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Diversity of the holopelagic Sargassum microbiome from the Great Atlantic Sargassum Belt to coastal stranding locations

Publication . Theirlynck, Tom; Mendonça, Inara Regina W.; Engelen, Aschwin; Bolhuis, Henk; Collado-Vides, Ligia; van Tussenbroek, Brigitta I.; García-Sánchez, Marta; Zettler, Erik; Muyzer, Gerard; Amaral-Zettler, Linda

The holopelagic brown macroalgae Sargassum natans and Sargassum fluitans form essential habitats for attached and mobile fauna which contributes to a unique biodiversity in the Atlantic Ocean. However, holopelagic Sargassum natans (genotype I & VIII) and Sargassum fluitans (genotype III) have begun forming large accumu-lations with subsequent strandings on the western coast of Africa, the Caribbean and northern Brazil, threatening local biodiversity of coastal ecosystems and triggering economic losses. Moreover, stranded masses of hol-opelagic Sargassum may introduce or facilitate growth of bacteria that are not normally abundant in coastal regions where Sargassum is washing ashore. Hitherto, it is not clear how the holopelagic Sargassum microbiome varies across its growing biogeographic range and what factors drive the microbial composition. We determined the microbiome associated with holopelagic Sargassum from the Great Atlantic Sargassum Belt to coastal stranding sites in Mexico and Florida. We characterized the Sargassum microbiome via amplicon sequencing of the 16S V4 region hypervariable region of the rRNA gene. The microbial community of holopelagic Sargassum was mainly composed of photo(hetero)trophs, organic matter degraders and potentially pathogenic bacteria from the Pseudomonadaceae, Rhodobacteraceae and Vibrionaceae. Sargassum genotypes S. natans I, S. natans VIII and S. fluitans III contained similar microbial families, but relative abundances and diversity varied. LEfSE analyses further indicated biomarker genera that were indicative of Sargassum S. natans I/VIII and S. fluitans III. The holopelagic Sargassum microbiome showed biogeographic patterning with high relative abundances of Vibrio spp., but additional work is required to determine whether that represents health risks in coastal environments. Our study informs coastal management policy, where the adverse sanitary effects of stranded Sargassum might impact the health of coastal ecosystems.

2023Journal article

Open access

Taxonomic insights into caulerpa (Bryopsidales, Chlorophyta) species in French Polynesia: confirmation of 13 species and reinstatement of c. pickeringii Harvey & Bailey

Publication . Lagourgue, Laura; Sauvage, Thomas; Zubia, Mayalen; Draisma, Stefano G. A.; Vieira, António Carlos; Engelen, Aschwin; Payri, Claude E.

Caulerpa J.V. Lamouroux is a genus of green macroalgae belonging to the family Caulerpaceae in the order Bryopsidales. The genus comprises 104 currently accepted species, of which 51 have been recorded from Pacific Islands. Among these islands, French Polynesia is found in the middle of the South Pacific Ocean and includes five archipelagos (i.e., the Austral, Gambier, Marquesas, Society, and Tuamotu Islands) where seaweed inventories have reported a total of 16 Caulerpa species so far based on morphology. Here, based on a sampling covering the five archipelagos of French Polynesia, we attempt to (i) verify the taxonomy of Caulerpa species present in these regions based on phylogeny, (ii) describe in more detail the specific diversity between the five archipelagos, and (iii) provide a morphological identification tool for these species. We successfully obtained 134 new tufA sequences for phylogenetic analyses, which corresponded to 13 species. We propose to resurrect C. pickeringii Harvey & Bailey for representatives of C. webbiana var. pickeringii and classify it in the Caulerpa subgenus Araucarioideae. We also transfer C. seuratii to C. pickeringii based on genetic results. A new morphological identification key is provided as well as an updated distribution of Caulerpa species across French Polynesia.

2024Journal article

Open access

Regional microbiome differentiation of the invasive Sargassum muticum (Fucales, Phaeophyceae) follows the generalist host hypothesis across the North East Atlantic

Publication . Aires, Tânia; Kläui, Anita; Hillebrand Engelen, Aschwin

Over 90% of introduced marine species are seaweeds. Seaweeds rely on their microbiome for host settlement, nutrition, development and health. As such, it is likely that microbiomes are involved in seaweed invasions. Sargassum muticum, indigenous to Southeast Asia, inhabits the North-east Atlantic from Norway to Morocco. This is the only known successful case of a non-clonal marine invader with almost no genetic variation over its large NE Atlantic introduced range. This makes it a very interesting model to study an invasive seaweeds microbiome, as it practically uncouples host genetic variation from microbiome variation. Associated bacteria potentially contribute to the plasticity and acclimation of S. muticum leading to its success over the last 50 years. Dispersing host organisms can either bring their acquired microbes along or obtain new ones locally, following the mutualist and generalist host hypothesis, respectively. We used partial 16S rRNA gene amplicon sequencing to characterize the total and core microbiome across S. muticum structures/tissues from five NE Atlantic regions, from Norway to Morocco, covering over 30 degrees of latitude. In contrast to host genotypes, highly diverse, regional, total and core microbiomes, with differentiation levels depending on tissue, bacterial community structure were detected. Atlantic S. muticum follows the generalist host hypothesis, possibly recruiting a new microbiome in each new region. This host promiscuity may promote the invasiveness of S. muticum. Diversity was lower in the young/annual tissues compared with the older tissues for the total bacterial community, suggesting that these are mostly transitory bacteria accumulating over time in the older parts. The total core microbiome included 10 OTUs, representing dominant community members commonly found in other seaweeds' cores. The core Granulosicoccus OTU followed a clear regional pattern where northern and southern regions clustered differentially, suggesting a regional signature even at an OTU level.

2022Journal article

Restricted access

Macroalgal microbiomes unveil a valuable genetic resource for halogen metabolism

Publication . Lavecchia, Anna; Fosso, Bruno; Engelen, Aschwin; Borin, Sara; Manzari, Caterina; Picardi, Ernesto; Pesole, Graziano; Placido, Antonio

Background Macroalgae, especially reds (Rhodophyta Division) and browns (Phaeophyta Division), are known for producing various halogenated compounds. Yet, the reasons underlying their production and the fate of these metabolites remain largely unknown. Some theories suggest their potential antimicrobial activity and involvement in interactions between macroalgae and prokaryotes. However, detailed investigations are currently missing on how the genetic information of prokaryotic communities associated with macroalgae may influence the fate of organohalogenated molecules. Results To address this challenge, we created a specialized dataset containing 161 enzymes, each with a complete enzyme commission number, known to be involved in halogen metabolism. This dataset served as a reference to annotate the corresponding genes encoded in both the metagenomic contigs and 98 metagenome-assembled genomes (MAGs) obtained from the microbiome of 2 red (Sphaerococcus coronopifolius and Asparagopsis taxiformis) and 1 brown (Halopteris scoparia) macroalgae. We detected many dehalogenation-related genes, particularly those with hydrolytic functions, suggesting their potential involvement in the degradation of a wide spectrum of halocarbons and haloaromatic molecules, including anthropogenic compounds. We uncovered an array of degradative gene functions within MAGs, spanning various bacterial orders such as Rhodobacterales, Rhizobiales, Caulobacterales, Geminicoccales, Sphingomonadales, Granulosicoccales, Microtrichales, and Pseudomonadales. Less abundant than degradative functions, we also uncovered genes associated with the biosynthesis of halogenated antimicrobial compounds and metabolites. Conclusion The functional data provided here contribute to understanding the still largely unexplored role of unknown prokaryotes. These findings support the hypothesis that macroalgae function as holobionts, where the metabolism of halogenated compounds might play a role in symbiogenesis and act as a possible defense mechanism against environmental chemical stressors. Furthermore, bacterial groups, previously never connected with organohalogen metabolism, e.g., Caulobacterales, Geminicoccales, Granulosicoccales, and Microtrichales, functionally characterized through MAGs reconstruction, revealed a biotechnologically relevant gene content, useful in synthetic biology, and bioprospecting applications.

2024-03-07Journal article

Open access

Synchronized broadcast spawning by six invertebrates (Echinodermata and Mollusca) in the north-western Red Sea

Publication . Webb, Alice E.; Engelen, Aschwin; Bouwmeester, Jessica; van Dijk, Inge; Geerken, Esmee; Lattaud, Julie; Engelen, Dario; de Bakker, Bernadette S.; de Bakker, Didier M.

On the evenings of June 11 and 12, 2019, 5 and 6 days before full moon, broadcast spawning by four echinoderm species and two mollusc species was observed on the Marsa Shagra reef, Egypt (25° 14′ 44.2" N, 34° 47′ 49.0" E). Water temperature was 28 °C and the invertebrates were observed at 2–8 m depth. The sightings included a single basket star Astroboa nuda (Lyman 1874), 2 large Tectus dentatus (Forskal 1775) sea snails, 14 individuals of the Leiaster cf. leachi (Gray 1840) sea star and 1 Mithrodia clavigera (Lamarck 1816) sea star, 3 Pearsonothuria graefei (Semper 1868) sea cucumbers, and 2 giant clams, Tridacna maxima (Röding 1798). The observations presented here provide relevant information on broadcast spawning of non-coral invertebrate taxa in the Red Sea, where spawning is considerably less well documented than in other tropical geographical regions such as the Indo-Pacifc and Caribbean.

2021-04Journal article

Open access