Summer shifts of bacterial communities associated with the invasive brown seaweed Sargassum muticum are location and tissue dependent.
ABSTRACT: 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.
Project description: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.
Project description:Brown seaweeds are known to present components with appealing bioactive properties eliciting great interest for industrial applications. However, their lipid content is generally disregarded beyond their fatty acid (FA) composition. This study thoroughly characterized the lipid profile of two brown seaweeds collected from Portuguese coast, the native Bifurcaria bifurcata and the invasive Sargassum muticum species, and bioprospecting for antioxidant activity. An integrated state-of-the-art approach including gas chromatography-mass spectrometry (GC-MS) and liquid chromatography-mass spectrometry (HILIC-ESI-MS/MS), allowed a comprehensive picture of FA and polar lipid content. Polar lipid profile of B. bifurcata and S. muticum included 143 and 217 lipid species respectively, distributed between glycolipids, phospholipids, and betaine lipids. Some of the lipid species found have been assigned biological activity and contain of n-3 and n-6 FA. Sargassum muticum presented the highest n-3 FA content. Low concentrations of extracts of both seaweeds displayed antioxidant activity, with S. muticum presenting more promising results. These findings contribute to the nutritional and industrial exploitation of both seaweeds, highlighting their relevance as viable sources of bioactive and added-value compounds. Sargassum muticum presented interesting lipid composition and bioactivity, which may represent an accessible opportunity for the exploitation of this invasive seaweed, especially taking advantage of Sargassum blooms.
Project description:The impact of invasive species on recipient communities can vary with environmental context and across levels of biological complexity. We investigated how an established invasive seaweed species affected the biomass, eco-physiology, carbon and nitrogen storage capacity of native seaweeds at sites with a different environmental setting due to a persistent upwelling in northern Spain. We removed the invasive Japanese wireweed Sargassum muticum from intertidal rock pools once every month during a one-year period and used an in-situ stable isotope pulse-chase labeling to estimate gross primary production (GPP), nitrogen uptake rate, 13C-carbon and 15N-nitrogen storage capacities. Following the addition of 13C-enriched bicarbonate and 15N-enriched nitrate to the seawater in the rock pools during the period of the low tide, we sampled macroalgal thalli at incoming tide to determine label uptake rate. After four days, we sampled macroalgal assemblages to determine both label storage capacity and biomass. After one year of removal there was no change in the macroalgal assemblage. However, both the GPP and 13C-carbon storage capacity were higher in the turf-forming Corallina spp. and, sometimes, in the canopy-forming Bifurcaria bifurcata. Nitrogen uptake rate followed similar, but more variable results. Although S. muticum inhibited carbon storage capacity of native species, the assemblage-level 13C-carbon storage was similar in the S. muticum-removed and control rock pools because the presence of the invasive species compensated for the functional loss of native species, particularly at sites where it was most abundant. No obvious effects were observed in relation to the environmental setting. Overall, the effect of the invasive S. muticum on carbon flow appeared to be mediated both by the effects on resource-use efficiency of native species and by its own biomass. Integrating physiological and assemblage-level responses can provide a broad understanding of how invasive species affect recipient communities and ecosystem functioning.
Project description:Interrelations between epiphytic bacteria and macroalgae are multifaceted and complicated, though little is known about the community structure, interaction and functions of those epiphytic bacteria. This study comprehensively characterized the epiphytic bacterial communities associated with eight different common seaweeds collected from a rocky intertidal zone on the Indian Ocean at Cape Vidal, South Africa. High-throughput sequencing analyses indicated that seaweed-associated bacterial communities were dominated by the phyla Proteobacteria, Bacteroidetes, Firmicutes, Cyanobacteria, Planctomycetes, Actinobacteria and Verrucomicrobia. Energy-dispersive X-ray (EDX) analysis showed the presence of elemental composition in the surface of examined seaweeds, in varying concentrations. Cluster analysis showed that bacterial communities of brown seaweeds (SW2 and SW4) were closely resembled those of green seaweeds (SW1) and red seaweeds (SW7) while those of brown seaweeds formed a separate branch. Predicted functional capabilities of epiphytic bacteria using PICRUSt analysis revealed abundance of genes related to metabolic and biosynthetic activities. Further important identified functional interactions included genes for bacterial chemotaxis, which could be responsible for the observed association and network of elemental-microbes interaction. The study concludes that the diversity of epiphytic bacteria on seaweed surfaces is greatly influenced by algal organic exudates as well as elemental deposits on their surfaces, which triggers chemotaxis responses from epiphytic bacteria with the requisite genes to metabolise those substrates.
Project description: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 ?-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 ?-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.
Project description:Seagrasses are important habitat-formers and ecosystem engineers that are under threat from bloom-forming seaweeds. These seaweeds have been suggested to outcompete the seagrasses, particularly when facilitated by eutrophication, causing regime shifts where green meadows and clear waters are replaced with unstable sediments, turbid waters, hypoxia, and poor habitat conditions for fishes and invertebrates. Understanding the situations under which seaweeds impact seagrasses on local patch scales can help proactive management and prevent losses at greater scales. Here, we provide a quantitative review of available published manipulative experiments (all conducted at the patch-scale), to test which attributes of seaweeds and seagrasses (e.g., their abundances, sizes, morphology, taxonomy, attachment type, or origin) influence impacts. Weighted and unweighted meta-analyses (Hedges d metric) of 59 experiments showed generally high variability in attribute-impact relationships. Our main significant findings were that (a) abundant seaweeds had stronger negative impacts on seagrasses than sparse seaweeds, (b) unattached and epiphytic seaweeds had stronger impacts than 'rooted' seaweeds, and (c) small seagrass species were more susceptible than larger species. Findings (a) and (c) were rather intuitive. It was more surprising that 'rooted' seaweeds had comparatively small impacts, particularly given that this category included the infamous invasive Caulerpa species. This result may reflect that seaweed biomass and/or shading and metabolic by-products like anoxia and sulphides could be lower for rooted seaweeds. In conclusion, our results represent simple and robust first-order generalities about seaweed impacts on seagrasses. This review also documented a limited number of primary studies. We therefore identified major knowledge gaps that need to be addressed before general predictive models on seaweed-seagrass interactions can be build, in order to effectively protect seagrass habitats from detrimental competition from seaweeds.
Project description:There is an increasing need to identify alternative feeds for livestock that do not compete with foods for humans. Seaweed might provide such a resource, but there is limited information available on its value as an animal feed. Here we use a multi-omics approach to investigate the value of two brown seaweeds, Ascophyllum nodosum (ASC) and Laminaria digitata (LAM), as alternative feeds for ruminants. These seaweeds were supplemented at 5% inclusion rate into a control diet (CON) in a rumen simulation fermenter. The seaweeds had no substantial effect on rumen fermentation, feed degradability or methane emissions. Concentrations of total bacteria, anaerobic fungi, biodiversity indices and abundances of the main bacterial and methanogen genera were also unaffected. However, species-specific effects of brown seaweed on the rumen function were noted: ASC promoted a substantial decrease in N degradability (-24%) due to its high phlorotannins content. Canonical correspondence analysis of the bacterial community revealed that low N availability led to a change in the structure of the bacterial community. ASC also decreased the concentration of Escherichia coli O157:H7 post-inoculation. In contrast, LAM which has a much lower phlorotannin content did not cause detrimental effects on N degradability nor modified the structure of the bacterial community in comparison to CON. This adaptation of the microbial community to LAM diets led to a greater microbial ability to digest xylan (+70%) and carboxy-methyl-cellulose (+41%). These differences among brown seaweeds resulted in greater microbial protein synthesis (+15%) and non-ammonia N flow (+11%) in LAM than in ASC diets and thus should led to a greater amino acid supply to the intestine of the animal. In conclusion, it was demonstrated that incorporation of brown seaweed into the diet can be considered as a suitable nutritional strategy for ruminants; however, special care must be taken with those seaweeds with high phlorotannin concentrations to prevent detrimental effects on N metabolism. This study highlights the value of combining fermentation and enzyme activity data with molecular characterization of the rumen microbiome in evaluating novel feeds for ruminants. Further experiments are required to determine the maximum seaweed inclusion rate tolerated by rumen microbes.
Project description:Seaweed-dominated coral reefs are becoming increasingly common as environmental conditions shift away from those required by corals and toward those ideal for rampant seaweed growth. How coral-associated organisms respond to seaweed will not only impact their fate following environmental change but potentially also the trajectories of the coral communities on which they rely. However, behavioral responses by coral-associated organisms to seaweeds are poorly understood. This study examined interactions between a guild of obligate and opportunistic coral-feeding butterflyfishes (Chaetodontidae) and scleractinian corals to determine whether fishes continue to interact with corals in contact with seaweed or if they are avoided. Under natural conditions, all species interacted almost exclusively with seaweed-free corals. In a controlled patch reef experiment, fishes avoided corals in physical contact with seaweed, irrespective of dietary preferences. When visual seaweed cues were removed, butterflyfish continued to avoid corals that had been in contact with the allelopathic Galaxaura filamentosa, suggesting that chemical cues produced by coral-seaweed interactions are repellent. These findings suggest that, due to deleterious visual and chemical cues produced by coral-seaweed interactions, coral-associated organisms may struggle to locate resources as seaweed-free corals decline in abundance.
Project description:The establishment of epibacterial communities is fundamental to seaweed health and fitness, in modulating ecological interactions and may also facilitate adaptation to new environments. Abiotic factors like salinity can determine bacterial abundance, growth and community composition. However, influence of salinity as a driver of epibacterial community composition (until species level) has not been investigated for seaweeds and especially under long time scales. We also do not know how abiotic stressors may influence the 'core' bacterial species of seaweeds. Following an initial (immediately after field collection) sampling of epibacterial community of an invasive red seaweed Agarophyton vermicullophylum, we conducted a long term mesocosm experiment for 5 months, to examine the influence of three different salinities (low, medium and high) at two different time points (3 months after start of experiment and 5 months, i.e., at the end of experiment) on the epibacterial community richness and composition of Agarophyton. Metagenomic sequencing showed that epibacterial communities changed significantly according to salinity and time points sampled. Epibacterial richness was significantly different between low and high salinities at both time points. Epibacterial richness also varied significantly between 3 months (after start of experiment) and 5 months (end of experiment) within low, medium and high salinity level. Irrespective of salinity levels and time points sampled 727 taxa consistently appeared in all Agarophyton samples hinting at the presence of core bacterial species on the surface of the alga. Our results indicate that both salinity and time can be major driving forces in structuring epibacterial communities of seaweeds with respect to richness and ?-diversity. We highlight the necessity of conducting long term experiments allowing us to detect and understand epibacterial succession over time on seaweeds.
Project description:A variety of different symbiotic microbial communities are harbored on the surface of seaweeds, the interactions of which depend upon nutritional exchanges between the microbes and the hosts. Metabolomic profiling is able to provide a comprehensive and unbiased snapshot of the metabolites associated with seaweed-microbe interactions. In this study, the relationships between phycosphere bacteria and the red alga Pyropia haitanensis were investigated on a metabolomic basis using gas chromatography-mass spectrometry, and the pathways of the interactions between the seaweed and its associated phycospheric microbes were revealed. Bacillus sp. WPySW2, one bacterial species isolated from the phycosphere of Pyropia species, had a significant influence on the metabolomic profile of the algae. Some of the intracellular metabolites such as phenylalanine, leucine, isoleucine, valine, proline, tyrosine, threonine, octadecanoic acid, hexadecanoic acid, and citric acid were downregulated in the thalli of P. haitanensis when it was co-cultured with Bacillus sp. WPySW2, while several special metabolites including melibiose, serine, glycerol-3-phosphate, galactosylglycerol, and alanine were upregulated. The results demonstrated that P. haitanensis grew better when it was co-cultured with Bacillus sp. WPySW2 at 20 °C. In conclusion, several main intracellular metabolites were downregulated and upregulated, which might have facilitated bacterial colonization.