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BY 4.0 license Open Access Published online by De Gruyter October 27, 2023

High-temperature stress induces bacteria-specific adverse and reversible effects on Ulva (Chlorophyta) growth and its chemosphere in a reductionist model system

  • Imen Hmani

    Imen Hmani is a PhD student at the National Institute of Marine Sciences and Technologies in Tunisia and the Faculty of Sciences of Tunis. She is studying the influence of the associated bacteria on algal secondary metabolite production. Global change is also among her research and targets to discover the effect of temperature on algal microbiome. Ms. Hmani also has expertise in seaweeds, organic extraction, antioxidant compounds and biological tests.

    , Fatemeh Ghaderiardakani

    Fatemeh Ghaderiardakani acquired her PhD in Life Sciences from the University of Birmingham, UK. She is a postdoc researcher at the Institute for Inorganic and Analytical Chemistry of the Friedrich Schiller University Jena, Germany. Her main research interests are the chemical communication of bacteria-macroalgae interactions, the bacterial-dependent development of Ulva sp. and the bacteria-mediated cold adaptation of Ulva.

    , Leila Ktari

    Leila Ktari holds a PhD in Marine Biotechnology. She specialises in seaweed biotechnology and is currently a researcher in the B3Aqua Laboratory at the National Institute of Marine Sciences and Technologies. Her research focuses on extracting bioactive substances with high added value, with particular interest in antifouling and antioxidant secondary metabolites.

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    , Monia El Bour

    Monia EL Bour holds a PhD in Aquatic Microbiology (Molecular Biology and Genetics) and is an expert in aquatic biotechnology, microbiology, biomonitoring and bioremediation and bio-valorisation of aquatic micro-organisms. She chairs the CIESM of Marine Microbiology and Biotechnology Committee C4 and is a member of Mediterranean Experts on Climate and Environmental Change (Medecc).

    and Thomas Wichard

    Thomas Wichard is a research group leader and lecturer in Analytical Chemistry at the Institute for Inorganic and Analytical Chemistry of the Friedrich Schiller University Jena (Germany). After being awarded a PhD in Biochemistry (Max Planck Institute for Chemical Ecology), he investigated the metal recruitment of nitrogen fixers at the Princeton Environmental Institute (USA). His team applies various analytical chemistry, chemical ecology, and molecular biology methodologies to understand the basis of eco-physiological processes in bacteria–macroalgae interactions (cross-kingdom interactions).

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From the journal Botanica Marina

Abstract

Axenic cultures of the green seaweed Ulva mutabilis were inoculated with bacteria providing essential algal growth and morphogenesis-promoting factors (AGMPFs) and were exposed to temperature shifts from 18 °C to 30 °C. The temperature-dependent effect of bacteria on longitudinal algal growth and the molecular composition of the chemosphere in the algal culture medium was explored. The reductionist tripartite model system of U. mutabilis, Roseovarius sp. MS2, and Maribacter sp. MS6 was applied as a reference and has been changed by substituting Roseovarius with isolates that phenocopy this strain. Rathayibacter festucae IH2 and Roseovarius aestuarii G8 boosted growth at 18 °C but slowed it down at 30 °C. Additional inoculation of Roseovarius sp. MS2 mitigated these adverse bacterial effects partially. At 30 °C, the molecular profile of the chemosphere differed dramatically between all tested tripartite communities, indicating different traits of the same bacterium with changing temperatures. Functional examinations should, therefore, accompany microbiome analysis to detect changing traits with the same microbiome composition.

The green macroalga Ulva, commonly known as sea lettuce, is found worldwide in coastal areas and faces changes in biotic and abiotic factors (Ghaderiardakani et al. 2020; Qu et al. 2021). Ulva is characterised by tolerance to a broad range of environmental conditions. High growth rates and photosynthetic activity lead to abundant natural biomass that causes the formation of green tides (Smetacek and Zingone 2013). The sea lettuce Ulva can grow over a wide range of temperatures, but growth rates may vary depending on the temperature (Xiao et al. 2016). Rising temperatures have various effects on seaweed populations; for example, slowing growth rates, stimulating the transcription of stress response genes, and increasing the activities of specific antioxidative enzymes (Cui et al. 2015; Kim et al. 2011; Sánchez de Pedro et al. 2023; Yang et al. 2019). As essential biotic factors such as associated bacteria affect the growth and morphogenesis of Ulva (Wichard 2015, 2023), understanding the cumulative effect of environmental factors and stressors is crucial, for example, for the maintenance of Integrated Multi-Trophic Aquaculture Recirculation Systems (IMTA-RAS) (Califano et al. 2020; Pintado et al. 2023).

Ulva mutabilis Føyn, recently reclassified as U. compressa (Steinhagen et al. 2019), is used as a model system to study the effect of epibionts. Roseovarius sp. MS2 and Maribacter sp. MS6 are two bacteria that provide essential algal growth and morphogenesis-promoting factors (AGMPFs); without these, a callus of U. mutabilis is formed under axenic conditions (Spoerner et al. 2012). The tripartite community of U. mutabilis, Roseovarius sp. MS2, and Maribacter sp. MS6 creates a specific chemosphere, i.e., a space where organisms interact via compounds such as infochemicals, nutrients, morphogens, and defence compounds (Alsufyani et al. 2017). Understanding the mechanisms and pathways underlying these interactions is essential for explaining ecological distribution, physiology, and responses to environmental variations (Ghaderiardakani et al. 2020; van der Loos et al. 2019). Whereas the Maribacter-factor has been recently identified as thallusin (Alsufyani et al. 2020), the Roseovarius-factor is still unknown, although it would be produced by various bacterial taxa (Grueneberg et al. 2016). Changes in temperature, irradiance, and micropollutants can negatively affect algae and bacterial communities, resulting in an increased prevalence of disease and dysbiosis (Egan et al. 2013; KleinJan et al. 2023; Sörenson et al. 2021). Understanding the connections between holobionts and their stressors in a changing environment may enable us to help vulnerable seaweed populations adapt to adverse conditions in aquaculture maintenance or ecosystem management (Ghaderiardakani et al. 2020; Saha et al. 2019).

Our study aimed to discover the effect of warm temperatures on bacteria-induced growth and the development of U. mutabilis, which is a direct descendant of the original isolate of B. Føyn (Føyn 1958), under standardised laboratory conditions to analyse the impact of global warming on specific bacteria and in turn on the growth of Ulva. Therefore, axenic gametes of U. mutabilis were inoculated with previously isolated bacteria from Ulva ohnoi M.Hiraoka et S. Shimada collected in the Mediterranean Sea (Hmani et al. 2023; Ismail et al. 2018) using established protocols for the preparation of axenic cultures (Califano et al. 2020; Spoerner et al. 2012). A tripartite community comprising Ulva and two bacterial taxa releasing AGMPFs was exposed to a temperature shift from 18 °C to 30 °C to determine whether the epiphytic bacteria releasing the Roseovarius-factor had temperature-dependent effects on algal growth and development. The molecular composition of their chemosphere was analysed using exo-metabolomics (Alsufyani et al. 2017) (Figure 1).

Figure 1: 
Workflow. Selected bacteria IH2, IH18, IH25, and G8 were collected from the surface of Ulva ohnoi, phenocopying the activity of Roseovarius sp. MS2 and forming a tripartite community with Maribacter sp. MS6 and the gametophyte of Ulva mutabilis (morphotype “slender”; strain FSU-UM5-1). Ulva mutabilis (25 mg dry weight) was cultivated with the two bacterial strains (OD620 = 0.001) under standard conditions (Wichard and Oertel 2010). Propagules of equal length were stressed by a temperature shift from 18 °C to 30 °C using continuous light (80 µmol photon m−2 s−1) to avoid chronobiological effects. Axenic cultures and tripartite communities were prepared according to Spoerner et al. (2012). exo-Metabolomics and multivariate analysis of the metabolite profiling of the supernatant (150 mL) of four tripartite communities were performed according to Alsufyani et al. (2017) and Ghaderiardakani et al. (2022). Drawings of Ulva were taken from Wichard (2023) under the terms of CC BY 4.0. Created with BioRender.com.
Figure 1:

Workflow. Selected bacteria IH2, IH18, IH25, and G8 were collected from the surface of Ulva ohnoi, phenocopying the activity of Roseovarius sp. MS2 and forming a tripartite community with Maribacter sp. MS6 and the gametophyte of Ulva mutabilis (morphotype “slender”; strain FSU-UM5-1). Ulva mutabilis (25 mg dry weight) was cultivated with the two bacterial strains (OD620 = 0.001) under standard conditions (Wichard and Oertel 2010). Propagules of equal length were stressed by a temperature shift from 18 °C to 30 °C using continuous light (80 µmol photon m−2 s−1) to avoid chronobiological effects. Axenic cultures and tripartite communities were prepared according to Spoerner et al. (2012). exo-Metabolomics and multivariate analysis of the metabolite profiling of the supernatant (150 mL) of four tripartite communities were performed according to Alsufyani et al. (2017) and Ghaderiardakani et al. (2022). Drawings of Ulva were taken from Wichard (2023) under the terms of CC BY 4.0. Created with BioRender.com.

Ulva-associated bacteria were isolated from the surface of U. ohnoi, which was collected from the coast of Tunisia (Ghar El Melh lagoon), by vortexing in sterile seawater and subsequently plating aliquots on marine agar (Ismail et al. 2018). About 50 bacteria were originally identified by their 16S rRNA gene sequences and phylogenetic analysis (Hmani et al. 2023; Ismail et al. 2018). Interestingly, several potential pathogens were associated with U.  ohnoi (Hmani et al. 2023). Using the Ulva morphogenetic bioassay array (Grueneberg et al. 2016), cultivatable bacteria were screened for those that could replace Roseovarius sp. MS2 and induce cell division and growth of U. mutabilis in the tripartite community. Herein, we focused on strains belonging to genera that were not previously identified as potential producers of AGMPFs (Ghaderiardakani et al. 2019; Grueneberg et al. 2016; Singh and Reddy 2014). As a result, two morphogenetically active strains of bacteria from the under-investigated phylum Actinomycetota were compared with two strains of the phylum α-Proteobacteria regarding their morphogenetic activity (Figure 2).

Figure 2: 
Bioassay for morphogenetic activity performed at 18 °C. Using a tripartite community with Ulva mutabilis, the morphogenetic activity of the thallusin-releasing bacteria Maribacter sp. was complemented by one out of the four strains isolated from the surface of Ulva ohnoi. Under standard conditions, axenic gametes (A) were cultivated in the tissue culture flask with the tested bacteria alone (B–E), in the presence of Roseovarius sp. (G–J) or with Maribacter sp. MS6 (L–O) in comparison to the controls (F and K). Arrows with closed heads indicate protrusion formation due to the lack of thallusin released by Maribacter sp. Arrows with open heads indicate rhizoid formation in the presence of Maribacter sp. Magnification bar = 100 µm.
Figure 2:

Bioassay for morphogenetic activity performed at 18 °C. Using a tripartite community with Ulva mutabilis, the morphogenetic activity of the thallusin-releasing bacteria Maribacter sp. was complemented by one out of the four strains isolated from the surface of Ulva ohnoi. Under standard conditions, axenic gametes (A) were cultivated in the tissue culture flask with the tested bacteria alone (B–E), in the presence of Roseovarius sp. (G–J) or with Maribacter sp. MS6 (L–O) in comparison to the controls (F and K). Arrows with closed heads indicate protrusion formation due to the lack of thallusin released by Maribacter sp. Arrows with open heads indicate rhizoid formation in the presence of Maribacter sp. Magnification bar = 100 µm.

Among the selected bacteria (Table 1), the Actinobacteria Rathayibacter festucae and Microbacterium phyllosphaerae were of particular interest. The genus Rathayibacter includes several species, for example, R. rathayi, that are plant pathogens transmitted to their host plants by seed gall nematodes (Murray et al. 2017; Riley and McKay 1990; Tarlachkov et al. 2020). We thus hypothesised that Rathayibacter might have a negative effect on the growth and development of Ulva. However, the morphogenetic bioassay, carried out at 18 °C, revealed that the selected bacteria were able to phenocopy the effects of Roseovarius sp. MS2 (positive control) (Figure 2B–E) and to complement Maribacter sp. MS6 and the tripartite community for complete morphogenesis (Figure 2L–O compared to K). The tested strains stimulated cell division compared to axenic cultures (Figure 2A, negative control) or inoculation with inactive strains such as Pseudomonas spp. (Grueneberg et al. 2016). Co-inoculation of the test strain with Roseovarius sp. MS2 but without Maribacter sp. MS6 did not further improve propagule growth under the conditions of the bioassay at 18 °C (Figure 2G–J compared to F).

Table 1:

Bacteria isolated from Ulva ohnoi and characterised by sequencing the 16S rRNA gene using the primers B8F (5′-AGAGTTTGATCMTGGCTCAG-3′) and U1492R (5′-GGTTACCTTGTTACGACTT-3′). GenBank accession numbers are given.

Phylum Isolate ID Size (bp) Closest matching species in the NCBI database Accession number Identity (%)
Proteobacteria IH25 850 Dinoroseobacter shibae MZ150448 99
G8 1055 Roseovarius aestuarii FN811290 98
Actinobacteria IH2 750 Rathayibacter festucae MZ150443 100
IH18 1189 Microbacterium phyllosphaerae MZ150453 98

To explore the differences in the growth and metabolite profile of the chemosphere of Ulva in response to an abrupt temperature increase, four distinct tripartite communities were subjected to a temperature shift from 18 °C to 30 °C. After 14 days of incubation, Ulva thalli were harvested, and their lengths were measured (Figure 3A). The tripartite community of the model system Ulva mutabilisRoseovarius sp.–Maribacter sp. did not show any significant differences upon the temperature shift and thus appeared to be temperature resilient. Noteworthy, M. phyllosphaerae could replace the activities of Roseovarius sp. at 30 °C. However, the strains Roseovarius aestuarius and Rathayibacter festucae did not sustain growth at 30 °C, and longitudinal growth was slowed by up to 50 % (Figure 3A). This result could be due to, for example, reduced levels of unidentified AGMPFs or harmful (bacterial) substances secreted in Ulva’s chemosphere by R. aestuarius or R. festucae at 30 °C. Two opposing biological activities of a bacterium in a changing environment have already been described in other marine interactions and referred to as Jekyll-and-Hyde chemistry (Seyedsayamdost et al. 2011).

Figure 3: 
Temperature shift experiment from 18 °C to 30 °C. (A) After the temperature shift, the longitudinal growth of the propagules of equal length in three different tripartite communities was measured with ImageJ software and compared with the established model system for Ulva mutabilis–Roseovarius sp. MS2–Maribacter sp. MS6. The error bars represent the confidence intervals (p = 0.95; n = 30 individuals with three replicates). Student’s t-tests showed significant differences between the thallus lengths of algae grown at 18 °C and 30 °C (***, p < 0.001). (B) Experiment replicate and after the addition of Roseovarius sp. MS2, the tripartite community of U. mutabilis–R. festucae–Maribacter sp., recovers partly in longitudinal growth within 14 days. (C and D) The main principal coordinates (PCo, C) and two canonical axes of the canonical analysis of the principal coordinates (CAP, D) were computed from the Bray–Curtis similarity matrix upon ln transformation and sum normalisation of the samples. For the constrained analysis, treatments at 18 °C were pooled. The experiment was carried out in triplicate. (E) Volcano plot illustrating the exo-metabolomic data of the Ulva–Rathayibacter–Maribacter community. The plots show significance versus fold-change (FC) on the y and x axes. “Up-regulated” and “down-regulated” refer to the temperature shift treatment from 18 °C to 30 °C. Points above the line have p < 0.1. Blue dots represent downregulated metabolites, and red dots indicate upregulated metabolites in the growth medium after a temperature shift from 18 °C to 30 °C. Arrow indicates the suggested identification of the fatty acid eicosatrienoic acid.
Figure 3:

Temperature shift experiment from 18 °C to 30 °C. (A) After the temperature shift, the longitudinal growth of the propagules of equal length in three different tripartite communities was measured with ImageJ software and compared with the established model system for Ulva mutabilisRoseovarius sp. MS2–Maribacter sp. MS6. The error bars represent the confidence intervals (p = 0.95; n = 30 individuals with three replicates). Student’s t-tests showed significant differences between the thallus lengths of algae grown at 18 °C and 30 °C (***, p < 0.001). (B) Experiment replicate and after the addition of Roseovarius sp. MS2, the tripartite community of U. mutabilisR. festucaeMaribacter sp., recovers partly in longitudinal growth within 14 days. (C and D) The main principal coordinates (PCo, C) and two canonical axes of the canonical analysis of the principal coordinates (CAP, D) were computed from the Bray–Curtis similarity matrix upon ln transformation and sum normalisation of the samples. For the constrained analysis, treatments at 18 °C were pooled. The experiment was carried out in triplicate. (E) Volcano plot illustrating the exo-metabolomic data of the UlvaRathayibacterMaribacter community. The plots show significance versus fold-change (FC) on the y and x axes. “Up-regulated” and “down-regulated” refer to the temperature shift treatment from 18 °C to 30 °C. Points above the line have p < 0.1. Blue dots represent downregulated metabolites, and red dots indicate upregulated metabolites in the growth medium after a temperature shift from 18 °C to 30 °C. Arrow indicates the suggested identification of the fatty acid eicosatrienoic acid.

We then checked whether the subsequent addition of the growth-promoting bacterium Roseovarius sp. MS2 could allow the development of Ulva to recover in the presence of R. festucae at 30 °C. The results showed that the adverse effect of R. festucae was partially compensated (Figure 3B), forming a quadripartite community. This observation implies that a complex and diverse microbiome can withstand and compensate for adverse effects to some extent and provide stable growth conditions for Ulva. Inoculation of beneficial Roseovarius sp. MS2 in the presence of R. festuca from the beginning of the cultivation might offset any adverse effects of the latter strain.

In particular, if a diverse group of bacteria contributes to the same trait (Grueneberg et al. 2016), it is still challenging to observe specific (e.g., adverse or beneficial) bacterial traits using solely explorative omics approaches without knowing the involved pathways. Without knowing the functional traits, this may also be why observations vary concerning microbiome-dependent effects on the host upon experiencing a stress stimulus such as a temperature shift. For example, although minor changes in the complex microbiome of brown algae did not contribute to adaptation processes following a thermal stimulus (Delva et al. 2023), the unknown ecophysiological traits of the bacteria within the native microbiome may have changed to the benefit of the algae. Allsup et al. (2023) demonstrated that inoculated tree seedlings exposed to cold winters or drought fared better in soil containing microbial populations from colder or drier areas. These findings underscore the significance of species relationships in shaping the ability of trees to adapt to climate change and predict greater potential resilience for trees (Allsup et al. 2023), as has also been suggested for macroalgae (Ghaderiardakani et al. 2020; Morrissey et al. 2021; van der Loos et al. 2019).

Our reductionist experiment indicates that traits of a native microbiome could balance the adverse or less beneficial effects of specific bacteria in a stress situation through the alternative traits of multiple bacterial resources (Figure 3B). This is most likely not the case for species of the genus Maribacter (Weiss et al. 2017) that produce the morphogen thallusin via unique biochemical pathways (J. Ulrich and T. Wichard, unpublished data) and cannot be easily replaced by other bacterial genera. It is noteworthy that recent studies have demonstrated that holobiont manipulation through bacteria inoculation in macroalgal aquaculture can be successfully carried out in a model IMTA-RAS and for disease management (Deutsch et al. 2023; Pintado et al. 2023). To ensure the longevity of the newly formed relationships between bacteria and algae, the molecular interactions that contribute to the niche’s resistance must be understood. The study of the exo-metabolome, the entity of all released metabolites by the holobiont, can disentangle the importance of chemical-mediated interactions.

The pool of released bacterial chemicals can be used to explain why algae may react differently under various stress scenarios. Although the tripartite community has not been altered during the temperature shift, the profile of substances it releases may change in response to environmental stress. To decipher these changes in the chemosphere, solid-phase extraction of metabolites was carried out to monitor the exo-metabolome in the culture medium. Sterile-filtered supernatants of the cultures were loaded on a hydrophilic–lipophilic balanced matrix (HLB Oasis cartridge, Waters, UK). The extracts were analysed by electrospray ionisation high-resolution mass spectrometry (ESI-HR-MS) in combination with ultra-high-pressure liquid reversed phase (C18) chromatography (UHPLC) and subsequent data analysis by Compound Discoverer (v. 3.1, Thermo Fisher Scientific, Germany) (Ghaderiardakani et al. 2022, Supplemental Material). After applying background corrections, the subsequent analysis revealed 893 unidentified compounds with mass/charge ratios from 100 to 1200 m/z. Those features were analysed using multivariate statistics (Alsufyani et al. 2017).

The various tripartite communities were already distinctly separated between the treatments of 18 °C and 30 °C; these were visualised by principal coordinates (PCo) analysis (Figure 3C), emphasising their temperature-dependent influence on the chemosphere. The chemosphere profiles of the four examined tripartite communities were substantially more varied at 18 °C than at 30 °C (Figure 3C). As a result, the supervised discriminant analysis defined five groups: one pooled group for all treatments of U. mutabilis grown at 18 °C and four groups of U. mutabilis cultured at 30 °C representing the four different tripartite communities (Supplementary Table S1). Subsequent canonical analysis of the principal coordinates of the a priori groups revealed that metabolite profiles were significantly different depending on the temperature (Figure 3D). Using the “leave-one-out” allocation approach (Anderson and Willis 2003; Ghaderiardakani et al. 2022), cross-validation between the a priori groups resulted in no misclassification error of the constrained groups (Figure 3D, Supplementary Table S1). Canonical analysis of principal coordinates (CAP) used the correlation coefficients between each sample and the canonical axes to identify essential biomarkers (Figure 3D). Interestingly, heat stress altered the molecular composition of the chemosphere in the presence of the same microbiome. This result demonstrates that the interactive relationship between algae and the bacteria responded to the temperature stress. As a result, microbiome analysis determining the bacterial composition alone is insufficient to assess bacteria-dependent responses to a stimulus.

Changes in the chemosphere of the tripartite community Ulva mutabilisRathayibacter festucaeMaribacter sp. were determined during the temperature shift from 18 °C to 30 °C in detail (Figure 3E). Apart from the increased amount of 8,11,14-eicosatrienoic acid (Supplementary Table S2), which can be found occasionally in minor amounts in Ulva (Kumari et al. 2014) but is more abundant in R. festucae, the identities of the 20 significantly and most strongly dysregulated compounds (p < 0.001) have yet to be confirmed. While it is evident that the chemosphere is determined by the composition of bacteria associated with Ulva under stress, the identification of the unknown compounds (i.e., m/z features, Supplementary Table S2) is still challenging for further studies.

In summary, regardless of the conditions, essential bacteria must provide Ulva with algal growth and morphogenesis-promoting factors. As a result, both bacteria and algae need to respond to the stimulus to the same extent. Observation of the longitudinal algal growth combined with exo-metabolomics of the chemosphere revealed that certain bacterial–algal interactions promoting algal growth were temperature sensitive. Our findings demonstrate how the individual stress-dependent behaviours of bacteria in terms of morphogenetic activity can be determined using controlled studies. Predicted negative impacts can be compensated by accompanying bacteria such that they no longer appear in the overall picture of a microbiome study. These bacteria may belong to the core microbiome that has evolved in holobiont establishment and ensures stress resilience under adverse conditions such as high temperatures. Our study contributes a first step in unravelling the adverse and beneficial molecular effects of bacteria within a microbiome due to a stress stimulus for macroalgae.


Corresponding author: Thomas Wichard, Institute for Inorganic and Analytical Chemistry, Friedrich Schiller University Jena, Lessingstr. 8, 07743 Jena, Germany, E-mail:

Award Identifier / Grant number: SPP 1158 / 424256657

Award Identifier / Grant number: CA20106

Award Identifier / Grant number: FA1406

Funding source: University Tunis-El Manar

About the authors

Imen Hmani

Imen Hmani is a PhD student at the National Institute of Marine Sciences and Technologies in Tunisia and the Faculty of Sciences of Tunis. She is studying the influence of the associated bacteria on algal secondary metabolite production. Global change is also among her research and targets to discover the effect of temperature on algal microbiome. Ms. Hmani also has expertise in seaweeds, organic extraction, antioxidant compounds and biological tests.

Fatemeh Ghaderiardakani

Fatemeh Ghaderiardakani acquired her PhD in Life Sciences from the University of Birmingham, UK. She is a postdoc researcher at the Institute for Inorganic and Analytical Chemistry of the Friedrich Schiller University Jena, Germany. Her main research interests are the chemical communication of bacteria-macroalgae interactions, the bacterial-dependent development of Ulva sp. and the bacteria-mediated cold adaptation of Ulva.

Leila Ktari

Leila Ktari holds a PhD in Marine Biotechnology. She specialises in seaweed biotechnology and is currently a researcher in the B3Aqua Laboratory at the National Institute of Marine Sciences and Technologies. Her research focuses on extracting bioactive substances with high added value, with particular interest in antifouling and antioxidant secondary metabolites.

Monia El Bour

Monia EL Bour holds a PhD in Aquatic Microbiology (Molecular Biology and Genetics) and is an expert in aquatic biotechnology, microbiology, biomonitoring and bioremediation and bio-valorisation of aquatic micro-organisms. She chairs the CIESM of Marine Microbiology and Biotechnology Committee C4 and is a member of Mediterranean Experts on Climate and Environmental Change (Medecc).

Thomas Wichard

Thomas Wichard is a research group leader and lecturer in Analytical Chemistry at the Institute for Inorganic and Analytical Chemistry of the Friedrich Schiller University Jena (Germany). After being awarded a PhD in Biochemistry (Max Planck Institute for Chemical Ecology), he investigated the metal recruitment of nitrogen fixers at the Princeton Environmental Institute (USA). His team applies various analytical chemistry, chemical ecology, and molecular biology methodologies to understand the basis of eco-physiological processes in bacteria–macroalgae interactions (cross-kingdom interactions).

Acknowledgements

The article is also based upon work from COST Action FA1406 “Phycomorph” and COST Action CA20106 “Tomorrow’s wheat of the sea’: Ulva, a model for an innovative mariculture”, supported by COST (European Cooperation in Science and Technology, www.cost.eu).

  1. Research ethics: Not applicable.

  2. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  3. Competing interests: The authors declare that they have no conflicts of interest regarding this article.

  4. Research funding: The study was supported by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) in the framework of the priority program (SPP 1158) “Antarctic Research with comparative investigations in Arctic ice areas” (424256657, FG, and TW). Research was financed by a grant provided by the University Tunis-El Manar and the Faculty of Sciences Tunis (IH).

  5. Data availability: The exo-metabolomics data are available in the public database Zenodo: https://zenodo.org/record/8316116.

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Supplementary Material

This article contains supplementary material (https://doi.org/10.1515/bot-2023-0053).


Received: 2023-07-07
Accepted: 2023-09-07
Published Online: 2023-10-27

© 2023 the author(s), published by De Gruyter, Berlin/Boston

This work is licensed under the Creative Commons Attribution 4.0 International License.

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