Microbial “gardening” by a seaweed holobiont: Surface metabolites attract protective and deter pathogenic epibacterial settlement
2019/05/10 by Mahasweta Saha, Florian Weinberger · 28 citations
Earth and Planetary Sciences · Environmental Science · #Marine and coastal plant biology #Coastal wetland ecosystem dynamics #Marine Biology and Ecology Research
paper · pdf · doi:10.1111/1365-2745.13193
Abstract
Abstract Epimicrobial communities on seaweed surfaces usually contain not only potentially pathogenic but also potentially beneficial micro‐organisms. Capacity of terrestrial plants for chemically mediated recruitment, that is, “gardening” of bacterial communities in the rhizosphere was recently demonstrated. Empirical evidence directly linking such chemical “gardening” with the beneficial role of gardened microbes in terrestrial plants is rare and largely missing for aquatic macrophytes. Here, we demonstrate that our model invasive seaweed holobiont Agarophyton vermiculophyllum possesses beneficial microbiota on its surface that provide protection from bacterial pathogens. Metabolites from the algal holobiont’s surface reduced settlement of opportunistic pathogens but attracted protective epibacterial settlement. We tested 58 different bacterial species (isolated from the surface of A. vermiculophyllum ) individually in tip bleaching assays. Kordia algicida was identified as a “significant pathogen” inducing a bleaching disease. In addition, nine other species significantly reduced the risk of algal bleaching and were thus “significantly protective”. Additionally, two “potential pathogens” and 10 “potential protectors” were identified. When 19 significant and potential protectors and 3 significant and potential pathogens were tested together, the protective strains fully prevented bleaching, suggesting that a component of A. vermiculophyllum’s epimicrobiome provides an associational defence against pathogens. Chemically mediated selective recruitment of microbes was demonstrated in bioassays, where A. vermiculophyllum surface metabolites attracted the settlement of protective strains, but reduced settlement of pathogens. Synthesis . The capacity of an aquatic macrophyte to chemically “garden” protective micro‐organisms to the benefit of strengthened disease resistance is demonstrated for the first time. Such a role of surface chemistry in “gardening” of microbes as found in the current study could also be applicable to other host plant—microbe interactions. Our results may open new avenues towards manipulation of the surface microbiome of seaweeds via chemical “gardening,” enhancing sustainable production of healthy seaweeds.
Citations
Cited by
- Cross-Host Protection of Marine Bacteria Against Macroalgal Disease
- Abiotic stress destabilizes the bacterial community of sugar kelp, Saccharina latissima (Phaeophyceae)
- Distribution and Evolutionary Trajectories of β-Lactamases in Vibrio: Genomic Insights from Carbenicillin-Hydrolyzing Class A β-Lactamases (CARB) in the Harveyi and Cholerae Clades
- Genomic, metabolic and phenotypic variability shapes ecological differentiation and intraspecies interactions of Alteromonas macleodii. [europepmc]
- Salinity and Time Can Alter Epibacterial Communities of an Invasive Seaweed. [europepmc]
- Warming, but Not Acidification, Restructures Epibacterial Communities of the Baltic Macroalga Fucus vesiculosus With Seasonal Variability. [europepmc]
- Bacterial Communities Show Algal Host ( Fucus spp.)/Zone Differentiation Across the Stress Gradient of the Intertidal Zone. [europepmc]
- Chemically Mediated Microbial "Gardening" Capacity of a Seaweed Holobiont Is Dynamic. [europepmc]
- The role of host promiscuity in the invasion process of a seaweed holobiont. [europepmc]
- A community perspective on the concept of marine holobionts: current status, challenges, and future directions. [europepmc]
- Microbiota-Macroalgal Relationships at a Hawaiian Intertidal Bench Are Influenced by Macroalgal Phyla and Associated Thallus Complexity. [europepmc]
- Understanding the metabolome and metagenome as extended phenotypes: The next frontier in macroalgae domestication and improvement. [europepmc]
- Impacts of environmental stress on resistance and resilience of algal-associated bacterial communities. [europepmc]
- Bacterial Biofilm Thickness and Fungal Inhibitory Bacterial Richness Both Prevent Establishment of the Amphibian Fungal Pathogen Batrachochytrium dendrobatidis. [europepmc]
- Becoming nose-blind-Climate change impacts on chemical communication. [europepmc]
- Insights into the potential for mutualistic and harmful host-microbe interactions affecting brown alga freshwater acclimation. [europepmc]
- Elevated Temperature-Induced Epimicrobiome Shifts in an Invasive Seaweed Gracilaria vermiculophylla . [europepmc]
- Shifting chemical defence or novel weapons? A review of defence traits in Agarophyton vermiculophyllum and other invasive seaweeds. [europepmc]
- Accessory microbiomes. [europepmc]
- Naturally occurring beneficial bacteria Vibrio alginolyticus X-2 protects seaweed from bleaching disease. [europepmc]
- Current knowledge of the Southern Hemisphere marine microbiome in eukaryotic hosts and the Strait of Magellan surface microbiome project. [europepmc]
- Coral endosymbiont growth is enhanced by metabolic interactions with bacteria. [europepmc]
- Importance of quorum sensing crosstalk in the brown alga Saccharina latissima epimicrobiome. [europepmc]
- Microbiomes of Thalassia testudinum throughout the Atlantic Ocean, Caribbean Sea, and Gulf of Mexico are influenced by site and region while maintaining a core microbiome. [europepmc]
- Epiphytic microbiome associated with intertidal seaweeds in the Mediterranean Sea: comparative analysis of bacterial communities across seaweed phyla. [europepmc]
- Horizontal gene transfer and symbiotic microorganisms regulate the adaptive evolution of intertidal algae, Porphyra sense lato. [europepmc]
- Integrating microbial communities into algal biotechnology: a pathway to enhanced commercialization. [europepmc]
- Abiotic stress destabilizes the bacterial community of sugar kelp, Saccharina latissima (Phaeophyceae). [europepmc]
Related