Abstract
Despite the relevance of complex root microbial communities for plant health, growth and productivity, the molecular basis of these plant-microbe interactions is not well understood. Verrucomicrobia are cosmopolitans in the rhizosphere, nevertheless their adaptations and functions are enigmatic since the proportion of cultured members is low. Here we report four cultivated Verrucomicrobia isolated from rice, putatively representing four novel species, and a novel subdivision. The aerobic strains were isolated from roots or rhizomes of Oryza sativa and O. longistaminata. Two of them are the first cultivated endophytes of Verrucomicrobia, as validated by confocal laser scanning microscopy inside rice roots after re-infection under sterile conditions. This extended known verrucomicrobial niche spaces. Two strains were promoting root growth of rice. Discovery of root compartment-specific Verrucomicrobia permitted an across-phylum comparison of the genomic conformance to life in soil, rhizoplane or inside roots. Genome-wide protein domain comparison with niche-specific reference bacteria from distant phyla revealed signature protein domains which differentiated lifestyles in these microhabitats. Our study enabled us to shed light into the dark microbial matter of root Verrucomicrobia, to define genetic drivers for niche adaptation of bacteria to plant roots, and provides cultured strains for revealing causal relationships in plant-microbe interactions by reductionist approaches.
Highlights
In land plants, roots are the primary site for interactions with diverse microbes, which are recruited from soil and filtered by the plant[1]
Across-phylum comparison of protein domains encoded in genomes of well-studied reference endophytes, root surface and soil bacteria, allowed to identify novel signature protein domains for compartments, and provided a broader insight in adaptations for plant-associated lifestyle that are common in distant phyla
Among a larger culture collection of roughly 250 strains of mainly Proteobacteria, Actinobacteria and Firmicutes, four divergent Verrucomicrobia were detected that had been isolated under aerobic culture conditions: Small colonies of slow-growing bacteria were found among fast-growing strains upon extended incubation of agar plates
Summary
Roots are the primary site for interactions with diverse microbes, which are recruited from soil and filtered by the plant[1]. The generally poor cultivation success of Verrucomicrobia has impaired progress in understanding their ecology and capacities[11].Culture-independent methods suggest verrucomicrobial communities in many diverse biomes including soils[11], where they drive biogeographical pattern changes[12]. Even in these studies, primer bias in commonly used PCR primers may lead to an underestimation of 16S rRNA genes during amplification[13]. Across-phylum comparison of protein domains encoded in genomes of well-studied reference endophytes, root surface and soil bacteria, allowed to identify novel signature protein domains for compartments, and provided a broader insight in adaptations for plant-associated lifestyle that are common in distant phyla
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