26 April 2021

Contrasting patterns of microbial dominance in the Arabidopsis thaliana phyllosphere
Citation: Lundberg, D. S., de Pedro Jové, R. Pramoj Na Ayutthaya, P., Karasov, T.L., Shalev, O., Poersch, K., Ding, W., Bollmann-Giolai, A., Bezrukov, I., and Weigel, D..  Contrasting Patterns of Microbial Dominance in the Arabidopsis Thaliana Phyllosphere. BioRxiv https://doi.org/10.1101/2021.04.06.438366.
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by Tatsuya Noborti

Aboveground organs of plants, or the phyllosphere, represent open and fluctuating habitats for microbes originating from various sources, such as soil, seeds, and from neighboring plants transferred via air, rain, insects, or other means. To date, the strain-level understanding of phyllosphere microbiome membership is limited, and best studied in the genus Pseudomonas. To better understand the ecology and host specificity in the phyllosphere microbiome, Lundberg et al. turned to another abundant yet less understood genus, Sphingomonas. The authors employed genomic techniques to analyze leaves of wild Arabidopsis thaliana and neighboring other plant species in spring, when A. thaliana plants were flourishing, and late summer, when there was no living A. thaliana. Amplicon sequencing of 16S rRNA genes revealed that both Sphingomonas and Pseudomonas dominated the leaf microbiome and were common endophytically, but Sphingomonas colonized more consistently in different seasons and had a broader host range than Pseudomonas. The authors established a genome-sequenced culture collection of endophytic Sphingomonas, which allowed for in-depth genome analyses at the strain level. The analysis revealed that Sphingomonas genomes are more diverse than Pseudomonas, and 16S rRNA information falls short in comprehending the diversity of plant-associated Sphingomonas. The authors also devised a cost-efficient metagenome approach in which Sphingomonas or Pseudomonas were enriched using cultivation on selective media before sequencing. The metagenome data showed that the most abundant strains of Sphingomonas and Pseudomonas in plants were not well represented in the soil, whereas some strains were shared between different plant species and, in some cases, between different seasons. These results suggest that leaf-to-leaf transmission may be a major source of these strains to the next generation. Overall, this study demonstrates the importance of strain-level analyses of the plant microbiome, and reveals shared and contrasting modes of interactions between leaves and dominant bacterial species in the phyllosphere.

About the first author: Derek S. Lundberg received his PhD in 2014 at the University of North Carolina at Chapel Hill, USA. There, in the lab of Jeff Dangl, he studied the Arabidopsis thaliana root microbiome. Since then, he has been a postdoc in the group of Detlef Weigel at the Max Planck Institute for Developmental Biology in Tübingen, Germany, studying leaf microbiomes. In the future, he is planning to focus on the interaction between plants and the bacterial genus Sphingomonas.  

22 April 2021

Experimental evidence of microbial inheritance in plants and transmission routes from seed to phyllosphere and root

Citation: Abdelfattah, A., Wisniewski, M., Schena, L., Tack, A.J.M.(2021). Experimental evidence of microbial inheritance in plants and transmission routes from seed to phyllosphere and root. Environmental Microbiology. doi.org/10.1111/1462-2920.15392.
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by Leticia Bianca Pereira

Soil is widely considered as the origin and main source of microorganisms associated with plants. However, the potential contribution of seeds to the assembly of the plant microbiome cannot be ignored. Seed microbiota remained relatively unknown, and were much less studied compared to well characterized plant compartments such as rhizosphere and phyllosphere.

Studies that demonstrate the microbiome's vertical inheritance (from seed to seedling) under natural conditions are challenging once plants are exposed to the soil with its high microbial diversity. To overcome this problem, Abdelfattah and colleagues developed a microcosm to grow common oak seedlings in microbe-free conditions while keeping the below- and aboveground plant parts separated. Using an amplicon-based approach of the ITS and 16S regions to characterize the fungal and bacterial community present in the embryo and pericarp of acorns, roots and phyllosphere of the developing seedling, the author were able to identify the transient and vertically transmitted microbiota from the seeds.

The authors found that the composition of the microbial community in embryo and pericarp greatly differed and the major part of the inherited microbiome is transmitted from the seed to the seedling. This emphasizes the ecological role of seeds as a reservoir and source for community assembly in new seedlings. Interestingly, the phyllosphere microbiota was derived mainly from the embryo microbiome, while the root microbiome represented a distinct subset of the seed microbiome. The authors also discuss the lack of information about the microbial community from embryo, since several unidentified fungal and bacterial taxa were found. Since the authors demonstrated that this seed environment is a crucial part of the vertical inheritance process, the importance of discovering of novel species that occupy this niche becomes apparent.

In summary, this study provides new information on the source and transmission of plant-associated microbes. This knowledge could increase our understanding of plant biology, and help in future biotechnological applications such as new strategies for breeding healthier crops.

About the first author : Ahmed Abdelfattah is a researcher at Institute of Environmental Biotechnology, Graz University of Technology, Austria. His research mainly focuses on microbial communities associated to plants, especially agricultural crops, including olive, citrus, strawberries, grape, wheat, and of course apples.He previously worked at Stockholm University, Sweden as postdoc to study the microbial community of oak trees with a special focus on their spatial distribution within the tree and the mechanisms of their inheritance.

14 April 2021

A complex immune response to flagellin epitope variation in commensal communities

Citation: Colaianni, N.R., Parys, K., Lee, H.-S., Conway, J.M., Kim, N.H., Edelbacher, N., Mucyn, T.S., Madalinski, M., Law, T.F., Jones, C.D., et al., 2021. A complex immune response to flagellin epitope variation in commensal communities. Cell Host Microbe. doi: 10.1016/j.chom.2021.02.006.
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by Giannis Stringlis

In nature, plants interact with many different microbes (pathogenic, beneficial or commensal). All these microbes produce similar conserved molecules known as microbe-associated molecular patterns (MAMPs). Perception of MAMPs by specialized plant receptors, known as pattern recognition receptors or PRRs, can lead to MAMP-triggered immunity (MTI). MTI is a first layer of defense employed by plants to restrict microbial colonization and pathogenesis. One well-characterized MAMP-PRR pair is that of bacterial flagellin and FLAGELLIN SENSING 2 (FLS2). Flagellin is the building block of bacterial flagellum, required for bacterial motility, and contains flg22, a 22-amino-acid peptide known for its immune-eliciting potential. Despite the fact that different bacteria are motile due to flagellin and possess flg22 peptides, most plant niches are colonized by millions of bacteria. Therefore, a delicate interplay occurs between flg22 of plant-associated bacteria and the plant immune system.

Researchers from Dangl and Belkhadir groups aimed to characterize the flg22 repertoire of Arabidopsis commensal bacteria and their ability to induce MTI and inhibit plant growth. Genome mining in more than 600 bacterial isolates revealed their categorization in three clades, based on diversity of flagellum proteins and flg22 sequence similarity. Synthesis of 97 flg22 peptide variants (representative of the three clades) and subsequent screening for MTI, revealed that some are immunogenic (mostly from Clade I bacteria; β-/γ-Proteobacteria) while most of the peptides (mostly from Clade III bacteria; Rhizobiales, Caulobacterales) avoid to induce MTI or cause growth inhibition via different modes of action. Based on their modes of action flg22 peptides were categorized as evading (avoid MTI activation), deviant (different levels of MTI) and antagonistic (antagonizing MTI activation by immunogenic peptides). Further analysis revealed that prevalent members of rhizosphere and phyllosphere bacterial communities produce antagonistic and evading flg22 peptides, achieving as such low MTI activation and successful colonization.

Analysis of a complex synthetic microbial community colonizing roots and leaves of Arabidopsis in vitro, revealed that evading flg22 peptides are enriched in both root- and shoot-associated microbes, while the immunogenic ones are depleted. However, under conditions of salt stress, leading to a weakened plant immune system, there is enrichment of immunogenic flg22 variants in Arabidopsis-associated microbes. This finding suggests that optimal function of the immune system is required to monitor bacterial presence based on flg22 immunogenicity.

This study demonstrates that complex plant-associated bacterial communities produce a cocktail of flg22 peptides to avoid strong MTI activation and represents an important step towards understanding why some microbes are successful plant colonizers while others are not.

About the co-authors : Nicholas R. Colaianni is a PhD student in the Dangl Lab at the University of North Carolina Chapel Hill, USA.

Katarzyna Parys is a collaborator at the Gregor Mendel Institute of Molecular Plant Biology GmbH, in Vienna, Austria.


26 March 2021

Temperature transcends partner specificity in the symbiosis establishment of a cnidarian
Citation: Herrera, M., Klein, S.G., Campana, S. et al. Temperature transcends partner specificity in the symbiosis establishment of a cnidarian. ISME J 15, 141–153 (2021). doi.org/10.1038/s41396-020-00768-y.
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by Mohammad Alnajjar

Corals live in a delicate symbiotic relationship with dinoflagellate algae in the family Symbiodiniaceae. This relationship, however, is fragile and can break down in response to environmental stressors such as increased temperature, a process known as coral bleaching. As warming sea surface temperatures, consequence of climate change, become more frequent and severe, coral reef ecosystems continue to decline worldwide. Yet, contrary to increasing research efforts on coral bleaching, little is known about the establishment and development of novel symbioses in rapidly warming environments. Certainly, symbiotic flexibility is an important factor when predicting how corals might respond to increasing temperatures. Unlike other studies, Herrera et al. (From the Red Sea Research Center in KAUST/Saudi Arabia) tested different combinations of host genotypes and their native symbionts, thus taking into account genotypic variability among hosts but also the potential constraints of symbiosis and functional diversity (e.g., thermal sensitivity) within Symbiodiniaceae.

The authors used the flexible model system Exaiptasia pallida to investigate how host specificity and temperature affect the symbiosis establishment of a cnidarian. They inoculated symbiont-free anemones originating from three geographically distinct locations (Hawaii, North Carolina, and the Red Sea) using a mixture of native symbiont strains (Breviolum minutum, Symbiodinium linucheae, S. microadriaticum, and a Breviolum ecotype from the Red Sea) at ‘optimal’ and elevated temperatures and performed deep ITS2 sequencing to assess colonization dynamics across the different thermal conditions. Furthermore, they measured PSII photochemical efficiency (Fv/Fm) as a proxy of the physiological performance of symbioses over time which highlights the importance of heterotrophic feeding on the response to temperature.

This study highlights the role of temperature and partner fidelity in the establishment and performance of symbiosis and further adds to the body of work showing that pre-exposure to elevated temperature is crucial for the thermal resilience of the cnidarian holobiont. Moreover, it shows the potential of using species from the Red Sea to study thermal resilience of the cnidarian holobiont. Finally, the authors also demonstrate the importance of active feeding for enduring thermal stress.

About the first author and the group: Marcela Herrera received her PhD in Marine Science from King Abdullah University of Science and Technology (KAUST), Saudi Arabia, in June 2020. At KAUST, she worked with Professor Manuel Aranda investigating the responses of symbiotic cnidarians to environmental change. The lab focuses on understanding the mechanisms underpinning cnidarian-dinoflagellate symbiosis using a broad range of tools (genomics, bioinformatics, ecology, microbiology). Recently, Marcela started a postdoc at the Marine Eco-Evo-Devo group in the Okinawa Institute of Science and Technology (OIST), Japan, working on genomics of local adaptation of reef fish.

7 March 2021

Versatile cyanobacteria control the timing and extent of sulfide production in a Proterozoic analog microbial mat
Citation: Klatt, J. M., Gomez-Saez, G. V., Meyer, S., Ristova, P. P., Yilmaz, P., Granitsiotis, M. S., et al. (2020). Versatile cyanobacteria control the timing and extent of sulfide production in a Proterozoic analog microbial mat. The ISME Journal. doi:10.1038/s41396-020-0734-z.
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by Mohammad Alnajjar

Cyanobacterial mats were hotspots of biogeochemical cycling throughout the Proterozoic.
Contemporary cyanobacterial mats in sulfidic springs allow us to look back in time and learn about biogeochemical cycling of the past. In a contemporary cyanobacterial mat thriving in a sulfidic spring (i.e., analogue to Proterozoic) anoxygenic photosynthesis by cyanobacteria is enhancing the diel oxygen budget. This counterintuitive effect emerges because versatile cyanobacteria disrupt positive feedbacks in the classical view of the sulfur cycle. This disruption is only apparent when considering the gradual response of microbial process interactions to diel light dynamics and benthic transport phenomena. These interesting interactions were investigated by a group of scientists from Max-Planck Institute for Marine Microbiology and their colleagues from universities and research institutions in Europe and the USA, by using a broad biogeochemical and molecular toolbox. The authors found that the dissolved organic carbon (DOC) released by oxygenic photosynthesis fuels sulfide production, likely by a specialized SRB population. Increased sulfide fluxes were only stimulated after the cyanobacteria switched from anoxygenic to oxygenic photosynthesis. O2 production triggered migration of large sulfur-oxidizing bacteria from the surface to underneath the cyanobacterial layer. The resultant sulfide shield tempered anoxygenic photosynthesis and allowed the oxygenic photosynthesis to occur for a longer duration over a diel cycle. The lack of cyanobacterial DOC supply to SRB during anoxygenic photosynthesis therefore maximized O2 export. This study highlights the importance of metabolic transitions in response to dynamic environmental parameters, and of resultant interactions between processes, for ecosystem function.

About the first author: Judith Klatt is an enthusiastic young scientist, who is full of energy and bright ideas, and at the same time, a great mother. She did her PhD in the microsensor group at the Max-Planck Institute for Marine Microbiology (MPI-MM) in 2015. Then she spent 2-years as postdoc at Geomicrobiology Lab, Earth and Environmental Sciences, University of Michigan. After that, she moved back to MPI-MM to continue her journey working on sulfidic microbial mats.

7 March 2021

Diatom modulation of select bacteria through use of two unique secondary metabolites
Citation: Shibl A.A., Isaac A., Ochsenkühn M.A., Cárdenas A., Fei C., Behringer G., Arnoux M., Drou N., Santos M.P., Gunsalus K.C., Voolstra C.R., Amin S.A.. Diatom modulation of select bacteria through use of two unique secondary metabolites. Proc Natl Acad Sci U S A. 2020 Nov 3;117(44):27445-27455.
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by Mohammad Alnajjar

Multicellular eukaryotes have dedicated structures to house microbiomes, whereas the mechanisms that enable diatoms and other phytoplankton species to actively modulate incoming microbes are mostly unknown. The marine microbial ecology laboratory team at the New York University in Abu-Dhabi and their colleagues from the MPI in Bremen, as well as scientists from KAUST and the University of Konstanz explored the ability of a widespread diatom, Asterionellopsis glacialis, to adopt specific mechanisms to promote association with potentially beneficial symbionts while repelling opportunists. They employed an integrated multi-omics approach (genomics, transcriptomics, metabolomics) to tease apart the functional and metabolic capacities of a bacterial consortium and a phytoplankton within a host-microbiome system. In addition, they targeted two bacterial genera, Roseobacteria and Alteromonas, to test the effects of two enigmatic secondary metabolites, azelaic acid and rosmarinic acid, on the growth and behavior of associated bacteria within the diatom photosphere. Their results suggest that a host phytoplankton cell goes through major transcriptional and metabolic reprogramming in order to modulate its microbiome through secondary metabolites. Therefore, the innate ability of an important unicellular eukaryotic group to modulate select bacteria in their microbial consortia is similar to higher eukaryotes, using unique secondary metabolites that regulate bacterial growth and behavior inversely across different bacterial populations.

About the first author: Ahmed Shibl received his PhD in Marine Science from King Abdullah University of Science and Technology (KAUST) in December 2015. At KAUST, he participated in several research expeditions to the Red Sea and Mediterranean Sea. After his doctoral studies, he spent a few months as a Postdoc in Xelu Moran’s lab (KAUST). After that, he went on a short-term visit as a Researcher in the Antunes Lab at Edge Hill University in the UK. In late 2017, he joined the Shady Amin Lab at New York University Abu Dhabi to study the diatom core microbiome and phytoplankton-bacteria interactions

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