Editorial: Chemically Mediated Interactions Between Marine Macrophytes and Microbes

Is it well-accepted that communication among organisms including land plants and aquatic macrophytes in terrestrial and aquatic ecosystems is largely achieved using information-conveying chemicals or “infochemicals” (Saha et al., 2019) which should be seen as a chemical “language” of life. Marine macrophytes and phytoplankton are dominant primary producers in marine ecosystems worldwide (e.g., Behrenfeld et al., 2001). They produce oxygen and form the base of food webs, are ecosystem engineers, and provide ecologically and economically valuable functions and services (e.g., Holdt and Kraan, 2011; Sarker et al., 2020; review by Pierella Karlusich et al., 2020). Phytoplankton and macrophytes are not single isolated entities but establish intimate relationships between them as well as with non-photosynthetic microbes (including bacteria, fungi, viruses) forming holobionts. These interactions in turn influence carbon and nutrient cycling, regulate the productivity and dynamics of aquatic food webs, and affect ocean–atmosphere fluxes of climatically relevant gases like dimethylsulphide and greenhouse gases like halocarbons. Associations and interactions between photosynthetic and non-photosynthetic organisms are chemically-mediated and are dependent on “cross-talk” infochemicals as well. However, our knowledge on the chemical “language of life” in aquatic ecosystems is still incipient (when compared to terrestrial environment). We do not know which infochemicals facilitate or inhibit the preferential attachment of macrophytes by microbes senso lato (i.e., including photosynthetic microalgae and cyanobacteria and heterotrophic bacteria), whether the selected macroalgae can stimulate the production of particular phycotoxins, whether microbes produce compounds (and if so, which chemicals) that act as deterrent of macrophytes grazing. Given the important role that the rapidly undergoing climate-driven changes (rising temperature, acidification, hypoxia, desalination) are playing in the aquatic ecosystems, potential modifications on such chemically mediated interactions (Schmidt and Saha, 2020) cannot be discarded. Identifying infochemicals and understanding their role have been challenging mainly by technical limitation. However, the emergence of cutting edge technical advances in the fields of analytical chemistry, cell biology, and the “omics” resources offer nowadays the possibilities to achieve rapid progress into the field of chemically mediated algae-microbe interactions under the present oceans. This Research Topic ensembles seven research articles and one review paper aimed at advancing our knowledge of the chemically mediated macroalgae—microalgae—microbe interactions. A plethora of commercial and environmental applications may rise from a better understanding of the interactions among marine macroalgae (seaweeds) and associated microbes. For example, Burgunter-Delamare et al. conducted an exhaustive characterization of the genomes-sequencing Saha et al. Editorial: Chemically Mediated Marine Macrophyte-Microbe Interactions of 10 bacteria associated to the model brown alga Ecotocarpus siliculosus. Also, the genome-based reconstruction of their metabolic networks was conducted. The potential metabolic activities were then compared with metabolites produced by the macroalga. This allowed to predict which bacteria could facilitate the growth of the macroalgae. From the most promising consortia, some preliminary co-culture experiments were conducted testing the exchange of selected chemicals between alga and bacteria suggesting beneficial metabolites exchanges in the holobiont. Califano et al. investigated to what extent Integrated Multi-trophic Aquaculture (IMTA) influences the microbiome associated with the commercially important green alga Ulva rigida, comparing diversity, and taxonomic composition of wild vs. IMTA-grown algae and surrounding water. Amplicon Sequence Variants (ASVs) revealed that prokaryotic richness was higher in aquaculture water than on wild samples, and in both cases, richness was also higher in water than on Ulva samples. Aquaculture thus promoted the presence of known morphogenesis-inducing bacteria, suggesting that IMTA may shape the microbial community of cultured Ulva, including previously undetected taxa with unknown traits. This knowledge can facilitate the establishment of sustainable and environmentally friendly aquaculture. On the other hand, a better understanding on how marine macroalgae deter undesired epibiotic growth may lead to the development of new, environmentally safer antifouling paints (Da Gama et al., 2014; Saha et al., 2017). Bioassayguided fractionation of glycolipids from the brown seaweed Sargassum vulgare led to the isolation of three sub-fractions that demonstrated promising antifouling activity toward marine bacteria and microalgae (Plouguerné et al.). The main compounds in these fractions are monogalactosyldiacylglycerols (MGDG), digalactosyldiacylglycerols (DGDG), and sulfoquinovosyldiacylglycerols (SQDG). These compounds appear to mediate microbial colonization of this macrophyte. Following this line, Ternon et al. characterized the surface metabolome and explored the bioactivity of surface extracts of four macroalgae, Dictyota dichotoma, Dictyota spiralis, Taonia atomaria, and Padina pavonica, that are common substrates of microalgae, including the toxic dinoflagellate Ostreopsis cf. ovata. Laboratory experiments combined with the analysis of the eukaryotic diversity (using 18S rRNA gene metabarcoding) of the organisms attached to the macroalgae in situ indicated that D. dichotoma could be the most bioactive macroalga, causing negative physiological responses on O. cf. ovata. However, the proliferation of O. cf. ovata depends on complex and multiple ecological factors. In fact, the blooms of this microalga may constitute a paradigm of the chemical ecology, due to the wide diversity of chemically driven responses exhibited by other microand macroorganisms exposed to Ostreopsis proliferations, as comprehensively reviewed by Pavaux et al. Ostreopsis produces toxins and attaches to the substrates (macroalgae, rocks, sand) by secreted mucopolysaccharides. These biomolecules may be involved in allelopathy and competitive interactions with the microbiota and predators’ deterrence leading to Ostreopsis blooms and also involved in the negative impacts on human health and certain benthic macrofauna. However, innovative tools and realistic experiments are needed to understand the dynamics and ecotoxicity of the Ostreopsis blooms and other benthic toxic dinoflagellates. With this objective, Tarazona-Janampa et al. using molecular and chemical tools characterized a wide range of bacterial assemblages associated to Prorocentrum lima species complex. In this case, the complex experiments conducted did not provide evidence that allelopathic interactions among the toxic microalgae and bacteria could play a definable role in the growth and toxin production by P. lima species complex. The results suggest that other internal physiological processes or environmental factors can modulate the toxicity of this microalgal blooms. Awiderangeofmicrobes,frombacteriatofungi,alsocolonize the internal tissues of macroalgae. However, chemically mediated interactions of macroalgae with these endosymbiotic microbes remain poorly explored to date and were addressed by Vallet et al. Novel α-hydroxy-γ-butenolides isolated from the obligate marine fungus Paradendryphiella salina were found to interfere with bacterial quorum sensing. Comparative metabolomics revealed the presence of α-hydroxy- γ -butenolides among all the P. salina strains isolated from different hosts. Also, a high metabolic variability related to the alga-host species was found, highlighting the key role of microbial chemical communication that may occur within the tissue of the macroalgal holobiont. Along with marine macro- and microalgae, seagrasses are also known to engage in chemically mediated interactions with surface associated microbes (Guan et al., 2017). Such defense can be dynamic in nature and has been recently shown to fluctuate at a seasonal scale (Guan et al., 2019). However, how such defense and the responsible infochemicals may respond to climate change induced stressors like marine heatwaves is not known yet. To answer this, Guan et al. demonstrate how climate change imposed stressors like marine heatwaves may alter the infochemicals produced by the seagrass Zostera marina in the Western Baltic. In a mesocosm study where the authors simulated near natural heatwaves, the capacity to deter microbial colonizers was to be significantly up-regulated in Z. marina from heatwave treatments (with one or three heatwaves)incomparisontoZ.marinaundercontrolconditions, suggesting defense regulation of Z. marina in response to marine heatwaves

Antifouling activity of twelve demosponges from Brazil

Benthic marine organisms are constantly exposed to fouling, which is harmful to most host species. Thus, the production of secondary metabolites containing antifouling properties is an important ecological advantage for sessile organisms and may also provide leading compounds for the development of antifouling paints. High antifouling potential of sponges has been demonstrated in the Indian and Pacific oceans and in the Caribbean and Mediterranean seas. Brazilian sponges remain understudied concerning antifouling activities. Only two scientific articles reported this activity in sponges of Brazil. The objective of this study was to test crude extracts of twelve species of sponges from Brazil against the attachment of the mussel Perna perna through laboratorial assays, and highlight promising species for future studies. The species Petromica citrina, Amphimedon viridis, Desmapsamma anchorata, Chondrosia sp., Polymastia janeirensis, Tedania ignis, Aplysina fulva, Mycale angulosa, Hymeniacidon heliophila, Dysidea etheria, Tethya rubra, and Tethya maza were frozen and freeze-dried before extraction with acetone or dichloromethane. The crude extract of four species significantly inhibited the attachment of byssus: Tethya rubra (p = 0.0009), Tethya maza (p = 0.0039), Petromica citrina (p = 0.0277), and Hymeniacidon heliophila (p = 0.00003). These species, specially, should be the target of future studies to detail the substances involved in the ability antifouling well as to define its amplitude of action

Antifouling activity of twelve demosponges from Brazil

Benthic marine organisms are constantly exposed to fouling, which is harmful to most host species. Thus, the production of secondary metabolites containing antifouling properties is an important ecological advantage for sessile organisms and may also provide leading compounds for the development of antifouling paints. High antifouling potential of sponges has been demonstrated in the Indian and Pacific oceans and in the Caribbean and Mediterranean seas. Brazilian sponges remain understudied concerning antifouling activities. Only two scientific articles reported this activity in sponges of Brazil. The objective of this study was to test crude extracts of twelve species of sponges from Brazil against the attachment of the mussel Perna perna through laboratorial assays, and highlight promising species for future studies. The species Petromica citrina, Amphimedon viridis, Desmapsamma anchorata, Chondrosia sp., Polymastia janeirensis, Tedania ignis, Aplysina fulva, Mycale angulosa, Hymeniacidon heliophila, Dysidea etheria, Tethya rubra, and Tethya maza were frozen and freeze-dried before extraction with acetone or dichloromethane. The crude extract of four species significantly inhibited the attachment of byssus: Tethya rubra (p = 0.0009), Tethya maza (p = 0.0039), Petromica citrina (p = 0.0277), and Hymeniacidon heliophila (p = 0.00003). These species, specially, should be the target of future studies to detail the substances involved in the ability antifouling well as to define its amplitude of action

Large-scale purification of pachydictyol A from the brown alga Dictyota dichotoma obtained from algal wash and evaluation of its antifouling activity against the freshwater mollusk Limnoperna fortunei

A scalable procedure was developed for the extraction and purification of pachydictyol A, the main diterpenoid isolated from the brown alga Dictyota dichotoma. The organic extract of this species is a complex mixture of a large variety of diterpenes, and in this work, the protocol was employed successfully for the purification of gram quantities of this compound from Patagonian D. dichotoma collected from algal wash. Pachydictyol A, together with other minor diterpenoids, was tested for antifouling activity against the invading freshwater mussel Limnoperna fortunei, using a byssal thread formation assay. The results obtained in the study showed a potent antifouling activity for pachydictyol A at 4.7 μg cm−2 disk load. As for the other diterpenoids, dictyoxide was also considerably active, while dictyol C and dictyotadiol had a considerably lower activity. Taking into account the large biomass of algal wash and the abundance of D. dichotoma, together with the effectiveness of the purification protocol, these results show that pachydictyol A and dictyoxide have a good chance to become natural, non-toxic, and ecologically friendly additives in antifouling paints for the protection of submersed structures against L. fortunei.Fil: Siless, Gastón Ezequiel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Unidad de Microanálisis y Métodos Físicos en Química Orgánica. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Unidad de Microanálisis y Métodos Físicos en Química Orgánica; ArgentinaFil: Garcia, Monica Teresita. Provincia de Buenos Aires. Gobernación. Comisión de Investigaciones Científicas. Centro de Investigaciones en Tecnología de Pinturas. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Centro de Investigaciones en Tecnología de Pinturas; ArgentinaFil: Perez, Miriam Cristina. Provincia de Buenos Aires. Gobernación. Comisión de Investigaciones Científicas. Centro de Investigaciones en Tecnología de Pinturas. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Centro de Investigaciones en Tecnología de Pinturas; ArgentinaFil: Blustein, Guillermo. Provincia de Buenos Aires. Gobernación. Comisión de Investigaciones Científicas. Centro de Investigaciones en Tecnología de Pinturas. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Centro de Investigaciones en Tecnología de Pinturas; ArgentinaFil: Palermo, Jorge Alejandro. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Unidad de Microanálisis y Métodos Físicos en Química Orgánica. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Unidad de Microanálisis y Métodos Físicos en Química Orgánica; Argentin