The Lys-motif receptor LYK4 mediates Enterobacter sp. SA187 triggered salt tolerance in Arabidopsis thaliana.

Root endophytes establish beneficial interactions with plants, improving holobiont resilience and fitness, but how plant immunity accommodates beneficial microbes is poorly understood. The multi-stress tolerance-inducing endophyte Enterobacter sp. SA187 triggers a canonical immune response in Arabidopsis only at high bacterial dosage (>108 CFUs ml-1 ), suggesting that SA187 is able to evade or suppress the plant defence system at lower titres. Although SA187 flagellin epitopes are recognized by the FLS2 receptor, SA187-triggered salt tolerance functions independently of the FLS2 system. In contrast, overexpression of the chitin receptor components LYK4 and LYK5 compromised the beneficial effect of SA187 on Arabidopsis, while it was enhanced in lyk4 mutant plants. Transcriptome analysis revealed that the role of LYK4 is intertwined with a function in remodelling defence responses with growth and root developmental processes. LYK4 interferes with modification of plant ethylene homeostasis by Enterobacter SA187 to boost salt stress resistance. Collectively, these results contribute to unlock the crosstalk between components of the plant immune system and beneficial microbes and point to a new role for the Lys-motif receptor LYK4 in beneficial plant-microbe interaction.

Coordinated bacterial and plant sulfur metabolism in Enterobacter sp. SA187-induced plant salt stress tolerance.

Enterobacter sp. SA187 is a root endophytic bacterium that maintains growth and yield of plants under abiotic stress conditions. In this work, we compared the metabolic wirings of Arabidopsis and SA187 in the free-living and endophytic interaction states. The interaction of SA187 with Arabidopsis induced massive changes in bacterial gene expression for chemotaxis, flagellar biosynthesis, quorum sensing, and biofilm formation. Besides modification of the bacterial carbon and energy metabolism, various nutrient and metabolite transporters and the entire sulfur pathway were up-regulated. Under salt stress, Arabidopsis resembled plants under sulfate starvation but not when colonized by SA187, which reprogramed the sulfur regulon of Arabidopsis. In accordance, salt hypersensitivity of multiple Arabidopsis sulfur metabolism mutants was partially or completely rescued by SA187 as much as by the addition of sulfate, L-cysteine, or L-methionine. Many components of the sulfur metabolism that are localized in the chloroplast were partially rescued by SA187. Finally, salt-induced accumulation of reactive oxygen species as well as the hypersensitivity of LSU mutants were suppressed by SA187. LSUs encode a central regulator linking sulfur metabolism to chloroplast superoxide dismutase activity. The coordinated regulation of the sulfur metabolic pathways in both the beneficial microorganism and the host plant is required for salt stress tolerance in Arabidopsis and might be a common mechanism utilized by different beneficial microbes to mitigate the harmful effects of different abiotic stresses on plants.

Author Correction: Bioprospecting desert plant Bacillus endophytic strains for their potential to enhance plant stress tolerance.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Bioprospecting desert plant Bacillus endophytic strains for their potential to enhance plant stress tolerance.

Plant growth-promoting bacteria (PGPB) are known to increase plant tolerance to several abiotic stresses, specifically those from dry and salty environments. In this study, we examined the endophyte bacterial community of five plant species growing in the Thar desert of Pakistan. Among a total of 368 culturable isolates, 58 Bacillus strains were identified from which the 16 most divergent strains were characterized for salt and heat stress resilience as well as antimicrobial and plant growth-promoting (PGP) activities. When the 16 Bacillus strains were tested on the non-host plant Arabidopsis thaliana, B. cereus PK6-15, B. subtilis PK5-26 and B. circulans PK3-109 significantly enhanced plant growth under salt stress conditions, doubling fresh weight levels when compared to uninoculated plants. B. circulans PK3-15 and PK3-109 did not promote plant growth under normal conditions, but increased plant fresh weight by more than 50% when compared to uninoculated plants under salt stress conditions, suggesting that these salt tolerant Bacillus strains exhibit PGP traits only in the presence of salt. Our data indicate that the collection of 58 plant endophytic Bacillus strains represents an important genomic resource to decipher plant growth promotion at the molecular level.

Phylogenetically diverse endophytic bacteria from desert plants induce transcriptional changes of tissue-specific ion transporters and salinity stress in Arabidopsis thaliana.

Salinity severely hampers crop productivity worldwide and plant growth promoting bacteria could serve as a sustainable solution to improve plant growth under salt stress. However, the molecular mechanisms underlying salt stress tolerance promotion by beneficial bacteria remain unclear. In this work, six bacterial isolates from four different desert plant species were screened for their biochemical plant growth promoting traits and salinity stress tolerance promotion of the unknown host plant Arabidopsis thaliana. Five of the isolates induced variable root phenotypes but could all increase plant shoot and root weight under salinity stress. Inoculation of Arabidopsis with five isolates under salinity stress resulted in tissue-specific transcriptional changes of ion transporters and reduced Na+/K+ shoot ratios. The work provides first insights into the possible mechanisms and the commonality by which phylogenetically diverse bacteria from different desert plants induce salinity stress tolerance in Arabidopsis. The bacterial isolates provide new tools for studying abiotic stress tolerance mechanisms in plants and a promising agricultural solution for increasing crop yields in semi-arid regions.

Ethylene induced plant stress tolerance by Enterobacter sp. SA187 is mediated by 2-keto-4-methylthiobutyric acid production.

Several plant species require microbial associations for survival under different biotic and abiotic stresses. In this study, we show that Enterobacter sp. SA187, a desert plant endophytic bacterium, enhances yield of the crop plant alfalfa under field conditions as well as growth of the model plant Arabidopsis thaliana in vitro, revealing a high potential of SA187 as a biological solution for improving crop production. Studying the SA187 interaction with Arabidopsis, we uncovered a number of mechanisms related to the beneficial association of SA187 with plants. SA187 colonizes both the surface and inner tissues of Arabidopsis roots and shoots. SA187 induces salt stress tolerance by production of bacterial 2-keto-4-methylthiobutyric acid (KMBA), known to be converted into ethylene. By transcriptomic, genetic and pharmacological analyses, we show that the ethylene signaling pathway, but not plant ethylene production, is required for KMBA-induced plant salt stress tolerance. These results reveal a novel molecular communication process during the beneficial microbe-induced plant stress tolerance.

Complete Genome Sequence Analysis of Enterobacter sp. SA187, a Plant Multi-Stress Tolerance Promoting Endophytic Bacterium.

Enterobacter sp. SA187 is an endophytic bacterium that has been isolated from root nodules of the indigenous desert plant Indigofera argentea. SA187 could survive in the rhizosphere as well as in association with different plant species, and was able to provide abiotic stress tolerance to Arabidopsis thaliana. The genome sequence of SA187 was obtained by using Pacific BioScience (PacBio) single-molecule sequencing technology, with average coverage of 275X. The genome of SA187 consists of one single 4,429,597 bp chromosome, with an average 56% GC content and 4,347 predicted protein coding DNA sequences (CDS), 153 ncRNA, 7 rRNA, and 84 tRNA. Functional analysis of the SA187 genome revealed a large number of genes involved in uptake and exchange of nutrients, chemotaxis, mobilization and plant colonization. A high number of genes were also found to be involved in survival, defense against oxidative stress and production of antimicrobial compounds and toxins. Moreover, different metabolic pathways were identified that potentially contribute to plant growth promotion. The information encoded in the genome of SA187 reveals the characteristics of a dualistic lifestyle of a bacterium that can adapt to different environments and promote the growth of plants. This information provides a better understanding of the mechanisms involved in plant-microbe interaction and could be further exploited to develop SA187 as a biological agent to improve agricultural practices in marginal and arid lands.

Rhizosphere microbiome metagenomics of gray mangroves (Avicennia marina) in the Red Sea.

Mangroves are unique, and endangered, coastal ecosystems that play a vital role in the tropical and subtropical environments. A comprehensive description of the microbial communities in these ecosystems is currently lacking, and additional studies are required to have a complete understanding of the functioning and resilience of mangroves worldwide. In this work, we carried out a metagenomic study by comparing the microbial community of mangrove sediment with the rhizosphere microbiome of Avicennia marina, in northern Red Sea mangroves, along the coast of Saudi Arabia. Our results revealed that rhizosphere samples presented similar profiles at the taxonomic and functional levels and differentiated from the microbiome of bulk soil controls. Overall, samples showed predominance by Proteobacteria, Bacteroidetes and Firmicutes, with high abundance of sulfate reducers and methanogens, although specific groups were selectively enriched in the rhizosphere. Functional analysis showed significant enrichment in 'metabolism of aromatic compounds', 'mobile genetic elements', 'potassium metabolism' and 'pathways that utilize osmolytes' in the rhizosphere microbiomes. To our knowledge, this is the first metagenomic study on the microbiome of mangroves in the Red Sea, and the first application of unbiased 454-pyrosequencing to study the rhizosphere microbiome associated with A. marina. Our results provide the first insights into the range of functions and microbial diversity in the rhizosphere and soil sediments of gray mangrove (A. marina) in the Red Sea.

Soil and Rhizosphere Associated Fungi in Gray Mangroves (Avicennia marina) from the Red Sea--A Metagenomic Approach.

Covering a quarter of the world's tropical coastlines and being one of the most threatened ecosystems, mangroves are among the major sources of terrestrial organic matter to oceans and harbor a wide microbial diversity. In order to protect, restore, and better understand these ecosystems, researchers have extensively studied their microbiology, yet few surveys have focused on their fungal communities. Our lack of knowledge is even more pronounced for specific fungal populations, such as the ones associated with the rhizosphere. Likewise, the Red Sea gray mangroves (Avicennia marina) remain poorly characterized, and understanding of their fungal communities still relies on cultivation-dependent methods. In this study, we analyzed metagenomic datasets from gray mangrove rhizosphere and bulk soil samples collected in the Red Sea coast, to obtain a snapshot of their fungal communities. Our data indicated that Ascomycota was the dominant phylum (76%-85%), while Basidiomycota was less abundant (14%-24%), yet present in higher numbers than usually reported for such environments. Fungal communities were more stable within the rhizosphere than within the bulk soil, both at class and genus level. This finding is consistent with the intrinsic patchiness in soil sediments and with the selection of specific microbial communities by plant roots. Our study indicates the presence of several species on this mycobiome that were not previously reported as mangrove-associated. In particular, we detected representatives of several commercially-used fungi, e.g., producers of secreted cellulases and anaerobic producers of cellulosomes. These results represent additional insights into the fungal community of the gray mangroves of the Red Sea, and show that they are significantly richer than previously reported.

Chemical compounds toxic to invertebrates isolated from marine cyanobacteria of potential relevance to the agricultural industry.

In spite of advances in invertebrate pest management, the agricultural industry is suffering from impeded pest control exacerbated by global climate changes that have altered rain patterns to favour opportunistic breeding. Thus, novel naturally derived chemical compounds toxic to both terrestrial and aquatic invertebrates are of interest, as potential pesticides. In this regard, marine cyanobacterium-derived metabolites that are toxic to both terrestrial and aquatic invertebrates continue to be a promising, but neglected, source of potential pesticides. A PubMed query combined with hand-curation of the information from retrieved articles allowed for the identification of 36 cyanobacteria-derived chemical compounds experimentally confirmed as being toxic to invertebrates. These compounds are discussed in this review.