Ulva Species Research Articles

Parameters affecting the analytical profile of fatty acids in the macroalgal genus Ulva

The fatty acids (FA) of Ulva have potential to contribute to nutrition. However the large variability of FA profiles of Ulva species; thus the quality and quantity of FA in relation to nutrition is poorly defined. Herein we investigate the FA profile of 74 cultured Ulva samples crossing five culture regimes, six extraction regimes and four post-harvesting processes. This is compared alongside a comprehensive review of FA profiles of Ulva spp. With regard to the literature, Ulva is characterised by C16:0 (30.5±11.5%), C18:3 n-3 (14.5±6.3%), C18:4 n-3 (12.5±5.4%), C16:4 n-3 (8.9±4.8%) and C18:1 n-7 (10.1±4.0%). The investigated Ulva fell within the reported range of specific FA. High nutrient conditions showed the most desirable FA profile for health, along with the highest total FA content (56mgg−1 dry weight equivalent) when extracted with an optimised protocol.

Seaweed salt from Ulva: A novel first step in a cascading biorefinery model

We compared post-harvest processing of two species of Ulva (chlorophyta) using 36 washing time-by-temperature combinations. We quantified the yield of crystallized salt after evaporation of the washing water as a target product and characterized the composition of salts and processed biomass, with the additional aim of improving the composition of the processed biomass for production of fertilizer, feed or fuel. Washing of biomass of Ulva ohnoi and Ulva tepida effectively reduced its mineral content with concomitant production of crystalline salts with Na:K ratios of 1.1-2.2 and a maximum of 19% soluble fiber (ulvan). The maximum yield of salt was 29% of the biomass for U. ohnoi and 36% for U. tepida. Salts from both species have potential for human health applications and functional foods. Washing increased the energy content of the biomass from both species by 20-50% to a maximum of 18 MJ kg⁻¹ and protein contents by 11-24% to a maximum of 27.4%. The production of seaweed salt is therefore a novel first step in a cascading biorefinery model for the utilization of macroalgal biomass which simultaneously improves the quality of the processed biomass for production of fertilizer, feed or fuel. (C) 2016 Elsevier B.V. All rights reserved.

The yield and quality of multiple harvests of filamentous Ulva tepida

Species of the genus Ulva are used for human consumption due to their nutritional qualities and we assess a new filamentous species, Ulva tepida. A critical step is to quantify the yield and quality of biomass over multiple harvests to ensure consistency throughout the production cycle. To do this, ropes were seeded with U. tepida and harvested fortnightly over 6 weeks of outdoor cultivation with biomass yield and quality quantified for each harvest. This cycle was repeated a further two times. The yield of biomass was not significantly different between harvests (13.6–23.0 g dry weight (dw) m-1 rope), however, the final harvest was highly variable. Consequently, we recommend a production cycle of two harvests. The quality of biomass, as determined by the key biochemical parameters for these two sequential harvests, was consistent. Carbohydrates were the major component (45 % dw) and were primarily dietary fibre (27 % dw) consisting of insoluble (18 % dw) and soluble (9 % dw, equates to ulvan) fibre, with consistent values between harvests. Protein, as the sum of amino acids (17 % dw), was also consistent between harvests. Similarly, the content of ash (31 % dw) and lipids (3 % dw), as well as the composition of minerals and fatty acids was consistent. These results quantify, for the first time, no negative effects of multiple harvests on the yield and quality of biomass and support this technique to optimise productivity and quality.

Abiotic factors influencing biomass accumulation of green tide causing Ulva spp. on Pyropia culture rafts in the Yellow Sea, China

Annually recurrent green-tides in the Yellow Sea have been shown to result from direct disposal into the sea of fouling Ulva from Pyropia aquaculture. The role abiotic factors play in Ulva biomass accumulation on rafts was studied to find ways to mitigate this problem. Dissolved inorganic nitrogen (DIN) was very high at all sites, but the highest Ulva biomass was associated with the lowest DIN and anthropogenic N. Under luxuriant background nutrient conditions, variability in temperature and periods of emersion, rather than pH, light and salinity determined Ulva biomass. Two dominant species of Ulva displayed differing tolerances to temperature and desiccation which helped explain why Ulva prolifera dominates floating green-tides. Rather than trying to mitigate green-tides only by reducing nutrient pollution, an earlier harvest of Pyropia in southern Jiangsu Province especially before temperatures increase greatly above 10°C during April, could reduce the biomass of U. prolifera disposed from rafts.

Supercritical fluid extraction of algae enhances levels of biologically active compounds promoting plant growth

The aim of this research was to screen plant growth biostimulant properties of supercritical CO2 macroalgal extracts. To this end secondary metabolites were isolated from the biomass of marine macroalgae from the Baltic Sea (species of Polysiphonia, Ulva and Cladophora). Chemical characteristics of the algal extracts were determined by inductively coupled plasma atomic emission spectroscopy for inorganic constituents and high-performance liquid chromatography and spectrophotometry for organic constituents. Inorganic (macro- and microelements) and organic (plant hormones: auxins and cytokinins; polyphenols) compounds were detected in the extract. Algal extracts were tested primarily on garden cress (Lepidium sativum L.; Brassicaceae) and wheat (Triticum aestivum L.; Poaceae). The extracts enhanced chlorophyll and carotenoid content in plant shoots, as well as root thickness and above-ground biomass. The most effective method of application of the extract was by foliar feed on cress and seed maceration for wheat. Algal extracts obtained by supercritical fluid extraction (SFE) were found to be a novel natural source of compounds, stimulating growth of cultivated plants. However, field trials will be required to show that the extracts can act as plant biopesticides and growth biostimulants.

The expansion of Ulva prolifera O.F. Müller macroalgal blooms in the Yellow Sea, PR China, through asexual reproduction

Since 2007, Ulva macroalgal blooms have occurred along the coastal areas of the Yellow Sea, China. These blooms are dominated by fragments of Ulva prolifera in the early stages of development. The objectives of this study were to identify the primary mode of asexual reproduction for U. prolifera and to evaluate the contribution of these thalli fragments to the formation of blooms. Four different growth and reproductive strategies of U. prolifera segments were found including: 1) tubular diameter becoming larger; 2) formation of new branches; 3) release of zoids; and 4) polarized growth. This is the first report showing the development of numerous blade-lets from a single segment, which is remarkably different from previous studies on other Ulva species. The results in the present study provide critical information to understand how this species is able to support its explosive growth during a bloom.

Macroalgal Morphogenesis Induced by Waterborne Compounds and Bacteria in Coastal Seawater.

Axenic gametes of the marine green macroalga Ulva mutabilis Føyn (Ria Formosa, locus typicus) exhibit abnormal development into slow-growing callus-like colonies with aberrant cell walls. Under laboratory conditions, it was previously demonstrated that all defects in growth and thallus development can be completely abolished when axenic gametes are inoculated with a combination of two specific bacterial strains originally identified as Roseobacter sp. strain MS2 and Cytophaga sp. strain MS6. These bacteria release diffusible morphogenetic compounds (= morphogens), which act similar to cytokinin and auxin. To investigate the ecological relevance of the waterborne bacterial morphogens, seawater samples were collected in the Ria Formosa lagoon (Algarve, Southern Portugal) at 20 sampling sites and tidal pools to assess their morphogenetic effects on the axenic gametes of U. mutabilis. Specifically the survey revealed that sterile-filtered seawater samples can completely recover growth and morphogenesis of U. mutabilis under axenic conditions. Morphogenetic activities of free-living and epiphytic bacteria isolated from the locally very abundant Ulva species (i.e., U. rigida) were screened using a multiwell-based testing system. The most represented genera isolated from U. rigida were Alteromonas, Pseudoalteromonas and Sulfitobacter followed by Psychrobacter and Polaribacter. Several naturally occurring bacterial species could emulate MS2 activity (= induction of cell divisions) regardless of taxonomic affiliation, whereas the MS6 activity (= induction of cell differentiation and cell wall formation) was species-specific and is probably a feature of difficult-to-culture bacteria. Interestingly, isolated bacteroidetes such as Algoriphagus sp. and Polaribacter sp. could individually trigger complete Ulva morphogenesis and thus provide a novel mode of action for bacterial-induced algal development. This study also highlights that the accumulation of algal growth factors in a shallow water body separated from the open ocean by barrier islands might have strong implications to, for example, the wide usage of natural coastal seawater in algal (land based) aquacultures of Ulva.

Ulva sapora sp. nov., an abundant tubular species of Ulva (Ulvales) from the tropical Pacific Ocean

:Previously defined by molecular studies undertaken in Japan and Australia as Ulva sp. 3 and in Hawaii as Ulva OTU6, Ulva sapora sp. nov. is described using combined morphological, anatomical, reproductive and molecular studies on 46 specimens from five localities on the tropical and subtropical east Australian coast. Ulva sapora is characterised by its unique internal transcribed spacer sequence and the following combination of characters: the main axis of the unbranched or branched filiform thallus increasing in breadth from the basal to the upper thallus, cells in surface view unordered except for short rows in some areas of the thallus, cells containing a single chloroplast covering half to the whole outer cell wall and containing 2–10 pyrenoids and many starch granules and reproduction by biflagellate zoids exhibiting differing phototactic responses. The new species is the result of the first critical taxonomic appraisal of the species of Ulva of the poorly investigated tropical east Australian marine macroalgal flora. Ulva sapora was the most abundant filiform species of Ulva in the region, accounting for 32% of the specimens collected during the study.

Candidate key genes for low-salinity adaptation identified by RNA-seq comparison between closely related Ulva species in marine and brackish waters

Candidate key genes for low-salinity adaptation identified by RNA-seq comparison between closely related Ulva species in marine and brackish waters

Molecular identification and nutrient analysis of the green tide species Ulva ohnoi M. Hiraoka & S. Shimada, 2004 (Ulvophyceae, Chlorophyta), a new report and likely nonnative species in the Gulf of Mexico and Atlantic Florida, USA

Molecular identification and nutrient analysis of the green tide species Ulva ohnoi M. Hiraoka & S. Shimada, 2004 (Ulvophyceae, Chlorophyta), a new report and likely nonnative species in the Gulf of Mexico and Atlantic Florida, USA

The chloroplast genome of the marine green macroalga Ulva fasciata Delile (Ulvophyceae, Chlorophyta)

We present the 96 005 bp circular chloroplast genome (cpDNA) of Ulva fasciata. This cpDNA was ∼4000 bp smaller than the cpDNA of Ulva sp. UNA00071828; however, this cpDNA was AT rich (75.1%) similar to Ulva sp. The U. fasciata cpDNA was also similar in gene content (101 identified genes) compared to Ulva sp., which included 71 protein-coding genes, 3 ribosomal RNAs (rRNAs) and 27 transfer RNAs (tRNAs). Only one tRNA, trnN(AUU), that was present in Ulva sp. was absent in U. fasciata. Five introns were present in the following genes of U. fasciata: petB (2), psbD (1), psaB (1) and rrl (1). Ulva sp. lacked introns in psbD and psaB, and introns present in atpA and psbB in Ulva sp. were absent in the homologous genes of U. fasciata. A gene arrangement comparison of both Ulva species showed that a ∼27 000 bp segment of DNA consisting of genes psbB to trnT(UGU) was inverted. Furthermore, a phylogenetic analysis of 1135 bp of the rbcL gene confirmed that this cpDNA and the previously published mitochondrial genome from this sample were indeed from U. fasciata.

Antimicrobial effects of marine algal extracts and cyanobacterial pure compounds against five foodborne pathogens

The marine environment is a proven source of structurally complex and biologically active compounds. In this study, the antimicrobial effects of a small collection of marine-derived extracts and isolates, were evaluated against 5 foodborne pathogens using a broth dilution assay. Results demonstrated that algal extracts from Padina and Ulva species and cyanobacterial compounds antillatoxin B, laxaphycins A, B and B3, isomalyngamide A, and malyngamides C, I and J showed antimicrobial activity against Gram positive foodborne pathogens (Listeria monocytogenes, Bacillus cereus and Staphylococcus aureus) at low concentrations (⩽500μg/ml). None of the algal extracts or cyanobacterial isolates had antibacterial activity against Gram negative bacteria (Escherichia coli and Salmonella enterica serovar Typhimurium).

The mitochondrial genome of the bloom-forming green alga Ulva prolifera

From 2007 to 2015, massive green tides formed by Ulva prolifera O.F. Müller have broken out for nine consecutive years in the Yellow Sea of China. Here, we determined the complete mitochondrial genome sequence of U. prolifera. The circular U. prolifera mitogenome is 63 845 bp in size, with the overall A + T content of 66.04% which is similar to the other three ulvophyceans (60.66%–67.83%). The mitogenome encodes 74 genes and the coding sequences account for 77.3% of the genome. Nine introns are identified in five genes and each of these introns contains an ORF. Two long tandem repeats identified have a period of 11 bp with a copy number of 62.5 and 19.5, respectively. The genome organization of U. prolifera is similar to that in Ulva sp., and its reduced spacer region makes it more compact than the latter. The present data will provide important information on phylogenetics and molecular evolution of Ulva species.

Intertidal seaweeds from North Atlantic Patagonian coasts, Argentina

The coasts located between 39°S and 41°S in the Argentinean biogeographic province have been described by impoverished seaweed assemblages, however the floristic information about this region is sparse. The aim of this study was to survey the intertidal seaweeds inhabiting three sites in the oceanographic system “El Rincon” (Buenos Aires, Argentina). A total of 42 taxa were identified with a dominance of Rhodophyta species. The sandstone outcrops (SO) had 29 taxa, whereas both the tidal flat (TF) and oyster reefs (OR) had 11 taxa. The estuarial species Ulva intestinalis and Ulva prolifera were recorded in TF, whereas calcified macroalgae were only found in SO. The differences in richness and composition of seaweed assemblages were associated with substrate type, wave exposure, incident light and salinity. These differences were also evidenced by a dissimilar number of functional groups, which was higher in SO with a dominance of filamentous macroalgae.

Revision of herbarium specimens of freshwater Enteromorpha-like Ulva (Ulvaceae, Chlorophyta) collected from Central Europe during the years 1849–1959

This paper presents results concerning the taxonomic revision of Ulva taxa originating from herbarium specimens dating back to 1849–1959. A staining and softening mixture was applied to allow a detailed morphometric analysis of thalli and cells and to detect many morphological details. The study focused on individuals collected exclusively from inland water ecosystems (having no contact with sea water). Detailed analysis concerned the following items: structures of thalli and cells, number of pyrenoids per cell, configuration of cells inside the thallus, occurrence or not of branching thallus, shapes of apical cells, and shape of chromatophores. The objective of the study was to confirm the initial identifications of specimens of Ulva held in herbaria. The study sought to determine whether saltwater species of the genus Ulva, e.g., Ulva compressa and U. intestinalis, could have been found in European freshwater ecosystems in 19th and 20th centuries. Moreover, the paper presents a method for the initial treatment of voucher specimens for viewing stained cellular structures that are extremely vulnerable to damage (the oldest specimens were more than 160 years old). The use of a glycerine-based softening mixture allowed the detailed analysis of the anatomic structure of cells as well as the determination of the number and size of pyrenoids, i.e., some of the key taxonomic features of Ulva taxa. Most of specimens were identified as belonging to the species U. flexuosa. Marine species such as Ulva intestinalis or U. compressa were not confirmed to occur in the inland water ecosystems of Central Europe in the 19th and 20th centuries.

Cryopreservation of gametophytic thalli of Ulva prolifera (Ulvales, Chlorophyta) from Korea

Cryopreservation is needed to ensure long-term storage without any genetic drift and contamination. To conserve Ulva species, gametophytic thalli of Ulva prolifera (Chlorophyta) were first cryopreserved at −196 °C using the two-step cooling method with cooling rate of 1 °C min−1 to −40 °C. Three cryoprotectants (dimethyl sulfoxide (DMSO), glycerol, and proline) at five concentrations (5, 10, 15, 20, and 25 %) and mixed cryoprotectants were assessed to determine the optimal solution. The mixture of cryoprotectants with the highest viability was 10 % glycerol in combination with 5 % DMSO and 5 % proline, with a viability of 89.2 %. The cryoprotectant treated singly with the highest viability was 20 % glycerol with a viability of 91.6 %. However, there was no statistically significant difference between 20 % glycerol and the mixed treatment. An evaluation of long-term storage in liquid nitrogen showed very high viability of 91.2–92.1 % with no statistically significant effect from storage time up to 120 days. The specimens developed normally in culture after cryopreservation for 120 days with the rate of gametogenesis reaching 95.7 % on the fourth day of culture. The released gametes developed normally into gametothalli. In conclusion, the use of glycerol as a cryoprotectant was very effective for cryopreservation of the gametothalli of U. prolifera. With 20 % glycerol, viability was very high as 91.6 %. The results suggest that gametothalli of U. prolifera can be cryopreserved completely by a treatment with 15–25 % glycerol singly as well as by a mixture of cryoprotectants with usual efficiency as a cryoprotectant.

Persistent occurrence of floating Ulva green tide in Hiroshima Bay, Japan: seasonal succession and growth patterns of Ulva pertusa and Ulva spp. (Chlorophyta, Ulvales)

Since the late 1980’s, a persistent green tide of floating Ulva without any clear seasonal fluctuation has occurred in Hiroshima Bay, Seto Inland Sea, Japan. We hypothesized that the persistence is due to the co-existence of Ulva species with different seasonal growth patterns, and monitored the seasonal composition and growth characteristics of the constituent Ulva within the green tide. Two morphological types of Ulva were identified, and one type, U. pertusa, was almost the sole constituent during winter and spring. The other type Ulva spp., which has marginal microscopic serrations on the thallus, was dominant during summer and autumn. Both Ulva showed the highest relative growth rate in early autumn, but growth of Ulva spp. was faster in summer than that of U. pertusa and inhibited in winter. U. pertusa had more eurythermal characteristics in which the growth rate remained relatively high in winter. Water temperature was the most correlated environmental variable for the seasonal growth of both Ulva types rather than light or nutrients, but more influential on Ulva spp. Recent increasing trend of ambient seawater temperature is considered to be favorable for the growth of both Ulva types and a causative factor of the green tide.

The green seaweed Ulva: a model system to study morphogenesis.

Green macroalgae, mostly represented by the Ulvophyceae, the main multicellular branch of the Chlorophyceae, constitute important primary producers of marine and brackish coastal ecosystems. Ulva or sea lettuce species are some of the most abundant representatives, being ubiquitous in coastal benthic communities around the world. Nonetheless the genus also remains largely understudied. This review highlights Ulva as an exciting novel model organism for studies of algal growth, development and morphogenesis as well as mutualistic interactions. The key reasons that Ulva is potentially such a good model system are: (i) patterns of Ulva development can drive ecologically important events, such as the increasing number of green tides observed worldwide as a result of eutrophication of coastal waters, (ii) Ulva growth is symbiotic, with proper development requiring close association with bacterial epiphytes, (iii) Ulva is extremely developmentally plastic, which can shed light on the transition from simple to complex multicellularity and (iv) Ulva will provide additional information about the evolution of the green lineage.

Changes to the biomass and species composition of Ulva sp. on Porphyra aquaculture rafts, along the coastal radial sandbank of the Southern Yellow Sea

Compositions, changes and biomass of attached Ulva species on Porphyra rafts along the radial sandbank in the Yellow Sea were investigated, and potential contributions to green tides was analyzed. Ulva prolifera, Ulva flexuosa and Ulva linza were all appeared throughout the investigated period. U. prolifera and U. flexuosa dominated attached Ulva population on Porphyra rafts. Attached Ulva species biomass showed obviously spatial and temporal variations. Temperature, Ulva microscopic propagules and human activities were main factors to influence attached Ulva species biomass. The total attached Ulva species biomass was more than 20,000 fresh weight tons in April, and the green tide causative species U. prolifera accounted 51.03% in April 2013 before green tides occurred. The high biomass of attached Ulva species would contribute most to green tides in the Yellow Sea. But how attached Ulva species on Porphyra rafts contributing to green tides in the Yellow Sea should be further studied.

Herbivore impacts on two morphologically similar bloom-forming Ulva species in a eutrophic bay

Herbivore impacts on macrophyte growth vary with the identity of the herbivores and macrophytes, as well as under different abiotic conditions. This interaction is further complicated by anthropogenic alterations to the environment, such as eutrophication. In this study, we utilized in situ herbivore exclusion experiments and mesocosm feeding preference assays to examine the impacts of different herbivores on the growth of two morphologically similar, co-occurring macroalgal bloom Ulva species in a nutrient-rich environment. We found that herbivory had a measurable impact on Ulva biomass, though the rate of consumption rarely surpassed growth for either Ulva species. We determined that the primary herbivores within the blooms were amphipods and mud crabs, and that their effects varied among study sites and months. Our results also confirmed that, even with a diverse suite of consumers, Ulva blooms are capable of escaping herbivore control, particularly early in the growing season when growth rates peak and herbivore activity is limited. Furthermore, our experiments revealed species-specific feeding preferences among herbivores, as well as differences in growth rates and chemistry between the two Ulva species, which likely influence bloom dynamics.