The sugar kelp Saccharina latissima II: Recent advances in farming and application

The sugar kelp Saccharina latissima has received intense scientific attention over the last decades. In recent years, interest in cultivation of the species has strongly increased in the North Atlantic Ocean and the Eastern Pacific Ocean, driven by the great potential of S. latissima to be utilised for various industrial applications, including food, feed, and biomaterials. Accordingly, current research has focused on improving farming methods and technology, environmental impacts, and site selection. In addition, many studies have investigated the varying chemical composition of S. latissima, extraction of commercially interesting components, and the use of the biomass and its derived components in various applications. This review provides a comprehensive overview of farming and applications of S. latissima from the last 15 years. Additional insights on other research topics, such as ecology, physiology, biochemical and molecular biology of S. latissima, are given in the first review, “The sugar kelp Saccharina latissima I: recent advances in a changing climate” (Diehl et al. 2023).publishedVersio

The Saccharina latissima microbiome: Effects of region, season, and physiology

IntroductionSaccharina latissima is a canopy-forming species of brown algae and, as such, is considered an ecosystem engineer. Several populations of this alga are exploited worldwide, and a decrease in the abundance of S. latissima at its southern distributional range limits has been observed. Despite its economic and ecological interest, only a few data are available on the composition of microbiota associated with S. latissima and its role in algal physiologyn.MethodsWe studied the whole bacterial community composition associated with S. latissima samples from three locations (Brittany, Helgoland, and Skagerrak) by 16S metabarcoding analyses at different scales: algal blade part, regions, season (at one site), and algal physiologic state.Results and DiscussionWe have shown that the difference in bacterial composition is driven by factors of decreasing importance: (i) the algal tissues (apex/meristem), (ii) the geographical area, (iii) the seasons (at the Roscoff site), and (iv) the algal host’s condition (healthy vs. symptoms). Overall, Alphaproteobacteria, Gammaproteobacteria, and Bacteroidia dominated the general bacterial communities. Almost all individuals hosted bacteria of the genus Granulosicoccus, accounting for 12% of the total sequences, and eight additional core genera were identified. Our results also highlight a microbial signature characteristic for algae in poor health independent of the disease symptoms. Thus, our study provides a comprehensive overview of the S. latissima microbiome, forming a basis for understanding holobiont functioning

Studies of host-microbiota interactions in the brown alga Saccharina latissima

Saccharina latissima est une des espèces de macroalgues brunes dites ingénieures qui participent à la formation des forêts de laminaires. Plusieurs populations naturelles sont exploitées autour du monde et elle fait également l'objet de développements croissants en aquaculture. Le but de ma thèse est de caractériser le microbiote bactérien et d’étudier les interactions hôte-microbiote au sein de l’holobionte S. latissima, pour comprendre dans quelles mesures la composition du microbiote influence la croissance de l’algue. L’étude du microbiote de S. latissima issues de populations naturelles de Roscoff (France), Helgoland (Allemagne) et Norvège sud (Skagerrak) par métabarcoding 16S a montré une différence de composition en fonction de la zone de la lame, de la zone géographique et de l’état physiologique de l’algue. Des isolements bactériens ont été fait pour avoir accès à la part cultivable du microbiote. La combinaison de ces résultats avec les données de métabarcoding a permis de sélectionner des souches bactériennes d’intérêt. Des cocultures algues-bactéries ont montré leur impact sur la croissance algale et des résultats inattendus ont mené à prendre en compte d’autres paramètres : l’état général de la plantule de départ, la composition de son microbiote initial et le phénomène de quorum sensing (QS). Les résultats montrent une corrélation entre l’augmentation du QS et une baisse de la croissance. Ensemble, ces résultats apportent de nouvelles données sur la composition du microbiote de S. latissima, de son impact sur l’hôte, et participent à la meilleure compréhension de l’holobionte algue, venant à l’appui de l’idée d’interdépendance entre l’hôte et son microbiote.Saccharina latissima is a kelp-forming species of brown algae and, as such, is considered a so-called ecosystem engineer. Several populations of this alga are exploited around the world. S. latissima is also currently undergoing increasing development in aquaculture. My PhD thesis aims to characterise the bacterial microbiota and study host-microbiota interactions within the S. latissima holobiont to understand how the microbiota composition influences algal growth. 16S metabarcoding analyses were used to study the microbiota of S. latissima natural populations from Roscoff (France), Helgoland (Germany) and Southern Norway (Skagerrak). They showed a difference in composition depending on the area of the blade, the geographical area and the algal physiological state. Bacterial isolates were used to gain access to the cultivable portion of the microbiota. Combining these results with the 16S metabarcoding data allowed us to select bacterial strains of interest. Algal-bacterial cocultures have shown their impact on algal growth, and unexpected results led us to consider other parameters: the general state of the starting seedling, the composition of its initial microbiota and the phenomenon of quorum sensing (QS). The results show a correlation between an increase of QS molecules and a decrease in algal growth. Together, these results on S. latissima microbiota’s composition help decipher its impact on the algal host and, more generally, contribute to a better understanding of the algal holobiont, supporting the idea of interdependence between the host and its microbiota

Etudes des interactions hôte-microbiote chez l’algue brune Saccharina latissima

Saccharina latissima is a kelp-forming species of brown algae and, as such, is considered a so-called ecosystem engineer. Several populations of this alga are exploited around the world. S. latissima is also currently undergoing increasing development in aquaculture. My PhD thesis aims to characterise the bacterial microbiota and study host-microbiota interactions within the S. latissima holobiont to understand how the microbiota composition influences algal growth. 16S metabarcoding analyses were used to study the microbiota of S. latissima natural populations from Roscoff (France), Helgoland (Germany) and Southern Norway (Skagerrak). They showed a difference in composition depending on the area of the blade, the geographical area and the algal physiological state. Bacterial isolates were used to gain access to the cultivable portion of the microbiota. Combining these results with the 16S metabarcoding data allowed us to select bacterial strains of interest. Algal-bacterial cocultures have shown their impact on algal growth, and unexpected results led us to consider other parameters: the general state of the starting seedling, the composition of its initial microbiota and the phenomenon of quorum sensing (QS). The results show a correlation between an increase of QS molecules and a decrease in algal growth. Together, these results on S. latissima microbiota’s composition help decipher its impact on the algal host and, more generally, contribute to a better understanding of the algal holobiont, supporting the idea of interdependence between the host and its microbiota.Saccharina latissima est une des espèces de macroalgues brunes dites ingénieures qui participent à la formation des forêts de laminaires. Plusieurs populations naturelles sont exploitées autour du monde et elle fait également l'objet de développements croissants en aquaculture. Le but de ma thèse est de caractériser le microbiote bactérien et d’étudier les interactions hôte-microbiote au sein de l’holobionte S. latissima, pour comprendre dans quelles mesures la composition du microbiote influence la croissance de l’algue. L’étude du microbiote de S. latissima issues de populations naturelles de Roscoff (France), Helgoland (Allemagne) et Norvège sud (Skagerrak) par métabarcoding 16S a montré une différence de composition en fonction de la zone de la lame, de la zone géographique et de l’état physiologique de l’algue. Des isolements bactériens ont été fait pour avoir accès à la part cultivable du microbiote. La combinaison de ces résultats avec les données de métabarcoding a permis de sélectionner des souches bactériennes d’intérêt. Des cocultures algues-bactéries ont montré leur impact sur la croissance algale et des résultats inattendus ont mené à prendre en compte d’autres paramètres : l’état général de la plantule de départ, la composition de son microbiote initial et le phénomène de quorum sensing (QS). Les résultats montrent une corrélation entre l’augmentation du QS et une baisse de la croissance. Ensemble, ces résultats apportent de nouvelles données sur la composition du microbiote de S. latissima, de son impact sur l’hôte, et participent à la meilleure compréhension de l’holobionte algue, venant à l’appui de l’idée d’interdépendance entre l’hôte et son microbiote

Études des interactions hôte-microbiote chez l’algue brune Saccharina latissima

Saccharina latissima is a kelp-forming species of brown algae and, as such, is considered a so-called ecosystem engineer. Several populations of this alga are exploited around the world. S. latissima is also currently undergoing increasing development in aquaculture. My PhD thesis aims to characterise the bacterial microbiota and study host-microbiota interactions within the S. latissima holobiont to understand how the microbiota composition influences algal growth. 16S metabarcoding analyses were used to study the microbiota of S. latissima natural populations from Roscoff (France), Helgoland (Germany) and Southern Norway (Skagerrak). They showed a difference in composition depending on the area of the blade, the geographical area and the algal physiological state. Bacterial isolates were used to gain access to the cultivable portion of the microbiota. Combining these results with the 16S metabarcoding data allowed us to select bacterial strains of interest. Algal-bacterial cocultures have shown their impact on algal growth, and unexpected results led us to consider other parameters: the general state of the starting seedling, the composition of its initial microbiota and the phenomenon of quorum sensing (QS). The results show a correlation between an increase of QS molecules and a decrease in algal growth. Together, these results on S. latissima microbiota’s composition help decipher its impact on the algal host and, more generally, contribute to a better understanding of the algal holobiont, supporting the idea of interdependence between the host and its microbiota.Saccharina latissima est une des espèces de macroalgues brunes dites ingénieures qui participent à la formation des forêts de laminaires. Plusieurs populations naturelles sont exploitées autour du monde et elle fait également l'objet de développements croissants en aquaculture. Le but de ma thèse est de caractériser le microbiote bactérien et d’étudier les interactions hôte-microbiote au sein de l’holobionte S. latissima, pour comprendre dans quelles mesures la composition du microbiote influence la croissance de l’algue. L’étude du microbiote de S. latissima issues de populations naturelles de Roscoff (France), Helgoland (Allemagne) et Norvège sud (Skagerrak) par métabarcoding 16S a montré une différence de composition en fonction de la zone de la lame, de la zone géographique et de l’état physiologique de l’algue. Des isolements bactériens ont été fait pour avoir accès à la part cultivable du microbiote. La combinaison de ces résultats avec les données de métabarcoding a permis de sélectionner des souches bactériennes d’intérêt. Des cocultures algues-bactéries ont montré leur impact sur la croissance algale et des résultats inattendus ont mené à prendre en compte d’autres paramètres : l’état général de la plantule de départ, la composition de son microbiote initial et le phénomène de quorum sensing (QS). Les résultats montrent une corrélation entre l’augmentation du QS et une baisse de la croissance. Ensemble, ces résultats apportent de nouvelles données sur la composition du microbiote de S. latissima, de son impact sur l’hôte, et participent à la meilleure compréhension de l’holobionte algue, venant à l’appui de l’idée d’interdépendance entre l’hôte et son microbiote

Exchange or Eliminate: The Secrets of Algal-Bacterial Relationships

Algae and bacteria have co-occurred and coevolved in common habitats for hundreds of millions of years, fostering specific associations and interactions such as mutualism or antagonism. These interactions are shaped through exchanges of primary and secondary metabolites provided by one of the partners. Metabolites, such as N-sources or vitamins, can be beneficial to the partner and they may be assimilated through chemotaxis towards the partner producing these metabolites. Other metabolites, especially many natural products synthesized by bacteria, can act as toxins and damage or kill the partner. For instance, the green microalga Chlamydomonas reinhardtii establishes a mutualistic partnership with a Methylobacterium, in stark contrast to its antagonistic relationship with the toxin producing Pseudomonas protegens. In other cases, as with a coccolithophore haptophyte alga and a Phaeobacter bacterium, the same alga and bacterium can even be subject to both processes, depending on the secreted bacterial and algal metabolites. Some bacteria also influence algal morphology by producing specific metabolites and micronutrients, as is observed in some macroalgae. This review focuses on algal-bacterial interactions with micro- and macroalgal models from marine, freshwater, and terrestrial environments and summarizes the advances in the field. It also highlights the effects of temperature on these interactions as it is presently known

Importance of quorum sensing crosstalk in the brown alga Saccharina latissima epimicrobiome

Summary: Brown macroalgae are colonized by diverse microorganisms influencing the physiology of their host. However, cell-cell interactions within the surface microbiome (epimicrobiome) are largely unexplored, despite the significance of specific chemical mediators in maintaining host-microbiome homeostasis. In this study, by combining liquid chromatography coupled to mass spectrometry (LC-MS) analysis and bioassays, we demonstrated that the widely diverse fungal epimicrobiota of the brown alga Saccharina latissima can affect quorum sensing (QS), a type of cell-cell interaction, as well as bacterial biofilm formation. We also showed the ability of the bacterial epimicrobiota to form and inhibit biofilm growth, as well as to activate or inhibit QS pathways. Overall, we demonstrate that QS and anti-QS compounds produced by the epimicrobiota are key metabolites in these brown algal epimicrobiota communities and highlight the importance of exploring this epimicrobiome for the discovery of new bioactive compounds, including potentially anti-QS molecules with antifouling properties

Metabolic Complementarity Between a Brown Alga and Associated Cultivable Bacteria Provide Indications of Beneficial Interactions

Brown algae are key components of marine ecosystems and live in association with bacteria that are essential for their growth and development. Ectocarpus siliculosus is a genetic and genomic model for brown algae. Here we use this model to start disentangling the complex interactions that may occur between the algal host and its associated bacteria. We report the genome-sequencing of 10 alga-associated bacteria and the genome-based reconstruction of their metabolic networks. The predicted metabolic capacities were then used to identify metabolic complementarities between the algal host and the bacteria, highlighting a range of potentially beneficial metabolite exchanges between them. These putative exchanges allowed us to predict consortia consisting of a subset of these ten bacteria that would best complement the algal metabolism. Finally, co-culture experiments were set up with a subset of these consortia to monitor algal growth as well as the presence of key algal metabolites. Although we did not fully control but only modified bacterial communities in our experiments, our data demonstrated a significant increase in algal growth in cultures inoculated with the selected consortia. In several cases, we also detected, in algal extracts, the presence of key metabolites predicted to become producible via an exchange of metabolites between the alga and the microbiome. Thus, although further methodological developments will be necessary to better control and understand microbial interactions in Ectocarpus, our data suggest that metabolic complementarity is a good indicator of beneficial metabolite exchanges in the holobiont