A switch of microbial flora coupled with ontogenetic niche shift in Leptinotarsa decemlineata

Abstract

In Leptinotarsa decemlineata, a final‐instar wandering larva typically undergoes an ontogenetic niche shift (ONS), from potato plant during the foraging stage to its pupation site below ground. Using high‐throughput sequencing of the bacterial 16S ribosomal RNA gene, we determined the hypothesis that the L. decemlineata pupae harbor stage‐specific bacteria to meet the physiological requirements for underground habitat. We identified 34 bacterial phyla, comprising 73 classes, 208 orders, 375 families, and 766 genera in the collected specimens. Microbes across phyla Proteobacteria, Firmicutes, Actinobacteria, and Bacteroidetes were enriched in the pupae, while those in the phylum Proteobacteria, Tenericutes, Firmicutes, and Bacteroidetes dominated in the larvae and adults. A total of 18 genera, including Blastococcus, Corynebacterium_1, Gordonia, Microbacterium, Nocardia, Nocardioides, Rhodococcus, Solirubrobacter, Tsukamurella, Enterococcus, Acinetobacter, Escherichia_Shigella, Lysobacter, Pseudomonas, and Stenotrophomonas, were specifically distributed in pupae. Moreover, soil sterilizing removed a major portion of bacteria in pupae. Specifically, both Enterococcus and Pseudomonas were eliminated in the soil sterilizing and antibiotic‐fed beetle groups. Furthermore, the pupation rate and fresh pupal weight were similar, whereas the emergence rate and adult weight were decreased in the antibiotic‐fed beetles, compared with controls. The results demonstrate that a switch of bacterial communities occurs in the pupae; the pupal‐specific bacteria genera are mainly originated from soil; this bacterial biodiversity improves pupa performance in soil. Our results provide new insight into the evolutionary fitness of L. decemlineata to different environmental niches.

Integrated Microbiome–Metabolome Analysis Reveals Stage-Dependent Alterations in Bacterial Degradation of Aromatics in Leptinotarsa decemlineata

“…The OTUs of bacteria obtained by PCR amplification and sequencing of culture-independent 16S rRNA (Kang et al, 2021 ) were analyzed using KEGG enrichment analysis. At KEGG level 1, metabolism was the most active one, especially in the pupa group ( Figure 1A ).…”

“…Dechloromonas belongs to proteobacteria. Among the 18 pupa-specific genera identified (Kang et al, 2021 ), Escherichia_Shigella, Acinetobacter, Pseudomonas, Lysobacter , and Stenotrophomonas are also proteobacteria. One or several genera listed above may be responsible for the catabolism of the benzoates in L. decemlineata pupae.…”

“…Functional prediction was carried out based on the operational taxonomic units (OTU) data downloaded from the NCBI Sequence Read Archive (SRA) database (Accession Number: PRJNA613266 ) (Kang et al, 2021 ). The OTU data were obtained by high-throughput sequencing of 16S rRNA genes from three biologically independent collections from three consecutive generations.…”

“…One of the strategies is enlisting the cooperation of bacteria (Lesperance and Broderick, 2020 ). These bacteria dramatically change during development (Chen et al, 2016 ; Kang et al, 2021 ). For instance, a shift of microbial flora coupled with ONS has been documented in L. decemlineata , where a total of 18 bacteria genera are specifically distributed in pupae.…”

“…For instance, a shift of microbial flora coupled with ONS has been documented in L. decemlineata , where a total of 18 bacteria genera are specifically distributed in pupae. In contrast, a subset of bacteria genera has larger populations in larvae and adults than those in pupae (Kang et al, 2021 ). Accordingly, we hypothesized that the stage-specific bacteria flora forms different symbiotic interplays with L. decemlineata to biodegrade stage-dependent aromatics from potato plant and agricultural soil, respectively.…”