Invasive seaweeds in rising temperatures: impacts and the role of acclimation and adaptation

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Publications

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

Integrating reproductive phenology in ecological niche models changed the predicted future ranges of a marine invader

Publication . Chefaoui, Rosa; Serebryakova, Alexandra; Engelen, Aschwin; Viard, Frédérique; Serrao, Ester

Aim Phenology of a wide diversity of organisms has a dependency on climate, usually with reproductive periods beginning earlier in the year and lasting longer at lower latitudes. Temperature and day length are known environmental drivers of the reproductive timing of many species. Hence, reproductive phenology is sensitive to warming and is important to be considered for reliable predictions of species distributions. This is particularly relevant for rapidly spreading non-indigenous species (NIS). In this study, we forecast the future ranges of a NIS, the seaweed Sargassum muticum, including its reproductive phenology. Location Coastal areas of the Northern Hemisphere (Pacific and Atlantic oceans). Methods We used ecological niche modelling to predict the distribution of S. muticum under two scenarios forecasting limited (RCP 2.6) and severe (RCP 8.5) future climate changes. We then refined our predictions with a hybrid model using sea surface temperature constraints on reproductive phenology. Results Under the most severe climate change scenario, we predicted northward expansions which may have significant ecological consequences for subarctic coastal ecosystems. However, in lower latitudes, habitats currently occupied by S. muticum will no longer be suitable, creating opportunities for substantial community changes. The temperature constraints imposed by the reproductive window were shown to restrict the modelled future species expansion strongly. Under the RCP 8.5 scenario, the total range area was expected to increase by 61.75% by 2100, but only by 1.63% when the reproductive temperature window was considered. Main conclusions Altogether these results exemplify the need to integrate phenology better to improve the prediction of future distributional shifts at local and regional scales.

2019-05Journal article

Open Access

Seaweed loads cause stronger bacterial community shifts in coastal lagoon sediments than nutrient loads

Publication . Aires, Tânia; Muyzer, Gerard; Serrao, Ester; Engelen, Aschwin

The input of nutrients from anthropogenic sources is the leading cause of coastal eutrophication and is usually coupled with algal/seaweed blooms. Effects may be magnified in semi-enclosed systems, such as highly productive coastal lagoon ecosystems. Eutrophication and seaweed blooms can lead to ecosystem disruption. Previous studies have considered only one of these factors, disregarding possible interactive effects and the effect of the blooming species' identity on sediment bacterial communities. We tested the effect of experimental nutrient loading and two common blooming seaweeds (Ulva rigida and Gracilaria vermiculophylla) in coastal lagoon sediments, on the structure of bacterial communities (using 16S rRNA amplicon sequencing) and corresponding putative functional potential (using PiCRUSt). At the Operational Taxonomic Unit (OTU) level, the addition of nutrients reduced bacterial community α-diversity and decreased the abundance of sulfate reducers (Desulfobacterales) compared to sulfur oxidizers/denitrifiers (Chromatiales and Campylobacterales), whereas this was not the case at the order level. Seaweed addition did not change bacterial α-diversity and the effect on community structure depended on the taxonomic level considered. The addition of Gracilaria increased the abundance of orders and OTUs involved in sulfate reduction and organic matter decomposition (Desulfobacterales, Bacteroidales, and Clostridiales, respectively), an effect which was also detected when only Ulva was added. Nutrients and the seaweeds combined only interacted for Ulva and nutrients, which increased known sulfide oxidizers and denitrifiers (order Campylobacterales). Seaweed enrichment affected putative functional profiles; a stronger increase of sulfur cycling KEGG pathways was assigned to nutrient-disturbed sediments, particularly with the seaweeds and especially Ulva. In contrast, nitrogen and sulfur cycle pathways showed a higher abundance of genes related to dissimilatory nitrate reduction to ammonium (DNRA) in Ulva+nutrients treatments. However, the other seaweed treatments increased the nitrogen fixation genes. Thiosulfate reduction, performed by sulfate-reducing bacteria, increased in seaweed treatments except when Ulva was combined with nutrients. In conclusion, the in situ addition of nutrients and the seaweeds to intertidal sediments affected the bacterial communities differently and independently. The predicted functional profile suggests a shift in relative abundances of putative pathways for nitrogen and sulfur cycles, in line with the taxonomic changes of the bacterial communities.

2019Journal article

Open Access

A genome-wide investigation of the worldwide invader Sargassum muticum shows high success albeit (almost) no genetic diversity

Publication . Le Cam, Sabrina; Daguin-Thiebaut, Claire; Bouchemousse, Sarah; Engelen, Aschwin; Mieszkowska, Nova; Viard, Frédérique

Twenty years of genetic studies of marine invaders have shown that successful invaders are often characterized by native and introduced populations displaying similar levels of genetic diversity. This pattern is presumably due to high propagule pressure and repeated introductions. The opposite pattern is reported in this study of the brown seaweed, Sargassum muticum, an emblematic species for circumglobal invasions. Albeit demonstrating polymorphism in the native range, microsatellites failed to detect any genetic variation over 1,269 individuals sampled from 46 locations over the Pacific-Atlantic introduction range. Single-nucleotide polymorphisms (SNPs) obtained from ddRAD sequencing revealed some genetic variation, but confirmed severe founder events in both the Pacific and Atlantic introduction ranges. Our study thus exemplifies the need for extreme caution in interpreting neutral genetic diversity as a proxy for invasive potential. Our results confirm a previously hypothesized transoceanic secondary introduction from NE Pacific to Europe. However, the SNP panel unexpectedly revealed two additional distinct genetic origins of introductions. Also, conversely to scenarios based on historical records, southern rather than northern NE Pacific populations could have seeded most of the European populations. Finally, the most recently introduced populations showed the lowest selfing rates, suggesting higher levels of recombination might be beneficial at the early stage of the introduction process (i.e., facilitating evolutionary novelties), whereas uniparental reproduction might be favored later in sustainably established populations (i.e., sustaining local adaptation).

2019-05Journal article

Open Access

Summer shifts of bacterial communities associated with the invasive brown seaweed Sargassum muticum are location and tissue dependent

Publication . Serebryakova, Alexandra; Aires, Tânia; Viard, Frédérique; Serrao, Ester; Engelen, Aschwin

Seaweed-associated microbiota experience spatial and temporal shifts in response to changing environmental conditions and seaweed physiology. These shifts may result in structural, functional and behavioral changes in the host with potential consequences for its fitness. They, thus, may help the host to adapt to changing environmental conditions. The current knowledge of seasonal variation of seaweed-associated microbiota is however still limited. In this study, we explored temporal and spatial variation of microbial communities associated with the invasive brown seaweed S. muticum. We sampled in northern and southern Portugal, in September, March and July-August (summer). In addition, as (pseudo-)perennial seaweeds display seasonal reproductive phenology, we sampled various parts of the individuals to disentangle the effect of temporal changes from those due to structural development variations. The diversity and structure of associated microbial communities were determined using next generation sequencing of the variable regions V5-7 of the 16S rDNA. We expected to find differentiation in associated microbial communities between regions and sampling months, but with differences depending on the seaweed structure examined. As expected, the study revealed substantial temporal shifts in S. muticum microbiome, for instance with large abundance of Rhodobacteraceae and Loktanella in September-March but prevalence of Pirellulales during the summer months. Variations between regions and tissues were also observed: in northern Portugal and on basal structures, bacterial diversity was higher as compared to the South and apical parts. All examined seaweed structures showed temporal differences in associated microbial community structure over time, except for holdfasts between September and March. Bacteria contributing to these changes varied spatially. Conversely to all other structures, the holdfast also did not show differences in associated community structure between southern and northern regions. Our study highlights the importance of structural microscale differentiations within seaweeds hosts with regard to their associated microbial communities and their importance across temporal and spatial dimensions.

2018Journal article

Open Access