Mechanisms Underlying the Rhizosphere-To-Rhizoplane Enrichment of Cellvibrio Unveiled by Genome-Centric Metagenomics and Metatranscriptomics.

Yunzeng Zhang,Entao Wang,Jin Xu,Nian Wang

doi:10.3390/microorganisms8040583

Yunzeng Zhang, Entao Wang + Show 2 more

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https://doi.org/10.3390/microorganisms8040583

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Abstract

Maintaining integrity of the plant cell walls is critical for plant health, however, our previous study showed that Cellvibrio, which is recognized by its robust ability to degrade plant cell walls, was enriched from the citrus rhizosphere to the rhizoplane (i.e., the root surface). Here we investigated the mechanisms underlying the rhizosphere-to-rhizoplane enrichment of Cellvibrio through genome-centric metagenomics and metatranscriptomics analyses. We recovered a near-complete metagenome-assembled genome representing a potentially novel species of Cellvibrio, herein designated Bin79, with genome size of 5.71 Mb across 11 scaffolds. Differential gene expression analysis demonstrated that plant cell wall degradation genes were repressed, whereas genes encoding chitin-degrading enzymes were induced in the rhizoplane compared with the rhizosphere. Enhanced expression of multi-drug efflux genes and iron acquisition- and storage-associated genes in the rhizoplane indicated mechanisms by which Bin79 competes with other microbes. In addition, genes involved in repelling plant immune responses were significantly activated in the rhizoplane. Comparative genomics analyses with five related Cellvibrio strains showed the importance of gene gain events for the rhizoplane adaptation of Bin79. Overall, this study characterizes a novel Cellvibrio strain and indicates the mechanisms involved in its adaptation to the rhizoplane from meta-omics data without cultivation.

Highlights

The genus Cellvibrio comprises Gram-negative, aerobic, flagellated rod-shaped, and cellulolytic bacteria
Owing to root excretion and sloughing, gradients of carbon sources, phytochemicals, as well as other nutrients are formed from the root surface to the surrounding soil, and certain microorganisms are attracted from bulk soil towards roots and form the rhizosphere microbiome [8]
In our previous study [6], we observed that several genera, including Cellvibrio, showed significantly higher relative abundance in the rhizoplane microbiome, a niche characterized by more intimate host–microbe interactions, compared with the rhizosphere microbiome, and the mechanisms underlying their rhizosphere-to-rhizoplane enrichment were further revealed at the whole microbial community level

Summary

Introduction

The genus Cellvibrio comprises Gram-negative, aerobic, flagellated rod-shaped, and cellulolytic bacteria. Plants have developed active cell wall integrity-monitoring systems to sense cell wall damage-associated signals, and complex defense responses, including production of reactive oxygen species and activation of hormone-mediated immune responses, will be triggered once the signals are detected [11]. Under such selective forces, only certain microbes from the rhizosphere microbiome can be further enriched and colonize the rhizoplane niche, leading to lower diversity and density of the microbial community in the rhizoplane compared with that of the rhizosphere [8,12]. We observed that Cellvibrio exhibited significantly higher relative abundance in the citrus rhizoplane than in the rhizosphere [6]

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