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- Regional microbiome differentiation of the invasive Sargassum muticum (Fucales, Phaeophyceae) follows the generalist host hypothesis across the North East AtlanticPublication . Aires, Tânia; Kläui, Anita; Hillebrand Engelen, AschwinOver 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.
- Host differentiation and compartmentalization of microbial communities in the Azooxanthellate Cupcorals Tubastrea coccinea and Rhizopsammia goesi in the CaribbeanPublication . Engelen, Aschwin; Aires, Tânia; Vermeij, Mark J. A.; Herndl, Gerhard J.; Serrao, Ester; Rodrigues Frade, PedroWe investigated the microbial communities associated with surface mucus layer, tissue, and gastrovascular cavity of two azooxanthellate Caribbean cup corals (Tubastrea coccinea and Rhizopsammia goesi) to explore potential differences in microbial community composition within and among these azooxanthellate scleractinian corals. Using next-generation sequencing of the V3-V6 region of the 16S rRNA gene we found that while alpha-diversity was overall very similar, the relative abundance of microbial taxa differed between host species and among locations within a polyp (i.e., compartments). The interspecific differentiation of microbial assemblages is only challenged by the relatively high similarity among mucus samples of both species. This suggests a stronger signal of the surrounding environment and weaker host control over the mucus compartment compared with the tissue and gastrovascular cavity. T. coccinea harbored four indicator OTUs (including a Pseudoalteromonas species, an unidentified Gammaproteobacteria, an unidentified OTU in the family Comamonadaceae and one in the genus Burkholderia). The single indicator for R. goesi was another undetermined OTU in the Comamonadaceae. The microbial communities of the gastrovascular cavity and the mucus overlapped substantially in indicator OTUs. None of these were exclusive of the gastrovascular cavity or mucus, while an OTU of the order Thiohalorhabdales occurred uniquely in the tissue. In contrast to the gastrovascular cavity and mucus, the tissue of both coral species was rich in chloroplasts of different algal taxa (mainly Ulvophyceae and Stramenopiles), and an OTU of the genus Roseivirga (family Flammeovirgaceae). The two coral species shared most indicator OTUs for microbial communities residing in their mucus and tissue, but not in their gastrovascular cavities. However, Endozoicomonadaceae occurred in the tissue of both coral species. The genus Pseudomonas was found in R. goesi but was virtually absent in .T coccinea. This study demonstrates the influence of coral compartments and species identities on the composition of microbial communities associated with azooxanthellate cup corals and emphasizes the important effects of within-polyp microhabitats in structuring the coral microbiome.
- The effects of grazing on the microbiome of an invasive brown seaweed (Sargassum Muticum)Publication . Aires, Tânia; Muyzer, G.; EA, Serrao; Engelen, AH
- Seaweed loads cause stronger bacterial community shifts in coastal lagoon sediments than nutrient loadsPublication . Aires, Tânia; Muyzer, Gerard; Serrao, Ester; Engelen, AschwinThe 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.
- Invasion is a community affair: clandestine followers in the bacterial community associated to green algae, Caulerpa racemosa, track the invasion sourcePublication . Aires, Tânia; Serrão, Ester; Kendrick, G.; Duarte, C. M.; ARNAUD-HAOND, SophieBiological invasions rank amongst the most deleterious components of global change inducing alterations from genes to ecosystems. The genetic characteristics of introduced pools of individuals greatly influence the capacity of introduced species to establish and expand. The recently demonstrated heritability of microbial communities associated to individual genotypes of primary producers makes them a potentially essential element of the evolution and adaptability of their hosts. Here, we characterized the bacterial communities associated to native and non-native populations of the marine green macroalga Caulerpa racemosa through pyrosequencing, and explored their potential role on the strikingly invasive trajectory of their host in the Mediterranean. The similarity of endophytic bacterial communities from the native Australian range and several Mediterranean locations confirmed the origin of invasion and revealed distinct communities associated to a second Mediterranean variety of C. racemosa long reported in the Mediterranean. Comparative analysis of these two groups demonstrated the stability of the composition of bacterial communities through the successive steps of introduction and invasion and suggested the vertical transmission of some major bacterial OTUs. Indirect inferences on the taxonomic identity and associated metabolism of bacterial lineages showed a striking consistency with sediment upheaval conditions associated to the expansion of their invasive host and to the decline of native species. These results demonstrate that bacterial communities can be an effective tracer of the origin of invasion and support their potential role in their eukaryotic host’s adaptation to new environments. They put forward the critical need to consider the 'meta-organism' encompassing both the host and associated micro-organisms, to unravel the origins, causes and mechanisms underlying biological invasions.
- Expressed sequence tags from heat-shocked seagrass Zostera noltii (Hornemann) from its southern distribution rangePublication . Massa, S. I.; Pearson, G. A.; Aires, Tânia; Kube, M.; Olsen, J. L.; Reinhardt, Richard; Serrão, Ester; ARNAUD-HAOND, SophiePredicted global climate change threatens the distributional ranges of species worldwide. We identified genes expressed in the intertidal seagrass Zostera noltii during recovery from a simulated low tide heat-shock exposure. Five Expressed Sequence Tag (EST) libraries were compared, corresponding to four recovery times following sub-lethal temperature stress, and a non-stressed control. We sequenced and analyzed 7009 sequence reads from 30 min, 2 h, 4 h and 24 h after the beginning of the heat-shock (AHS), and 1585 from the control library, for a total of 8594 sequence reads. Among 51 Tentative UniGenes (TUGs) exhibiting significantly different expression between libraries, 19 (37.3%) were identified as ‘molecular chaperones’ and were over-expressed following heat-shock, while 12 (23.5%) were ‘photosynthesis TUGs’ generally under-expressed in heat-shocked plants. A time course analysis of expression showed a rapid increase in expression of the molecular chaperone class, most of which were heat-shock proteins; which increased from 2 sequence reads in the control library to almost 230 in the 30 min AHS library, followed by a slow decrease during further recovery. In contrast, ‘photosynthesis TUGs’ were under-expressed 30 min AHS compared with the control library, and declined progressively with recovery time in the stress libraries, with a total of 29 sequence reads 24 h AHS, compared with 125 in the control. A total of 4734 TUGs were screened for EST-Single Sequence Repeats (EST-SSRs) and 86 microsatellites were identified.► Response to heat stress is very fast but gene expression returns to normal after 24 h. ► Photosynthesis-related genes were under-expressed after heat-shock. ► Heat-shock caused a quick rise in heat shock proteins and molecular chaperone expression.
- Glacial vicariance drives phylogeographic diversification in the amphi-boreal kelp Saccharina latissimaPublication . MACHADO, JOÃO NEIVA; Paulino, Cristina; Nielsen, Mette M.; Krause-Jensen, Dorte; Saunders, Gary W.; Assis, Jorge; Barbara, Ignacio; Tamigneaux, Eric; Gouveia, Licínia; Aires, Tânia; Marba, Nuria; Bruhn, Annette; Pearson, Gareth; Serrao, Ester A.Glacial vicariance is regarded as one of the most prevalent drivers of phylogeographic structure and speciation among high-latitude organisms, but direct links between ice advances and range fragmentation have been more difficult to establish in marine than in terrestrial systems. Here we investigate the evolution of largely disjunct (and potentially reproductively isolated) phylogeographic lineages within the amphi-boreal kelp Saccharina latissima s.l. Using molecular data (COI, microsatellites) we confirm that S. latissima comprises also the NE Pacific S. cichorioides complex and is composed of divergent lineages with limited range overlap and genetic admixture. Only a few genetic hybrids were detected throughout a Canadian Arctic/NW Greenland contact zone. The degree of genetic differentiation and sympatric isolation of phylogroups suggest that S. latissima s.l. represents a complex of incipient species. Phylogroup distributions compared with paleo-environmental reconstructions of the cryosphere further suggest that diversification within S. latissima results from chronic glacial isolation in disjunct persistence areas intercalated with ephemeral interglacial poleward expansions and admixture at high-latitude (Arctic) contact zones. This study thus supports a role for glaciations not just in redistributing pre-existing marine lineages but also as a speciation pump across multi-glacial cycles for marine organisms otherwise exhibiting cosmopolite amphi-boreal distributions.
- 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, PedroUnderstanding 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.
- Host and Environmental Specificity in Bacterial Communities Associated to Two Highly Invasive Marine Species (Genus Asparagopsis)Publication . Aires, Tânia; Serrão, Ester; Engelen, Aschwin H.As habitats change due to global and local pressures, population resilience, and adaptive processes depend not only on their gene pools but also on their associated bacteria communities. The hologenome can play a determinant role in adaptive evolution of higher organisms that rely on their bacterial associates for vital processes. In this study, we focus on the associated bacteria of the two most invasive seaweeds in southwest Iberia (coastal mainland) and nearby offshore Atlantic islands, Asparagopsis taxiformis and Asparagopsis armata. Bacterial communities were characterized using 16S rRNA barcoding through 454 next generation sequencing and exploratory shotgun metagenomics to provide functional insights and a backbone for future functional studies. The bacterial community composition was clearly different between the two species A. taxiformis and A. armata and between continental and island habitats. The latter was mainly due to higher abundances of Acidimicrobiales, Sphingomonadales, Xanthomonadales, Myxococcales, and Alteromonadales on the continent. Metabolic assignments for these groups contained a higher number of reads in functions related to oxidative stress and resistance to toxic compounds, more precisely heavy metals. These results are in agreement with their usual association with hydrocarbon degradation and heavy-metals detoxification. In contrast, A. taxiformis from islands contained more bacteria related to oligotrophic environments which might putatively play a role in mineralization of dissolved organic matter. The higher number of functional assignments found in the metagenomes of A. taxiformis collected from Cape Verde Islands suggest a higher contribution of bacteria to compensate nutrient limitation in oligotrophic environments. Our results show that Asparagopsis-associated bacterial communities have host-specificity and are modulated by environmental conditions. Whether this environmental effect reflects the host's selective requirements or the locally available bacteria remains to be addressed. However, the known functional capacities of these bacterial communities indicate their potential for eco-physiological functions that could be valuable for the host fitness.
- Hologenome theory supported by cooccurrence networks of species-specific bacterial communities in siphonous algae (Caulerpa)Publication . Aires, Tânia; Moalic, Yann; Serrao, Ester A.; ARNAUD-HAOND, SophieThe siphonous algae of the Caulerpa genus harbor internal microbial communities hypothesized to play important roles in development, defense and metabolic activities of the host. Here, we characterize the endophytic bacterial community of four Caulerpa taxa in the Mediterranean Sea, through 16S rRNA amplicon sequencing. Results reveal a striking alpha diversity of the bacterial communities, similar to levels found in sponges and coral holobionts. These comprise (1) a very small core community shared across all hosts (< 1% of the total community), (2) a variable portion (ca. 25%) shared by some Caulerpa taxa but not by all, which might represent environmentally acquired bacteria and (3) a large (> 70%) species-specific fraction of the community, forming very specific clusters revealed by modularity in networks of cooccurrence, even in areas where distinct Caulerpa taxa occurred in sympatry. Indirect inferences based on sequence homology suggest that these communities may play an important role in the metabolism of their host, in particular on their ability to grow on anoxic sediment. These findings support the hologenome theory and the need for a holistic framework in ecological and evolutionary studies of these holobionts that frequently become invasive.
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