larvae feeding. (A) The colony-forming units of bacteria in the LB medium. (B) Alpha diversity of the Shannon index at the bacterial genus level. (C) Phylum-level relative frequency in healthy and M. verticalis larvae-feeding aerobic rice rhizosphere bacteria. (D) Heatmap of genus-level in healthy and M. verticalis larvae-feeding aerobic rice rhizosphere bacteria. (E) Genus-level relative frequency in healthy and M. verticalis larvae-feeding aerobic rice rhizosphere bacteria. The relative frequency of log₁₀ fold change (log₁₀FC) was included in the plot. CK, healthy aerobic rice; Mv, M. verticalis larvae-feeding aerobic rice; HGM, Haguoma; HZB, Haoziba; and NG, Nuoguo

Fig. 3

The diversity and composition of rhizosphere fungi after M. verticalis larvae feeding. (A) The colony-forming units of fungi in Thayer–Martin medium with rose bengal and 0.003% streptomycin sulfate. (B) Alpha diversity of Shannon index at the fungal genus level. (C) Phylum-level relative frequency in healthy and M. verticalis larvae-feeding aerobic rice rhizosphere fungi. (D) Heatmap of genus-level in healthy and M. verticalis larvae-feeding aerobic rice rhizosphere fungi. (E) Genus-level relative frequency in healthy and M. verticalis larvae-feeding aerobic rice rhizosphere fungi. The relative frequency of log₁₀ fold change (log₁₀FC) was included in the plot. CK, healthy aerobic rice; Mv, M. verticalis larvae-feeding aerobic rice; HGM, Haguoma; HZB, Haoziba; and NG, Nuoguo

Fig. 4

Significant differences in genus abundance that discriminate healthy and M. verticalis larvae-feeding aerobic rice rhizosphere microorganisms. LDA (LDA value > 2.0 and P value ≤ 0.05) scores of top featured bacterial (A) and fungal (B) genera in healthy and M. verticalis larvae-feeding aerobic rice rhizosphere. The square and circle represent the CK and Mv groups, respectively. CK, healthy aerobic rice; Mv, M. verticalis larvae-feeding aerobic rice; HGM, Haguoma; HZB, Haoziba; and NG, Nuoguo

Fig. 5

M. verticalis larvae-feeding induced changed aerobic rice rhizosphere soil microbial community and composition. Histogram showing significantly different phyla (A) and genera (B). (C) Aerobic rice rhizosphere soil bacterial community. (D) Histogram showing significantly different genera. (E) Aerobic rice rhizosphere soil fungi community. CK, healthy aerobic rice; Mv, M. verticalis larvae-feeding aerobic rice

Fig. 6

Rhizosphere microbial community functional prediction. (A) Statistical differences in predicated bacterial functional characteristics between CK and Mv rhizosphere soil at KEGG level 2 (A) and KEGG level 3 (B). (C) Statistical differences in predicated fungal functional characteristics between CK and Mv rhizosphere soil. The relative abundance of log₁₀ fold change (log₁₀FC) was included in the plot. CK, healthy aerobic rice; Mv, M. verticalis larvae-feeding aerobic rice; HGM, Haguoma; HZB, Haoziba; and NG, Nuoguo

Fig. 7

Relationship between soil properties and rhizosphere microbial community structures. (A) Relationship between healthy aerobic rice rhizosphere soils properties and rhizosphere microbial community structures. (B) Relationship between M. verticalis larvae-feeding aerobic rice rhizosphere soils properties and rhizosphere microbial community structures. ^*, ^**, and ^*** indicate significant differences at P < 0.05, P < 0.01, and P < 0.001

Fig. 8

Relationships between M. verticalis larvae density and aerobic rice rhizosphere soil microbial composition. Relationships between M. verticalis larvae density and the relative abundance of Bradyrhizobium (A) and Talaromyces (B) genera. CK, healthy aerobic rice; Mv, M. verticalis larvae-feeding aerobic rice