Microbial rhodopsins on leaf surfaces of terrestrial plants

Atamna-Ismaeel, Nof; Finkel, Omri M.; Glaser, Fabian; Sharon, Itai; Schneider, R.; Post, Anton F.; Spudich, John L.; Mering, Christian von; Vorholt, Julia A.; Iluz, David; Béjà, Oded; Belkin, Shimshon

doi:10.1111/j.1462-2920.2011.02554.x

Cited by 88 publications

(72 citation statements)

References 37 publications

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“…One such trait, as is apparent from the ubiquity of light-sensing and light protection genes, is the exposure to solar radiation. The ability to sense and utilize light by phyllosphere microbes is emerging as a general trend (39)(40)(41). Indeed, the prevalence of light-sensing and light utilization mechanisms, such as rhodopsin, PYP, and, notably, anoxygenic photosystem genes, reiterates the contention that light is an important resource and signal in the leaf surface habitat.…”

Section: Discussionmentioning

confidence: 99%

Metagenomic Signatures of Bacterial Adaptation to Life in the Phyllosphere of a Salt-Secreting Desert Tree

Finkel

Delmont

Post

et al. 2016

Appl Environ Microbiol

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The leaves of Tamarix aphylla, a globally distributed, salt-secreting desert tree, are dotted with alkaline droplets of high salinity. To successfully inhabit these organic carbon-rich droplets, bacteria need to be adapted to multiple stress factors, including high salinity, high alkalinity, high UV radiation, and periodic desiccation. To identify genes that are important for survival in this harsh habitat, microbial community DNA was extracted from the leaf surfaces of 10 Tamarix aphylla trees along a 350-km longitudinal gradient. Shotgun metagenomic sequencing, contig assembly, and binning yielded 17 genome bins, six of which were >80% complete. These genomic bins, representing three phyla (Proteobacteria, Bacteroidetes, and Firmicutes), were closely related to halophilic and alkaliphilic taxa isolated from aquatic and soil environments. Comparison of these genomic bins to the genomes of their closest relatives revealed functional traits characteristic of bacterial populations inhabiting the Tamarix phyllosphere, independent of their taxonomic affiliation. These functions, most notably light-sensing genes, are postulated to represent important adaptations toward colonization of this habitat. IMPORTANCEPlant leaves are an extensive and diverse microbial habitat, forming the main interface between solar energy and the terrestrial biosphere. There are hundreds of thousands of plant species in the world, exhibiting a wide range of morphologies, leaf surface chemistries, and ecological ranges. In order to understand the core adaptations of microorganisms to this habitat, it is important to diversify the type of leaves that are studied. This study provides an analysis of the genomic content of the most abundant bacterial inhabitants of the globally distributed, salt-secreting desert tree Tamarix aphylla. Draft genomes of these bacteria were assembled, using the culture-independent technique of assembly and binning of metagenomic data. Analysis of the genomes reveals traits that are important for survival in this habitat, most notably, light-sensing and light utilization genes.

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Section: Discussionmentioning

confidence: 99%

Metagenomic Signatures of Bacterial Adaptation to Life in the Phyllosphere of a Salt-Secreting Desert Tree

Finkel

Delmont

Post

et al. 2016

Appl Environ Microbiol

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“…One of the possible advantages of foliar application is that it avoids the adverse influences of many biotic and abiotic factors on soil environment (Pandey et al 2013). Another is the wide surface area of global terrestrial plants (an estimated 6.4×10 8 km 2 ) (Atamna-Ismaeel et al 2012;Penuelas and Terradas 2014), with an immensely diverse microbes (of up to 10 6 -10 7 cells per cm 2 leaf surface) for plant growth promotion (Lindow and Brandl 2003). In view of these aspects, the inoculation of R. palustris onto plant leaf surface would potentially improve plant growth in a more straightforward way, and such effects would inevitably reflect on soil microbial properties due to the important roles of microbes on the plant-soil ecosystem.…”

Section: Introductionmentioning

confidence: 99%

The foliar spray of Rhodopseudomonas palustris grown under Stevia residue extract promotes plant growth via changing soil microbial community

Feng

Wang

et al. 2015

J Soils Sediments

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Purpose The extract of Stevia residue is an ideal substitute for cultivation of the purple nonsulfur bacterium, like Rhodopseudomonas palustris (R. palustris). But the influence of R. palustris grown under residue extract on its downstream application is still not well-characterized. The objective of this study was to assess the effect of foliar spray of R. palustris grown under Stevia residue extract on the plant growth and soil microbial properties. Materials and methods A pot experiment was carried out under the greenhouse condition, consisting of four treatments varying in the sprayed substances: sterilized water (control), R. palustris grown under the chemical medium supplemented with L-tryptophan (SyT), R. palustris grown under Stevia residue extract supplemented with L-tryptophan (ExT), and R. palustris grown under Stevia residue extract supplemented with NH 4 Cl (ExT). The net photosynthesis rate of the uppermost leaves was measured with a portable photosynthesis system. Soil microbial activity was analyzed by microcalorimetry. Soil bacterial community components were determined by real-time quantitative PCR (qPCR) and high-throughput sequencing techniques. Results and discussion Compared with SyT, the R. palustris grown under Stevia residue extract not only improved the plant biomass and the net photosynthetic rate to a large extent, but also increased soil microbial metabolic activity and altered community compositions as well. The treatments receiving R. palustris, especially ExT and ExN, increased the relative abundances of some functional guilds involved in C turnover and nutrient cycling in soil, including Acidobacteria, Actinobacteria, Proteobacteria, Gemmatimonadaetes, Nitrospirae, and Planctomycetes. Conclusions R. palustris grown under the Stevia residue extract showed advantages over that under the chemical medium on both plant growth and soil microbial properties. One of the possible reasons could result from the increases in microbial activity and several bacterial keystone guilds involved into C and nutrient cycling, both of which potentially contribute to the improved plant growth. The results would be conducive to the downstream application of R. palustris in an economical way.

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“…The gene encoding the first discovered member of this group was detected in the genome sequence of an uncultured γ-proteobacterium from oceanic waters (5). Since then, PRs have turned out to be highly abundant in the oceans (6)(7)(8)(9), and organisms containing them, including a cyanobacterium (10) can be found in many other habitats as well (7,(11)(12)(13). In vivo experiments have shown that pumping of protons by PR can lead to increases in growth rate under nutrient-limited conditions (6,14,15), production of ATP (16), increased fixation of CO 2 (6,17), and/or survival under starvation or stress conditions (16,(18)(19)(20).…”

Section: Introductionmentioning

confidence: 99%

Expression of holo-proteorhodopsin in Synechocystis sp. PCC 6803

Chen

Steen

Dekker

et al. 2016

Metabolic Engineering

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Retinal-based photosynthesis may contribute to the free energy conversion needed for growth of an organism carrying out oxygenic photosynthesis, like a cyanobacterium. After optimization, this may even enhance the overall efficiency of phototrophic growth of such organisms in sustainability applications. As a first step towards this, we here report on functional expression of the archetype proteorhodopsin in Synechocystis sp. PCC 6803. Upon use of the moderate-strength psbA2 promoter, holo-proteorhodopsin is expressed in this cyanobacterium, at a level of up to 10 5 molecules per cell, presumably in a hexameric quaternary structure, and with approximately equal distribution (on a protein-content basis) over the thylakoid and the cytoplasmic membrane fraction. These results also demonstrate that Synechocystis sp. PCC 6803 has the capacity to synthesize alltrans-retinal. Expressing a substantial amount of a heterologous opsin membrane protein causes a substantial growth retardation Synechocystis, as is clear from a strain expressing PROPS, a nonpumping mutant derivative of proteorhodopsin. Relative to this latter strain, proteorhodopsin expression, however, measurably stimulates its growth.

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Microbial rhodopsins on leaf surfaces of terrestrial plants

Cited by 88 publications

References 37 publications

Metagenomic Signatures of Bacterial Adaptation to Life in the Phyllosphere of a Salt-Secreting Desert Tree

Metagenomic Signatures of Bacterial Adaptation to Life in the Phyllosphere of a Salt-Secreting Desert Tree

The foliar spray of Rhodopseudomonas palustris grown under Stevia residue extract promotes plant growth via changing soil microbial community

Expression of holo-proteorhodopsin in Synechocystis sp. PCC 6803

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