Microbial “gardening” by a seaweed holobiont: Surface metabolites attract protective and deter pathogenic epibacterial settlement

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.

Salinity and Time Can Alter Epibacterial Communities of an Invasive Seaweed

“…Seaweed metabolites are known to affect bacterial attachment and growth (reviewed by Saha et al, 2017). Also, it has been demonstrated that seaweed surface metabolites can influence the overall epibacterial community composition when compared to non-living substrata (Lachnit et al, 2010) and can selectively attract beneficial and repel pathogenic bacteria (Saha and Weinberger, 2019). Thus, only microorganisms which can adapt to the specific surface chemistry conditions on a host surface might be able to settle on it, fitting the 'niche' model (Dumbrell et al, 2010).…”

“…To cope with seasonally fluctuating colonizing pressure, macrophytes including seaweeds in turn have been reported to seasonally up or downregulate the production of antifouling defense (Saha and Wahl, 2013;Wang et al, 2017;Guan et al, 2019) influencing seaweed-bacteria interaction and also interaction with other foulers. We have recently demonstrated that the surface chemistry of Agarophyton is capable of selectively recruiting bacterial colonizers (Saha and Weinberger, 2019) and from previous studies we are aware that the antifouling defense of seaweeds including Agarophyton undergoes seasonal fluctuations indicating a change in the surface chemistry of the alga over time (Saha and Wahl, 2013;Wang et al, 2018). Although in this current study we have not investigated the surface metabolome of Agarophyton at different timepoints, i.e., T0, T1, and T2, we may speculate that a seasonal fluctuation in the surface chemistry of the algae may have resulted in the selective recruitment of the bacterial colonizers on the surface of the alga and thereby different community composition at different timepoints.…”

“…Seaweeds are host to a diverse array of bacteria colonizing their surfaces -together forming a single entity called the seaweed holobiont (Egan et al, 2013). Some of these bacteria are essential for the health and normal morphological development of the seaweed host (Wichard et al, 2015;Saha and Weinberger, 2019), consumption of organic matter and nitrogen source (De Oliveira et al, 2012) and provide associational chemical defense against micro and macro colonizers (reviewed by Dahms and Dobretsov, 2017;Saha et al, 2017;Saha and Weinberger, 2019). Given this crucial ecological role of epibiotic bacteria, it is important to know how composition and richness of these epibacteria is controlled by the host and environmental factors.…”

A community perspective on the concept of marine holobionts: current status, challenges, and future directions

“…Microbial gardening -the act of frequently releasing growth-enhancing or inhibiting chemicals or metabolites that favor the development of a microbial community beneficial to the host (see e.g. Saha and Weinberger 2019). Microbiome -the combined genetic information encoded by the microbiota; may also refer to the microbiota itself or the microbiota and its environment (see Marchesi and Ravel 2015).…”

Genomic, metabolic and phenotypic variability shapes ecological differentiation and intraspecies interactions of Alteromonas macleodii

“…Alternatively, colonization might occur in a neutral manner, comparable to other Alteromonas spp. with a similar CAZyme profile 80 . Considering nucleotide substitution rates of ca.…”