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- Physiological potential of the chlorophyte Caulerpa prolifera for proliferation across the Mediterranean-Atlantic basins in a warmer oceanPublication . Olivé, Irene; E, Varela-Álvarez; Silva, João; Serrao, Ester; Santos, RuiOcean warming is altering the metabolic balances of organisms, favouring the expansion of thermo-tolerant individuals. The fast-growing macroalga Caulerpa prolifera is rapidly expanding in the Ria Formosa lagoon (Portugal), a connection area between Mediterranean and Atlantic basins. We investigated the metabolic capacity of C. prolifera to cope with ocean warming, to elucidate its expansion potential. The photosynthetic and respiratory plasticity of 4 populations of C. prolifera spread along the Mediterranean−Atlantic basins was assessed under a temperature range of 20 to 30°C. In addition, molecular markers were used to investigate the genetic identity of the strain found in Ria Formosa, which confirmed its Mediterranean origin. All examined populations showed large physiological thermo tolerance and metabolic plasticity to warming. The photosynthetic efficiency of C. prolifera improved by 50% with temperature, and the maximum photosynthetic production doubled along the temperature range tested. Respiration did not vary with temperature, whereas the metabolic quotient increased by more than 70%when temperature increased from 20 to 25−30°C. Minor differences in the photosynthetic descriptors were detected among populations, reflecting light- and dark-adapted physiology of Mediterranean and Atlantic populations, respectively. Our results show that all tested populations of C. prolifera have the physiological potential to cope with temperature increases up to 30°C, which indicates that ocean warming may contribute to the expansion of C. prolifera in the Mediterranean− Atlantic basins.
- Mediterranean Species of Caulerpa Are Polyploid with Smaller Genomes in the Invasive OnesPublication . E, Varela-Álvarez; Gómez Garreta, A.; Rull Lluch, J.; Salvador Soler, N.; Serrão, Ester; Siguán, M. A. R.Caulerpa species are marine green algae, which often act as invasive species with rapid clonal proliferation when growing outside their native biogeographical borders. Despite many publications on the genetics and ecology of Caulerpa species, their life history and ploidy levels are still to be resolved and are the subject of large controversy. While some authors claimed that the thallus found in nature has a haplodiplobiontic life cycle with heteromorphic alternation of generations, other authors claimed a diploid or haploid life cycle with only one generation involved. DAPI-staining with image analysis and microspectrophotometry were used to estimate relative nuclear DNA contents in three species of Caulerpa from the Mediterranean, at individual, population and species levels. Results show that ploidy levels and genome size vary in these three Caulerpa species, with a reduction in genome size for the invasive ones. Caulerpa species in the Mediterranean are polyploids in different life history phases; all sampled C. taxifolia and C. racemosa var. cylindracea were in haplophasic phase, but in C. prolifera, the native species, individuals were found in both diplophasic and haplophasic phases. Different levels of endopolyploidy were found in both C. prolifera and C. racemosa var. cylindracea. Life history is elucidated for the Mediterranean C. prolifera and it is hypothesized that haplophasic dominance in C. racemosa var. cylindracea and C. taxifolia is a beneficial trait for their invasive strategies.
- Development and characterization of twelve microsatellite markers for Porphyra linearis GrevillePublication . E, Varela-Álvarez; Paulino, Cristina; Serrao, EsterThe genus Porphyra (and its sister genus Pyropia) contains important red algal species that are cultivated and/or harvested for human consumption, sustaining a billion-dollar aquaculture industry. A vast amount of research has been focused on species of this genus, including studies on genetics and genomics among other areas. Twelve novel microsatellite markers were developed here for Porphyra linearis. Markers were characterized using 32 individuals collected from four natural populations of P. linearis with total heterozygosity varying from 0.098 to 0.916. The number of alleles per locus ranged from 2 to 18. All markers showed cross amplification with Porphyra umbilicalis and/or Porphyra dioica. These polymorphic microsatellite markers are useful for investigating population genetic diversity and differentiation in P. linearis and may become useful for other genetic research on the reproductive biology of this important species.
- Phycobiliproteins, nitrogenous compounds and fatty acid contents in field-collected and cultured gametophytes of Porphyra dioica, a red sea vegetablePublication . E, Varela-Álvarez; Tobin, Paul R.; Guiheneuf, Freddy; FitzGerald, Richard J.; Stengel, Dagmar B.The extensive variation in the biochemical composition of algal species is used as a source of potential bioactive compounds for applications in the agri-food industry and in the field of functional foods. Among these species, Porphyra/Pyropia spp. (nori, laver) are red sea vegetables which provide the foundation for a billion-dollar industry. In this study, we determine the growth and biochemical composition of distinct reproductive traits (females vs. males) in Porphyra dioica. In order to characterize and enhance through cultivation the bioactive profiles and biochemical composition of this sea vegetable, we determined the effects of environmental parameters (light and nutrients) on the growth of different life history traits (females vs. males) in cultured and field samples of P. dioica. In field-collected samples, females contained higher contents of phycoerythrin (9.71 ± 3.13 mg g−1 DW), PUFA (omega-3 fatty acids, 12.25 ± 0.78 mg g−1 DW; eicosapentaenoic acid, 11.54 ± 0.92 mg g−1 DW) and total fatty acids (TFA) (31.58 ± 2.5 mg g−1 DW) than males. The total nitrogen (TN) content was similar in both traits in the field, but the protein nitrogen (PN) was higher in males from field collections (42.80 mg g−1 DW). In culture, males and females responded differently to applied environmental factors, with an increase of some omega-6 fatty acids (e.g. 20:4 n-6 with an increase of 4.98 %TFA, 0.1 mg g−1 DW) in females and omega-7,9 fatty acids in males (increase of 13.75 %TFA, 0.79 mg g−1 DW in omega-7 and 1.59 %TFA in omega-9) associated with exposure to adverse conditions (N starvation under low light intensity). We discuss the possibility of using P. dioica as a promising source of functional new food products such as enriched nori in bioactive compounds such as monounsaturated and polyunsaturated fatty acids.
- Genomic DNA isolation from green and brown algae (Caulerpales and Fucales) for microsatellite library constructionPublication . E, Varela-Álvarez; Andreakis, N.; Lago-Lestón, Asunción; Pearson, G. A.; Serrão, Ester; Procaccini, G.; Duarte, C. M.; Marbà, N.A method for isolating high-quality DNA is presented for the green algae Caulerpa sp. (C. racemosa, C. prolifera, and C. taxifolia) and the brown alga Sargassum muticum. These are introduced, and invasive species in Europe, except for the native C. prolifera. Previous methods of extraction, using cetyl trimethyl ammonium bromide or various commercial kits, were used to isolate genomic DNA but either no DNA or DNA of very low quality was obtained. Genomic libraries were attempted with Caulerpa sp. on three occasions and either the restriction enzyme, the Taq polymerase, or the T4 ligase was inhibited, probably by the large amount of polysaccharides in these algae. The method presented here consists of the rapid isolation of stable nuclei, followed by DNA extraction. Yields of 6–10 μg genomic DNA from 1 g fresh blades were obtained. After genomic DNA was isolated from fresh material, the quality was checked by agarose gel. Quantification of DNA concentration was performed using UV spectrophotometric measurement of the A260/A280 ratio. The DNA was suitable for PCR, cloning, and hybridization. The DNA isolated using this method allowed successful construction of microsatellite libraries for Caulerpa species and S. muticum. The technique is inexpensive and appropriate for the isolation of multiple samples of DNA from a small amount of fresh material.
- Influence of irradiance, dissolved nutrients and salinity on the colour and nutritional characteristics of Gracilariopsis longissima (Rhodophyta)Publication . Bermejo, Ricardo; Macias, Manuel; Sanchez-Garcia, Fini; Love, Robyn; E, Varela-Álvarez; Hernandez, IgnacioColour is immediately perceived by the consumer and crucial for food product attractiveness. In this study, the possibility of obtaining different colour morphotypes in the rhodophyte Gracilariopsis longissima using short cultivation protocols (i.e. 9 days) was explored. In a first factorial experiment, the effects of salinity (25‰, 35‰ and 45‰), irradiance (60 and 270 μmol photons m− 1 s − 1 ) and nutrient conditions (N and P enrichment, no enrichment) on the growth, pigment concentration and colour of G. longissima were assessed. The results indicated that growth rate and phycocyanin were influenced by the three variables, whereas the concentration of other pigments (chlorophyll a, carotenoids and phycoerythrin) was significantly influenced by irradiance and nutrient conditions. The colour, defined as the Red, Green, Blue (RGB) signal from the photographed thalli, was mainly affected by irradiance and nutrient conditions. In a second experiment, four culture conditions yielding contrasting colour morphotypes and growth rates were repeatedly scaled up in the experiment to get enough biomass and to analyze nutritional properties (lipids, proteins, tissue N and P). The colour morphotypes and the corresponding culture conditions selected were: i) dark red; high salinity, low irradiance, nutrient enrichment; ii) light red; medium salinity, high irradiance, nutrient enrichment; iii) brownish; low salinity, low irradiance; no enrichment; and iv) green-yellowish; low salinity, high irradiance, no enrichment. These conditions caused marked differences in the nutritional properties of the thalli. The light red colour showed the best nutritional characteristics. Overall, G. longissima was not a suitable source of omega 3, but can be a source of Fe (0.34–0.53 mg g− 1 DW) and K (103–161 mg g− 1 DW), and its K:Na ratio can be enhanced under increasing salinity. The fast ecophysiological response, and its wide tolerance to environmental conditions, makes this species an excellent candidate for the development of short cultivation protocols.
- The rediscovery of Caulerpa prolifera in Ria Formosa, Portugal, 60 years after the previous recordPublication . Cunha, A. H.; E, Varela-Álvarez; Paulo, D. S.; Sousa, Inês; Serrão, EsterThe westernmost occurrence of Caulerpa prolifera on the Atlantic European coast has been accepted in recent decades, to be Huelva province, southern Spain. In April 2011, this species was found in Ria Formosa, southern Portugal, extending its westernmost limit along the Iberian Peninsula coastline. In the course of research into this species it was discovered that this alga had been found in Ria Formosa in the 19th century by the naturalist Welwitsch and subsequently in the 1930s by others but it was never found in the many field studies conducted in Ria Formosa during the past few decades. The species had therefore either become extinct in the area or persisted as a cryptic undetected stage. In order to investigate the source of colonization and to verify the genetic identity, a partial cpDNA region (tufA gene) was sequenced. Comparisons of nucleotide similarity in sequences from the Ria Formosa and from populations of the Atlantic and Mediterranean confirmed the Caulerpa prolifera identification and gave clues about a possible origin of this population as deriving from expansion of a Mediterranean source rather than one from the western Atlantic.
- Microsatellite markers for the giant kelp macrocystis pyriferaPublication . Alberto, F.; Whitmer, A.; Coelho, N. C.; Zippay, M.; E, Varela-Álvarez; Raimondi, P. T.; Reed, D. C.; Serrão, EsterWe report the isolation and characterization of 16 microsatellite loci to study the population genetics of the giant kelp, Macrocystis pyrifera. Markers were obtained by screening a genomic library enriched for microsatellite motifs. Of the 37 primer pairs defined, 16 amplified clean polymorphic microsatellites and are described. These loci identified a number of alleles ranging from three to forty (mean = 16.5, and gene diversity ranging from 0.469 to 0.930 (mean = 0.774). The isolation and characterization of these highly polymorphic markers will greatly benefit much needed studies on the molecular ecology of this important macroalga.
- Niche conservatism and spread of seaweed invasive lineages with different residence time in the Mediterranean SeaPublication . Chefaoui, Rosa; E, Varela-ÁlvarezMarine algae invasions attract a lot of interest as they are altering the structure of marine ecosystems. However, niche dynamics and risk predictions of marine invasions integrating phylogeographic structure in the analyses have not yet been investigated. In this study, we perform a comprehensive analysis of two invasive lineages of Caulerpa taxifolia with different residence time in the Mediterranean Sea for a better understanding of their invasive processes. We performed lineage-based and species-based niche models to assess the risk of invasion, the spatial overlap, and the variables delimiting the distribution of the two lineages. We also compared the effect of using different extents on niche overlap and niche shift analyses. Intraspecific models with pooled occurrences accurately found two separate regions susceptible of invasion for each invasive lineage in the Mediterranean, while species-based predictions underestimated invaded regions. The invasive lineages spread across colder coastal areas than the species. Altogether, we provide evidence that different invasive lineages of algae show dissimilar environmental responses and invasive ranges that are not detectable by species-based analyses. Moreover, niche overlap and niche shift analyses seem to depend greatly on the geographical extent used. According to the most appropriate extent (worldwide), the invaded range did not show niche shift, and thus, no evidence of a post-introduction adaptation scenario was found as both lineages invaded habitats similar to their Australian native locations. Actions to prevent further spreading of the most recent invasive lineage are needed.
- Concise review of the genus Caulerpa J.V. LamourouxPublication . Zubia, Mayalen; Draisma, Stefano G. A.; Morrissey, Kathryn Lee; Varela-Álvarez, Elena; De Clerck, OlivierThe genus Caulerpa is highly diverse, especially in the Caribbean Sea, the Indo-Malay archipelago and the temperate waters of southern Australia. Currently, more than 100 species are recognized worldwide. Despite recent advances in taxonomy and phylogeny, there is still confusion about the delimitation and identification of some species due to tremendous phenotypic plasticity. Caulerpa is known to occupy a wide range of environmental niches and to have great invasive potential. More studies are necessary to understand better the ecology (invasiveness, the functional role of its microbiome) and the biology (reproduction, life cycle, and metabolism) of Caulerpa species, especially for economical species. Very few species, mainly C. lentillifera and C. racemosa known as green caviar, have been cultivated. Caulerpa is consumed mostly in Asia and Oceania, but its popularity tends to be on the increase in western countries with new nutritional practices (vegetarians, vegans, health foods). Being naturally enriched in essential nutrients and various health-promoting compounds, Caulerpa species are promising candidates for the design of functional foods and in the health and well-being sectors. The diversity of Caulerpa offers a remarkable potential for valorization with innovation opportunities. Caulerpa farming can bring significant economic and environmental (e.g., bioremediation, blue carbon pump) benefits if these farms are established in a sustainable approach.