Marine macrophytes holobionts: Acclimation and adaptation mechanisms across oceans in a global change scenario

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Publications

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

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eDNA metabarcoding for diet analyses of green sea turtles (Chelonia mydas)

Publication . Díaz-Abad, Lucía; Bacco-Mannina, Natassia; Madeira, Fernando Miguel; Neiva, J.; Aires, Tania; Serrao, Ester; Regalla, Aissa; Patrício, Ana R.; Rodrigues Frade, Pedro

Understanding sea turtle diets can help conservation planning, but their trophic ecology is complex due to life history characteristics such as ontogenetic shifts and large foraging ranges. Studying sea turtle diet is challenging, particularly where ecological foraging observations are not possible. Here, we test a new minimally invasive method for the identifcation of diet items in sea turtles. We fngerprinted diet content using DNA from esophageal and cloacal swab samples by metabarcoding the 18S rRNA gene. This approach was tested on samples collected from green turtles (Chelonia mydas) from a juvenile foraging aggregation in the Bijagós archipelago in Guinea-Bissau. Esophagus samples (n=6) exhibited a higher dietary richness (11±5 amplicon sequence variants (ASVs) per sample; average±SD) than cloacal ones (n=5; 8±2 ASVs). Overall, the diet was dominated by red macroalgae (Rhodophyta; 48.2±16.3% of all ASVs), with the main food item in the esophagus and cloaca being a red alga belonging to the Rhodymeniophycidae subclass (35.1±27.2%), followed by diatoms (Bacillariophyceae; 7.5±7.3%), which were presumably consumed incidentally. Seagrass and some invertebrates were also present. Feeding on red algae was corroborated by feld observations and barcoding of food items available in the benthic habitat, validating the approach for identifying diet content. We conclude that identifcation of food items using metabarcoding of esophageal swabs is useful for a better understanding of the relationships between the feeding behavior of sea turtles and their environment.

2021Journal article

Open Access

Acidification increases abundances of Vibrionales and Planctomycetia associated to a seaweed-grazer system: potential consequences for disease and prey digestion efficiency

Publication . Aires, Tânia; Serebryakova, Alexandra; Viard, Frederique; Serrao, Ester A.; Engelen, Aschwin H.

Ocean acidification significantly affects marine organisms in several ways, with complex interactions. Seaweeds might benefit from rising CO2 through increased photosynthesis and carbon acquisition, with subsequent higher growth rates. However, changes in seaweed chemistry due to increased CO2 may change the nutritional quality of tissue for grazers. In addition, organisms live in close association with a diverse microbiota, which can also be influenced by environmental changes, with feedback effects. As gut microbiomes are often linked to diet, changes in seaweed characteristics and associated microbiome can affect the gut microbiome of the grazer, with possible fitness consequences. In this study, we experimentally investigated the effects of acidification on the microbiome of the invasive brown seaweed Sargassum muticum and a native isopod consumer Synisoma nadejda. Both were exposed to ambient CO2 conditions (380 ppm, pH 8.16) and an acidification treatment (1,000 ppm, pH 7.86) for three weeks. Microbiome diversity and composition were determined using high-throughput sequencing of the variable regions V5-7 of 16S rRNA. We anticipated that as a result of acidification, the seaweed-associated bacterial community would change, leading to further changes in the gut microbiome of grazers. However, no significant effects of elevated CO2 on the overall bacterial community structure and composition were revealed in the seaweed. In contrast, significant changes were observed in the bacterial community of the grazer gut. Although the bacterial community of S. muticum as whole did not change, Oceanospirillales and Vibrionales (mainly Pseudoalteromonas) significantly increased their abundance in acidified conditions. The former, which uses organic matter compounds as its main source, may have opportunistically taken advantage of the possible increase of the C/N ratio in the seaweed under acidified conditions. Pseudoalteromonas, commonly associated to diseased seaweeds, suggesting that acidification may facilitate opportunistic/pathogenic bacteria. In the gut of S. nadejda, the bacterial genus Planctomycetia increased abundance under elevated CO2. This shift might be associated to changes in food (S. muticum) quality under acidification. Planctomycetia are slow-acting decomposers of algal polymers that could be providing the isopod with an elevated algal digestion and availability of inorganic compounds to compensate the shifted C/N ratio under acidification in their food. In conclusion, our results indicate that even after only three weeks of acidified conditions, bacterial communities associated to ungrazed seaweed and to an isopod grazer show specific, differential shifts in associated bacterial community. These have potential consequences for seaweed health (as shown in corals) and isopod food digestion. The observed changes in the gut microbiome of the grazer seem to reflect changes in the seaweed chemistry rather than its microbial composition.

2018-03Journal article

Open Access

Microbial surface biofilm responds to the growth-reproduction-senescence cycle of the dominant coral reef macroalgae Sargassum spp.

Publication . Glasl, Bettina; Haskell, Jasmine B.; Aires, Tania; Serrao, Ester; Bourne, David G.; Webster, Nicole S.; Frade, Pedro Rodrigues

Macroalgae play an intricate role in microbial-mediated coral reef degradation processes due to the release of dissolved nutrients. However, temporal variabilities of macroalgal surface biofilms and their implication on the wider reef system remain poorly characterized. Here, we study the microbial biofilm of the dominant reef macroalgae Sargassum over a period of one year at an inshore Great Barrier Reef site (Magnetic Island, Australia). Monthly sampling of the Sargassum biofilm links the temporal taxonomic and putative functional metabolic microbiome changes, examined using 16S rRNA gene amplicon and metagenomic sequencing, to the pronounced growth-reproduction-senescence cycle of the host. Overall, the macroalgal biofilm was dominated by the heterotrophic phyla Firmicutes (35% ± 5.9% SD) and Bacteroidetes (12% ± 0.6% SD); their relative abundance ratio shifted significantly along the annual growth-reproduction-senescence cycle of Sargassum. For example, Firmicutes were 1.7 to 3.9 times more abundant during host growth and reproduction cycles than Bacteroidetes. Both phyla varied in their carbohydrate degradation capabilities; hence, temporal fluctuations in the carbohydrate availability are potentially linked to the observed shift. Dominant heterotrophic macroalgal biofilm members, such as Firmicutes and Bacteroidetes, are implicated in exacerbating or ameliorating the release of dissolved nutrients into the ambient environment, though their contribution to microbial-mediated reef degradation processes remains to be determined.

2021-11-06Journal article

Open Access

Impact of persistently high sea surface temperatures on the rhizobiomes of Zostera marina in a Baltic Sea benthocosms

Publication . Cúcio, Catarina; Brakel, Janina; Weinberger, Florian; Wahl, Martin; Teles, Ana; Muyzer, Gerard; Aires, Tania; Engelen, Aschwin

Persistently high marine temperatures are escalating and threating marine biodiversity. The Baltic Sea, warming faster than other seas, is a good model to study the impact of increasing sea surface temperatures. Zostera marina, a key player in the Baltic ecosystem, faces susceptibility to disturbances, especially under chronic high temperatures. Despite the increasing number of studies on the impact of global warming on seagrasses, little attention has been paid to the role of the holobiont. Using an outdoor benthocosm to replicate near-natural conditions, this study explores the repercussions of persistent warming on the microbiome of Z. marina and its implications for holobiont function. Results show that both seasonal warming and chronic warming, impact Z. marina roots and sediment microbiome. Compared with roots, sediments demonstrate higher diversity and stability throughout the study, but temperature effects manifest earlier in both compartments, possibly linked to premature Z. marina die-offs under chronic warming. Shifts in microbial composition, such as an increase in organic matter-degrading and sulfur-related bacteria, accompany chronic warming. A higher ratio of sulfate-reducing bacteria compared to sulfide oxidizers was found in the warming treatment which may result in the collapse of the seagrasses, due to toxic levels of sulfide. Differentiating predicted pathways for warmest temperatures were related to sulfur and nitrogen cycles, suggest an increase of the microbial metabolism, and possible seagrass protection strategies through the production of isoprene. These structural and compositional variations in the associated microbiome offer early insights into the ecological status of seagrasses. Certain taxa/genes/pathways may serve as markers for specific stresses. Monitoring programs should integrate this aspect to identify early indicators of seagrass health. Understanding microbiome changes under stress is crucial for the use of potential probiotic taxa to mitigate climate change effects. Broader-scale examination of seagrass-microorganism interactions is needed to leverage knowledge on host-microbe interactions in seagrasses.

2024-05Journal article

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