The plant rhizosheath–root niche is an edaphic “mini-oasis” in hyperarid deserts with enhanced microbial competition

Abstract

Plants have evolved unique morphological and developmental adaptations to cope with the abiotic stresses imposed by (hyper)arid environments. Such adaptations include the formation of rhizosheath–root system in which mutualistic plant–soil microbiome associations are established: the plant provides a nutrient-rich and shielded environment to microorganisms, which in return improve plant-fitness through plant growth promoting services. We hypothesized that the rhizosheath–root systems represent refuge niches and resource islands for the desert edaphic microbial communities. As a corollary, we posited that microorganisms compete intensively to colonize such “oasis” and only those beneficial microorganisms improving host fitness are preferentially selected by plant. Our results show that the belowground rhizosheath–root micro-environment is largely more hospitable than the surrounding gravel plain soil with higher nutrient and humidity contents, and cooler temperatures. By combining metabarcoding and shotgun metagenomics, we demonstrated that edaphic microbial biomass and community stability increased from the non-vegetated soils to the rhizosheath–root system. Concomitantly, non-vegetated soil communities favored autotrophy lifestyle while those associated with the plant niches were mainly heterotrophs and enriched in microbial plant growth promoting capacities. An intense inter-taxon microbial competition is involved in the colonization and homeostasis of the rhizosheath zone, as documented by significant enrichment of antibiotic resistance genes and CRISPR-Cas motifs. Altogether, our results demonstrate that rhizosheath–root systems are “edaphic mini-oases” and microbial diversity hotspots in hyperarid deserts. However, to colonize such refuge niches, the desert soil microorganisms compete intensively and are therefore prepared to outcompete potential rivals.

Diversity and adaptation properties of actinobacteria associated with Tunisian stone ruins

“…Driven by the substantial overlap in the structures of newly discovered antimicrobial compounds from Streptomyces , researchers have begun to focus on rare actinobacteria, which are viewed as vast potential reservoirs of novel natural products ( Dhakal et al, 2017 ). Some of the rare actinobacteria detected in this study, such as members of Actinokineospora , Micromonospora , and Nocardia , inhibited the growth of pathogen indicator organisms, showing their potential as antagonist strains, which should give these bacteria a competitive advantage during stone colonization: they are equipped to compete for space and resources against the other members of the community, as recently showed during the colonization of “mini-oases” plant-mediated in hyperarid desert ecosystems ( Marasco et al, 2022 ). Also, these microorganisms should not be ignored for their potential in the research for natural products with biotechnological applications.…”

“…Data related to climate (max and min temperature and precipitation) were collected from climate knowledgeportal.worldbank.org, considering the period 1991-2020. Aridity values were obtained from the package R Envirem (Title and Bemmels, 2018) at the resolution of 1 km 2 and mapped as described in (Marasco et al, 2022). At each location, three areas of 1 m × 1 m were sampled, and further used as replicates.…”

Function-Based Rhizosphere Assembly along a Gradient of Desiccation in the Former Aral Sea

“…These results are in line with a recent study by Hanusch and colleagues ( 40 ) suggesting that more deterministic processes such as niche filtering and biotic interactions are the main drivers of community assembly over the course of succession. A recent study conducted in a hyperarid environment also suggested that plants may have coevolved with specific bacterial taxa that possess the capacity to improve the fitness and survival of the host plant ( 41 ). Our study suggests a strong host-driven selection for specific functional traits of the plant-associated microbial community over the course of the revegetation event.…”

The antibiotic crisis: On the search for novel antibiotics and resistance mechanisms

“…These microbial hotspots are particularly enriched in microbial cells when developed in extreme environments, such as harsh terrestrial ecosystems (deserts and drylands) and oligotrophic waters (Red Sea and brine pools). For example, the plant rhizosphere – the soil region directly influenced by plant roots – contains 3–4 orders of magnitude higher population density than surrounding bulk soils (Lv et al., 2023 ), which is exacerbated in deserts where nutrients (notably soil C, N and P) are limited (Marasco et al., 2022 ). While the rhizosphere microbiome is generally studied as a functionality and ecosystem service delivery hotbed, this microbial hotspot concomitantly hosts heightened intense competition between colocalized microorganisms for nutrients and space (Marasco et al., 2022 ).…”