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Influential Insider: Wolbachia, an Intracellular Symbiont, Manipulates Bacterial Diversity in Its Insect Host.

ABSTRACT: Facultative intracellular symbionts like the α-proteobacteria Wolbachia influence their insect host phenotype but little is known about how much they affect their host microbiota. Here, we quantified the impact of Wolbachia infection on the bacterial community of the cabbage root fly Delia radicum by comparing the microbiota of Wolbachia-free and infected adult flies of both sexes. We used high-throughput DNA sequencing (Illumina MiSeq, 16S rRNA, V5-V7 region) and performed a community and a network analysis. In both sexes, Wolbachia infection significantly decreased the diversity of D. radicum bacterial communities and modified their structure and composition by reducing abundance in some taxa but increasing it in others. Infection by Wolbachia was negatively correlated to 8 bacteria genera (Erwinia was the most impacted), and positively correlated to Providencia and Serratia. We suggest that Wolbachia might antagonize Erwinia for being entomopathogenic (and potentially intracellular), but would favor Providencia and Serratia because they might protect the host against chemical plant defenses. Although they might seem prisoners in a cell, endocellular symbionts can impact the whole microbiota of their host, hence its extended phenotype, which provides them with a way to interact with the outside world.

SUBMITTER: Ourry M

PROVIDER: S-EPMC8234596 | biostudies-literature | 2021 Jun

REPOSITORIES: biostudies-literature

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Influential Insider: Wolbachia, an Intracellular Symbiont, Manipulates Bacterial Diversity in Its Insect Host.

Ourry Morgane M Crosland Agathe A Lopez Valérie V Derocles Stéphane A P SAP Mougel Christophe C Cortesero Anne-Marie AM Poinsot Denis D

Microorganisms 20210616 6

Facultative intracellular symbionts like the α-proteobacteria Wolbachia influence their insect host phenotype but little is known about how much they affect their host microbiota. Here, we quantified the impact of Wolbachia infection on the bacterial community of the cabbage root fly Delia radicum by comparing the microbiota of Wolbachia-free and infected adult flies of both sexes. We used high-throughput DNA sequencing (Illumina MiSeq, 16S rRNA, V5-V7 region) and per ...[more]

PMID: 34208681

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Project description:Insect-transmitted plant-pathogenic bacteria may alter their vectors' fitness, survival, behavior, and metabolism. Because these pathogens interact with their vectors on the cellular and organismal levels, potential changes at the biochemical level might occur. "Candidatus Liberibacter asiaticus" (CLas) is transmitted in a persistent, circulative, and propagative manner. The genome of CLas revealed the presence of an ATP translocase that mediates the uptake of ATP and other nucleotides from medium to achieve its biological processes, such as growth and multiplication. Here, we showed that the levels of ATP and many other nucleotides were significantly higher in CLas-infected than healthy psyllids. Gene expression analysis showed upregulation for ATP synthase subunits, while ATPase enzyme activity showed a decrease in ATPase activity. These results indicated that CLas stimulated Diaphorina citri to produce more ATP and many other energetic nucleotides, while it may inhibit their consumption by the insect. As a result of ATP accumulation, the adenylated energy charge (AEC) increased and the AMP/ATP and ADP/ATP ratios decreased in CLas-infected D. citri psyllids. Survival analysis confirmed a shorter life span for CLas-infected D. citri psyllids. In addition, electropenetrography showed a significant reduction in total nonprobing time, salivation time, and time from the last E2 (phloem ingestion) to the end of recording, indicating that CLas-infected psyllids were at a higher hunger level and they tended to forage more often. This increased feeding activity reflects the CLas-induced energetic stress. In conclusion, CLas alters the energy metabolism of its psyllid vector, D. citri, in order to secure its need for energetic nucleotides.IMPORTANCE Insect transmission of plant-pathogenic bacteria involves propagation and circulation of the bacteria within their vectors. The transmission process is complex and requires specific interactions at the molecular and biochemical levels. The growth of the plant-pathogenic bacteria in the hemolymph of their vectors indicated that the hemolymph contains all the necessary nutrients for their growth. In addition to nutrients, "Candidatus Liberibacter asiaticus" (CLas) can take up energetic nucleotides, such as ATP, from its vector, Diaphorina citri, using ATP translocase. In this study, we found that the CLas pathogen manipulates the energy metabolism of its insect vector. The accumulation of ATP in CLas-infected D. citri psyllids indicated that CLas induces ATP production to fulfill its need for this energetic compound. As a result of ATP accumulation, a shorter life span and altered feeding behavior were observed. These findings increase our knowledge of insect transmission of the persistent-circulative-propagative type of plant pathogens vectored by insects.

Dataset Information

Influential Insider: Wolbachia, an Intracellular Symbiont, Manipulates Bacterial Diversity in Its Insect Host.

Publications

Influential Insider: <i>Wolbachia</i>, an Intracellular Symbiont, Manipulates Bacterial Diversity in Its Insect Host.

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