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Establishment of a tripartite community of U. mutabilis with novel bacteria. Three-week-old U. mutabilis gametophytes are shown inoculated with bacteria isolated from different Ulva species in pairwise combination. Axenic gametes of U. mutabilis were inoculated with (A) Microbacterium sp. EC19 only, and together with (B) Microbacterium sp. UL19, (C) Planococcus sp. E1, (D) Paracoccus sp. E34, (E) Cellulophaga sp. UL16 or (F) Paracoccus sp. UL2. (D-F) Due to the complementary functional traits of the bacteria, the tripartite community can completely recover the morphogenesis of U. mutabilis, whereas the bacterial isolates UL19 and E1 do not contribute to the algal development. The bioassay system was scaled up using sterile culture flasks. Scale bars = 100 μm.
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The green marine macroalgae of the class Ulvophyceae (Ulvophytes) are common algae distributed worldwide particularly in intertidal areas, which play a key role in aquatic ecosystems. They are potentially valuable resources for food, animal feed and fuel but can also cause massive nuisance blooms. Members of Ulvaceae, like many other seaweeds, harb...
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... morpho- logical scores by Marshall et al. (2006) (Table 1), but different func- tional traits for growth and morphogenesis were not determined at that time. Therefore, in our study, bacterial strains were se- lected according to their two main functional traits (Figs 1 and 2) in order to define new tripartite communities with U. muta- bilis (Fig. 4) or U. intestinalis (Fig. 5). Importantly, there was no species-specificity between U. intestinalis and U. mutabilis, be- cause a range of bacteria can perform their eco-physiological functions similarly in both species (Figs 1 and ...
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... and in combination with any one of E34, UL16 or UL2, which phenocopy the Roseovarius sp. MS2 (Figs 4 and 5). Upon inoculations, bacteria grew and formed a cluster around the rhizoid of U. intestinalis (Fig. 6A) resembling the tripartite U. mutabilis-Roseovarius-Maribacter sys- tem (Spoerner et al. 2012). ...
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... However, it is unlikely that the water column microbiome itself could affect our results since water and macroalgal microbiomes greatly differ (Minich et al., 2018;Michotey et al., 2020;Quigley et al., 2020). Other less explored sources of microbial variation could be related to the competitive lottery model, in which Sargassum microbial associations are functionally related and not necessarily taxonomically similar (Burke et al., 2011;Ghaderiardakani et al., 2017). Morphologically different structures can also harbor unique strains of bacteria (Serebryakova et al., 2018;Quigley et al., 2020). ...
Holopelagic Sargassum has been causing massive strandings on tropical Atlantic Ocean shorelines. Describing the microbiome associated with Sargassum and how it changes after stranding is important to identify potential microbial introductions to coastal environments, as well as sources of potential biotechnological resources. In this study, stranding simulation exploratory experiments were conducted for S. fluitans III and S. natans VIII on shipboard with minimum external influence. Samples for microbiome identification were collected just after removing healthy Sargassum from the seawater (0 hr) and after 24 and 48 hrs of stranding simulation under environmental conditions. The bacterial community was identified by sequencing 16S rRNA gene V3-V4 hypervariable regions, generating a total of 1,565 Amplicon Sequence Variants (ASVs). Of those, 588 were shared between Sargassum species and only 25 persisted throughout the stranding. Stranding also changed the dominance of Microtrichales and Rhodobacterales orders at 0 hr to Alteromonadales and Vibrionales after 24 hrs of exposure, the latter representing up to 92% of the relative abundance in the bacterial community. The increase in Vibrionales reinforces the need to monitor stranding sites for any potential pathogenic bacteria. At the functional level, phototrophs were the main group at 0 hr, shifting to chemoheterotrophs and fermentation within the first 24 hrs of Sargassum exposure to air conditions. The fermentative groups native to Sargassum use stranded biomass as substrate for growth, and therefore constitute the bacteria with higher biotechnological potential.
Keywords:
Brown tide; Microbial community; Dysbiosis; High-throughput sequencing; Amplicon Sequence Variants
... In coastal marine ecosystems, macroalgae and seagrasses are increasingly recognised as hosts of microbiomes that include nitrogen-fixing taxa (Cardini et al., 2018;Mohr et al., 2021), carbon-degrading taxa , and impact overall host health either positively or negatively (Li et al., 2022). Factors provided by associated microbes are important for macrophyte health, as demonstrated by developmental abnormalities in axenic seaweed cultures (Croft et al., 2005;Ghaderiardakani et al., 2017). Despite this increasing evidence that macrophytes host important microbes, much remains unknown about the molecular basis underlying host-microbe interactions. ...
... We isolated strains of the genus Marinomonas, other strains of which control the morphology of its green seaweed host, Ulva (Singh et al., 2011). While we have no evidence yet for the same effect of Marinomonas on the kelp host we studied here, other studies have shown the importance of bacteria in the phenotype of seaweed, where development is thwarted in the absence of key taxa (Croft et al., 2005;Ghaderiardakani et al., 2017). ...
In coastal marine ecosystems, kelp forests serve as a vital habitat for numerous species and significantly influence local nutrient cycles. Bull kelp, or Nereocystis luetkeana, is a foundational species in the iconic kelp forests of the northeast Pacific Ocean and harbours a complex microbial community with potential implications for kelp health. Here, we report the isolation and functional characterisation of 16 Nereocystis‐associated bacterial species, comprising 13 Gammaproteobacteria, 2 Flavobacteriia and 1 Actinomycetia. Genome analyses of these isolates highlight metabolisms potentially beneficial to the host, such as B vitamin synthesis and nitrogen retention. Assays revealed that kelp‐associated bacteria thrive on amino acids found in high concentrations in the ocean and in the kelp (glutamine and asparagine), generating ammonium that may facilitate host nitrogen acquisition. Multiple isolates have genes indicative of interactions with key elemental cycles in the ocean, including carbon, nitrogen and sulphur. We thus report a collection of kelp‐associated microbial isolates that provide functional insight for the future study of kelp–microbe interactions.
... A large proportion of isolates obtained in this study belonged to those groups and may have a role in Ulva sp. growth, as it has previously been shown for Microbacterium sp., which promotes the development of the thallus and rhizoids of U. intestinalis (Ghaderiardakani et al. 2017). Moreover, Zobellia sp., Shewanella sp., Vibrio sp., and Pseudoalteromonas sp. ...
Macroalgae harbor a rich epiphytic microbiota that plays a crucial role in algal morphogenesis and defense mechanisms. This study aims to isolate epiphytic cultivable microbiota from Ulva sp. surfaces. Various culture media were employed to evaluate a wide range of cultivable microbiota. Our objective was to assess the antibacterial and biofilm-modulating activities of supernatants from isolated bacteria.
69 bacterial isolates from Ulva sp. were identified based on 16S rRNA gene sequencing. Their antibacterial activity and biofilm modulation potential were screened against three target marine bacteria : 45%, mostly affiliated with Gammaproteobacteria and mainly grown on diluted R2A medium (R2Ad), showed strong antibacterial activity while 18% had a significant impact on biofilm modulation. Molecular network analysis was carried out on four bioactive bacterial supernatants, revealing new molecules potentially responsible for their activities. R2Ad offered the greatest diversity and proportion of active isolates. The molecular network approach holds promise for both identifying bacterial isolates based on their molecular production and characterizing antibacterial and biofilm-modulating activities.
... Microorganisms able to flourish in association with macroalgae living in such distinctive and challenging ecological niches are expected to possess unique adaptive mechanisms and diversity. Recently, studies using Chlorophyta Ulva species have shown that the macroalgae-associated bacterial community, including Actinomycetota, can have beneficial and adverse effects on host growth and development depending on environmental stress conditions (Ghaderiardakani et al., 2017;Hmani et al., 2023). In the single study harnessing exclusively the diversity and bioactive potential of the Actinomycetota culturable community associated with kelp from the northern Portuguese shore, a rich reservoir of taxonomically diverse strains producing antimicrobial and anticancer metabolites was uncovered (Girão et al., 2019). ...
Actinomycetota, associated with macroalgae, remains one of the least explored marine niches. The secondary metabolism of Actinomycetota, the primary microbial source of compounds relevant to biotechnology, continues to drive research into the distribution, dynamics, and metabolome of these microorganisms. In this study, we employed a combination of traditional cultivation and metagenomic analysis to investigate the diversity of Actinomycetota in two native macroalgae species from the Portuguese coast. We obtained and taxonomically identified a collection of 380 strains, which were distributed across 12 orders, 15 families, and 25 genera affiliated with the Actinomycetia class, with Streptomyces making up approximately 60% of the composition. Metagenomic results revealed the presence of Actinomycetota in both Chondrus crispus and Codium tomentosum datasets, with relative abundances of 11% and 2%, respectively. This approach identified 12 orders, 16 families, and 17 genera affiliated with Actinomycetota, with minimal overlap with the cultivation results. Acidimicrobiales emerged as the dominant actinobacterial order in both macroalgae, although no strain affiliated with this taxonomic group was successfully isolated. Our findings suggest that macroalgae represent a hotspot for Actinomycetota. The synergistic use of both culture‐dependent and independent approaches proved beneficial, enabling the identification and recovery of not only abundant but also rare taxonomic members.
... The use of model systems has enabled us to determine direct, microbially mediated effects, and their underlying mechanisms in a number of model eukaryotic hosts, particularly those associated with one or a few microbial symbionts, such as for the bobtail squid Euphrymna scolopes and its bacterial symbiont Aliivibrio fisheri 20 . Within macroalgal systems, the clearest demonstrations of the role of complex microbial communities on host function (reviewed in ref. 21) are from the model algae Ulva spp [22][23][24] and Ectocarpus spp 12,25 . Beyond model systems, there has been work exploring the role of microbiota in the function of hosts such as mosquitos 15,[26][27][28] and daphnia 16,29 . ...
Host-associated microbiota are critical for eukaryotic host functioning, to the extent that hosts and their associated microbial communities are often considered “holobionts”. Most studies of holobionts have focused on descriptive approaches or have used model systems, usually in the laboratory, to understand host-microbiome interactions. To advance our understanding of host-microbiota interactions and their wider ecological impacts, we need experimental frameworks that can explore causation in non-model hosts, which often have highly diverse microbiota, and in their natural ecological setting (i.e. in the field). We used a dominant habitat-forming seaweed, Hormosira banksii , to explore these issues and to experimentally test host-microbiota interactions in a non-model holobiont. The experimental protocols were aimed at trying to disentangle microbially mediated effects on hosts from direct effects on hosts associated with the methods employed to manipulate host-microbiota. This was done by disrupting the microbiome, either through removal/disruption using a combination of antimicrobial treatments, or additions of specific taxa via inoculations, or a combination of thew two. The experiments were done in mesocosms and in the field. Three different antibiotic treatments were used to disrupt seaweed-associated microbiota to test whether disturbances of microbiota, particularly bacteria, would negatively affect host performance. Responses of bacteria to these disturbances were complex and differed substantially among treatments, with some antibacterial treatments having little discernible effect. However, the temporal sequence of responses antibiotic treatments, changes in bacterial diversity and subsequent decreases in host performance, strongly suggested an effect of the microbiota on host performance in some treatments, as opposed to direct effects of the antibiotics. To further test these effects, we used 16S-rRNA-gene sequencing to identify bacterial taxa that were either correlated, or uncorrelated, with poor host performance following antibiotic treatment. These were then isolated and used in inoculation experiments, independently or in combination with the previously used antibiotic treatments. Negative effects on host performance were strongest where specific microbial antimicrobials treatments were combined with inoculations of strains that were correlated with poor host performance. For these treatments, negative host effects persisted the entire experimental period (12 days), even though treatments were only applied at the beginning of the experiment. Host performance recovered in all other treatments. These experiments provide a framework for exploring causation and disentangling microbially mediated vs. direct effects on hosts for ecologically important, non-model holobionts in the field. This should allow for better predictions of how these systems will respond to, and potentially mitigate, environmental disturbances in their natural context.
... It is commonly recognized that Ulva-associated bacteria have been extensively studied with functions related to host growth and morphological development (Dhanya et al. 2016;Ghaderiardakani et al. 2017;Habbu et al. 2016;Wichard 2023), yet species of Ulva also harbour a rich diversity of endophytic fungi like many other seaweeds. Endophytic fungi can colonize the inner tissues of algae without causing any visible damage or disease symptoms (Zhang et al. 2016). ...
Several studies have shown that endophytic fungal metabolites possess vital biological activities; nevertheless , there is a lack of knowledge regarding the medicinally important marine endophytic fungi associated with the seaweeds mainly found in the Bay of Bengal, Bangladesh. In this study, six endophytic fungi, belonging to five genera and four classes, were isolated from the well-known chlor-ophyte, Ulva sp. and were most closely related to Chaeto-mium globosum, Nigrospora magnoliae, Curvularia sp., Curvularia moringae, Aspergillus terreus and Collariella sp. This is the first report of these fungi as endophytes associated with Ulva sp. from the Bay of Bengal, Bangladesh. A preliminary biological evaluation of the ethyl acetate extract of each endophytic fungal crude extract was the prime objective of this research, e.g., antimicrobial assay, 2,2-diphenyl-1-picrylhydrazyl free radical scavenging activity and brine shrimp lethality bioassay. Evaluation of test results revealed that each fungal crude extract possessed one or more relevant biological activities. Preliminary chemical screening using TLC and NMR spectroscopic analysis revealed the presence of several secondary metabolites in the crude fungal extracts. These findings suggest that the marine endophytic fungus may be a valuable source for investigating potentially bioactive chemicals or leads for novel drug candidates.
... Morphogenesis agents 22 21,22 , whereas in brown and green algae a co-culture of different strains is required for morphogenic development [23][24][25] ( Fig. 2). This symbiotic relationship appears to be supported in model testing of anti-fouling measures. ...
Fouling of maritime infrastructure is pervasive due to abundant biological and chemical activity within the oceanic environment. Marine biofilms and their successional growths are prevalent issues in biofouling, but current industrial and research-based analyses often do not provide a holistic view of the fouling biodiversity. Cathodic protection is a longstanding system safeguarding infrastructure from the corrosive marine environment, but limited studies on interactions between biological growth and cathodic activity have been conducted in the context of marine fouling. This review identifies knowledge gaps in the understanding of marine fouling and highlights approaches to better direct development of effective anti-fouling measures.
... MS2 and Maribacter sp. MS6 forming a tripartite community (Ghaderiardakani et al., 2017;Spoerner et al., 2012). Crossing strains with different mating types is well-described (Føyn, 1959(Føyn, , 1960Hoxmark, 1976). ...
... To complete normal morphogenesis, Ulva mutabilis/compressa requires associated bacteria in a mutualistic relationship exchanging infochemicals (Kessler et al., 2018;Spoerner et al., 2012). The diverse Ulva microbiome changes in natural populations in relation to environmental parameters or bloom formation (Ghaderiardakani et al., 2017(Ghaderiardakani et al., , 2020van der Loos et al., 2022). Currently, few published genome sequences of Ulva-associated bacteria are available, but these resources are expected to add an extra layer of complexity and to shed light on the molecular functions shared by these microbiome partners (Alsufyani et al., 2020;Morales-Reyes et al., 2022). ...
Green seaweeds exhibit a wide range of morphologies and occupy various ecological niches, spanning from freshwater to marine and terrestrial habitats. These organisms, which predominantly belong to the class Ulvophyceae, showcase a remarkable instance of parallel evolution toward complex multicellularity and macroscopic thalli in the Viridiplantae lineage. Within the green seaweeds, several Ulva species ("sea lettuce") are model organisms for studying carbon assimilation, interactions with bacteria, life cycle progression, and morphogenesis. Ulva species are also notorious for their fast growth and capacity to dominate nutrient-rich, anthropogenically disturbed coastal ecosystems during "green tide" blooms. From an economic perspective, Ulva has garnered increasing attention as a promising feedstock for the production of food, feed, and biobased products, also as a means of removing excess nutrients from the environment. We propose that Ulva is poised to further develop as a model in green seaweed research. In this perspective, we focus explicitly on Ulva mutabilis/compressa as a model species and highlight the molecular data and tools that are currently available or in development. We discuss several areas that will benefit from future research or where exciting new developments have been reported in other Ulva species.
... Additionally, Ghaderiardakani et al. (2017) demonstrated that specific bacteria are essential to ensure proper algae growth and differentiation of stem and rhizoid cells. Recently, several studies highlighted the crucial and important role of Ulva-associated bacteria (Wichard et al., 2015;Weiss et al., 2017;Comba-Gonzaĺez et al., 2021); in fact, special chemical mediators are used to ensure that the communication between alga and its associated bacteria and those mediators may be an important source of bioactive molecules and enzymes (Alsufyani et al., 2020). ...
... Among the isolated strains, these authors identified one strain closely related to Paracoccus sp. Interestingly, Paracoccus sp. have been described to have growthpromoting and morphogenesis-inducing function in Ulva (Ghaderiardakani et al., 2017). In this study, isolate IH1 has been found to belong to Paracoccus genus, supporting that species of this genus belong to the resident flora of epiphytic community of Ulva sp. in Ghar El Melh Lagoon. ...
... The functional role of associated bacteria in maintaining their host health has been described in several studies leading to the holobiont concept (Egan et al., 2013;Ghaderiardakani et al., 2020). Ghaderiardakani et al. (2017) demonstrated in Ulva holobiont that there are always specific strains with functions related to growth and morphological development. These authors identified Microbacterium sp. and Paracoccus sp. ...
Seaweed surfaces harbor diverse epibiotic bacterial communities with functions related to morphogenesis, host health, and defense. Among seaweed holobionts, culturable strains can represent innovative sources of bioactive compounds and enzymes. The global industrial demand for microbial enzymes is continually growing in order to improve certain manufacturing processes with new perspectives of industrial exploitation. In this regard, the present study focuses on the enzymatic production and the antimicrobial activities of culturable epibiotic bacteria of Ulva from the Tunisian coast. Culturable associated bacteria were isolated and molecular identification was realized by 16S rRNA gene sequencing. For each strain, eight enzymatic activities were investigated: amylase, hemolysis, DNase, cellulase, lecithinase, lipase, gelatinase, and chitinase. The antimicrobial activity of Ulva-associated bacteria was evaluated against seven pathogenic bacteria, Escherichia coli, Vibrio anguillarum, Vibrio alginoliticus, Pseudomonas aeruginosa, Aeromonas hydrophila, Salmonella typhymurium, and Staphylococcus aureus, and one yeast, Candida albicans. The antibiotic resistance of isolated strains was determined for 15 commonly used antibiotics. The phylogenetic analysis revealed that the isolates belonged to Alphaproteobacteria (3), Gammaproteobacteria (5), Actinobacteria (3), and Firmicutes (4) phyllum. The majority of the isolates (66%) produced simultaneously more than one enzyme. Hemolysis was produced by 46.6% of isolates, while DNase was produced by 33% of strains. On the other hand, 13% of strains produced lecithinase, gelatinase, cellulase, and lipase. No chitinase was produced by the isolated bacteria. In addition, 60% of isolates displayed antimicrobial activity against at least one pathogenic strain. All Ulva ohnoi-associated bacteria were resistant to at least seven commonly used antibiotics. These results highlighted the occurrence of several enzymatic activities within Ulva-associated bacteria that can have potential uses in the industrial sector.
... First report of Planomicrobium okeanokoites from Southern Hemisphere example, a bacterium associated with Ulva mutabilis is responsible for the development of blade morphology, its adhesiveness to the substratum, and growth [53]. This study may open a gateway for further research to know about the mode of interactions and how they affect the physiology and metabolism of each other. ...
Gram-positive, aerobic, motile, rod-shaped, mesophilic epiphytic bacterium Planomicrobium okeanokoites was isolated from the surface of endemic species Himantothallus grandifolius in Larsemann Hills, Eastern Antarctica. The diversity of epiphytic bacterial communities living on marine algae remains primarily unexplored; virtually no reports from Antarctic seaweeds. The present study used morpho-molecular approaches for the macroalgae and epiphytic bacterium characterization. Phylogenetic analysis was performed using mitochondrial genome encoded COX1 gene; chloroplast genome encodes rbcL; nuclear genome encoded large subunit ribosomal RNA gene (LSU rRNA) for Himantothallus grandifolius and ribosomal encoded 16S rRNA for Planomicrobium okeanokoites. Morphological and molecular data revealed that the isolate is identified as Himantothallus grandifolius, which belongs to Family Desmarestiaceae of Order Desmarestiales in Class Phaeophyceae showing 99.8% similarity to the sequences of Himantothallus grandifolius, from King George Island, Antarctica (HE866853). The isolated bacterial strain was identified on the basis of chemotaxonomic, morpho-phylogenetic, and biochemical assays. A phylogenetic study based on 16S rRNA gene sequences revealed that the epiphytic bacterial strain SLA-357 was closest related to the Planomicrobium okeanokoites showing 98.7% sequence similarity. The study revealed the first report of this species from the Southern Hemisphere to date. Also, there has been no report regarding the association between the Planomicrobium okeanokoites and Himantothallus grandifolius; however, there are some reports on this bacterium isolated from sediments, soils, and lakes from Northern Hemisphere. This study may open a gateway for further research to know about the mode of interactions and how they affect the physiology and metabolism of each other.
