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Morphological and ultrastructural studies on Ulva flexuosa subsp. pilifera (Chlorophyta) from Poland

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Ulva flexuosa subsp. pilifera (Kütz.) M. J. Wynne 2005 (= Enteromorpha pilifera Kützing 1845) was previously found in Argentina, the Czech Republic, Germany, Hungary, Romania, Slovakia and Sweden, recently also in Poland. The genus Ulva was first time described as Enteromorpha. Interestingly, Enteromorpha is used nowadays as a synonym for Ulva, a development which is based on molecular data. The morphologies of both young and mature specimens were studied, and most life cycle stages could be observed. Further, the formation of calcium carbonate crystals on the surface of Ulva thalli seems to influence the arrangement of the cells. A detailed ultrastructural (TEM) analysis of cell walls is presented. The TEM reveals in great details highly complex, irregular structures with stratification lines.
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Introduction
e genus Ulva is a representative of the family Ulvaceae
and has the following characteristics: (i) macroscopic, lamen-
tous, thread-like, membranous (sheet-like); (ii) reproduction
by biagellate or quadriagellate gametes or zoospores; (iii)
multilayered cell walls are thick and made of microbrils,
which are usually irregularly arranged; (iv) each cell contains
one parietal and cup-shaped chloroplast with one or several
pyrenoids; (v) a widely distributed marine genus with its few
freshwater representatives [1,2]. Many species are adapted
to wide ranges of habitats, with variable parameters such as
salinity, temperature, water quality, and grow successfully in
nutrient-rich habitats causing green tides and marine fouling
[3,4]. Ulva species usually grow in form of typical vividly
green tube- or leaf-shaped thalli, oen also with various types
of branches, attached to the substrate by rhizoids, or later as
free-oating intestinoid clusters [5]. During its life cycle, Ulva
forms morphologically similar haploid and diploid thalli, both
of which produce asexual zoospores by mitotic division of
vegetative cells [1]. Ulva exuosa, taxonomically complicated
macroalgal species, is distributed in coastal seawaters nearly
worldwide [5]. According to Mareš [5] this species has many
dierent morphological forms, and several important unify-
ing characteristics: branching, cell structure, and chloroplast
structure.
Ulva (syn. Enteromorpha) exuosa subsp. pilifera (Kütz.) M.J.
Wynne 2005 (= Enteromorpha pilifera Kützing 1856) has been
observed at four sampling sites in Poland [610]. In studies
reported from around the world, Ulva exuosa subsp. pilifera has
been identied in many inland sampling sites, namely in Sweden
[11], Slovakia and the Czech Republic [12,13], Argentina [14],
in England [15], Germany and Hungary [13].
According to the current knowledge, freshwater Ulva,
including U. exuosa subsp. pilifera [8,1013], appear only
as monostromatic tubular or sometimes leaf-like thalli (e.g.
U. intestinalis, U. compressa, U. exuosa). is makes a major
dierence from the marine Ulva, which frequently grow also
in form of distromatic frondose thalli. e thallus of Ulva
exuosa subsp. pilifera can reach a length of up to 1 m, and it
is poorly branched but has numerous proliferations. Accord-
ing to Starmach [12] and Pliński [16], cells of this species are
rectangular rounded (22–30 × 12 μm) or sometimes polygonal
rounded, and are arranged in longitudinal and crosswise rows.
Chloroplasts are parietal, girdle-shaped, covering most of
the cell wall, with 2 (rarely 4) pyrenoids occur in a cell. e
zoospores are about 10 μm long and 5 μm wide in diameter.
Male gametes (6.3 × 2.7 μm) are slightly smaller than female
gametes (6.7 × 3.4 μm). It is generally known that gametes can
germinate without the fertilization process. e number of
pyrenoids can change during the lifespan of thalli, pyrenoids
Abstract
Ulva exuosa subsp. pilifera (Kütz.) M. J. Wynne 2005 (= Enteromorpha pilifera Kützing 1845) was previously found in Argentina,
the Czech Republic, Germany, Hungary, Romania, Slovakia and Sweden, recently also in Poland. e genus Ulva was rst time
described as Enteromorpha. Interestingly, Enteromorpha is used nowadays as a synonym for Ulva, a development which is based
on molecular data. e morphologies of both young and mature specimens were studied, and most life cycle stages could be
observed. Further, the formation of calcium carbonate crystals on the surface of Ulva thalli seems to inuence the arrangement
of the cells. A detailed ultrastructural (TEM) analysis of cell walls is presented. e TEM reveals in great details highly complex,
irregular structures with stratication lines.
Keywords: green algae, ultrastructure, cell wall, Ulva exuosa subsp. pilifera, Poland
Journal homepage: pbsociety.org.pl/journals/index.php/asbp
ORIGINAL RESEARCH PAPER Received: 2012.11.19 Accepted: 2013.05.14 Published electronically: 2013.06.21 Acta Soc Bot Pol 82(2):157–163 DOI: 10.5586/asbp.2013.013
Morphological and ultrastructural studies on Ulva exuosa subsp. pilifera
(Chlorophyta) from Poland
Beata Messyasz
1
,
Joanna Czerwik-Marcinkowska
2
*, Andrzej Massalski
2
, Bohuslav Uher
3
, Andrzej Rybak
1
, Lidia
Szendzina
1
, Marta Pikosz
1
1
Institute of Environmental Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland
2
Institute of Biology, The Jan Kochanowski University in Kielce, Świetokrzyska 15, 25-406 Kielce, Poland
3
Department of Botany and Zoology, Masaryk University, Kotlářská 2, 611 37 Brno, Czech Republic
* Corresponding author. Email: marcinko@kielce.com.pl
Handling Editor: Andrzej Bodył
This is an Open Access digital version of the article distributed
under the terms of the Creative Commons Attribution 3.0 License
(creativecommons.org/licenses/by/3.0/), which permits redistribution, commercial
and non-commercial, provided that the article is properly cited.
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Acta Societatis Botanicorum Poloniae
Polish Botanical Society
Elektronicznie podpisany przez Polish Botanical Society
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may be numerous in the autospores but less numerous in the
mature cells. However, as Griths [17] suggested, it is dicult
to correlate the presence or absence of pyrenoids with any of
other major diacritical features.
In the 1970’s, ultrastructural studies led to a reclassication
of this group [18,19]. Most studies of Ulva marine species
have been concerned with the ultrastructure aspects of the
rhizoid cell morphology [20], the mitosis process [21], the
zoospores [22] and their agellar apparatus [19], as well as
the chloroplast lamellar system [23]. e ultrastructure of the
genus Enteromorpha cell wall was addressed only a few times
[14,18], and systematic observation throughout the whole life
cycle is still missing. As described by Leonardi and Cáceres
[14], during zygote formation in U. exuosa subsp. pilifera the
19 hours old cell developed – a primary and secondary cell
wall, shown at low magnication, and although there was an
indication of brillar structure, no details could be discerned.
In another study focused on marine Ulva exuosa [24], high
Ca
2+
concentration resulted in a thickening and smoothing of
the cell wall internal layers, increase in the number of starch
granules, as well as in dimension and the number of cytoplasmic
lipid droplets. It was also evident that in marine Ulva forms
the chloroplast occupies the majority of the cell volume. e
main purpose of this study was to improve our knowledge
of the Ulva exuosa subsp. pilifera cell wall ultrastructure. In
addition, we show dierences in the size and arrangement of
vegetative cells in dependence of thallus age and occurrence
of calcium carbonate precipitates.
Material and methods
Sporophytes samples of Ulva exuosa subsp. pilifera (Kütz.)
M. J. Wynne were collected in the Malta Reservoir (Fig. 1). is
is an articial reservoir, which was constructed for recreation
in 1952 by damming the waters of the Cybina River. The
research was carried out in June 2011 when freshwater Ulva
was in its optimal ontogenetic phase. e material was directly
transferred into laboratory in bottles lled with water from the
sampling locality. Identication was mainly based according to
Bliding [25], Koeman and van den Hoek [2628], Blomster et
al. [29,30], Brodie et al. [31]. e criteria for description and/
or identication of Ulva exuosa subsp. pilifera were as follow:
(i) the macroscopic morphology of the plants (including colour
and texture); (ii) the structure of the basal region of the axis
(and, if present, of branches); (iii) the form and arrangement
of the cells in surface view; (iv) the number of pyrenoids per
cell; (v) the appearance of the chloroplast in surface view; (vi)
the cell size. For transmission electron microscopy (TEM), cells
were xed as previously described [32]. Ultra-thin sections
were cut with glass knives on a Reichert-Jung ultramicrotome
(Austria). Observations and photographs were made with
a TESLA BS 500 electron microscope. Laboratory analysis
included the measurement of thalli (length, width, presence
of proliferations) and examination of the morphology of cells
(length, width and the size of cells, number of pyrenoids, and
the shape and arrangement of cells) with a light microscope
(400×). All the graphics were prepared with the ProCap so-
ware [33]. e basic physico-chemical parameters of the water
(temperature, conductivity, concentration of oxygen, Cl
and
pH) were measured with a YSI Professional Plus handheld
multiparameter meter at the sites where Ulva was growing.
Samples for our physico-chemical studies were collected in
the end of June 2011, whereas Rybak et al. [10] performed the
sampling in April and May 17th, 2011.
Results
In freshwater habitats, and in the Malta Reservoir, the domi-
nant taxon was Ulva exuosa subsp. pilifera. e material was
studied using a combination of classical morphological methods
and ultrastructural techniques. No signicant dierence was
observed in the size of Ulva thalli between young and mature
(ready for sporulation/gametogenesis) specimens. e water
parameters such as depth, pH, electrolytic conductivity, oxygen
concentration, and average concentrations of NO
3−
, NH
4+
,
P-PO
4
3−
, PO
4
3−
, NaCl and Cl
are shown in Tab. 1.
Light microscopy
In the present study, thalli of Ulva exuosa subsp. pilifera
taken from the surface of the Malta Reservoir on 16 June 2011
were varied in size and had many proliferations. alli of the
submerged specimens (young thalli) were from 10.1 to 65.1
cm long and 0.2–1.5 cm wide. Free-oating thalli (mature and
dying thalli) were from 14.9 to 55.1 cm long and 0.5–2.0 cm
wide (Tab. 1). Neither gametes nor zooids were observed in
our material. Vegetative cells contained one parietal, perforated
chloroplast with pyrenoids and transverse cell walls without
plasmodesmata. In the case of cell measurements, all material
was divided into young and mature thalli groups and analyzed
separately. ese measurements showed that in young thalli
rectangular cells were in the range of 32–56 × 20–35 μm and
they formed clear longitudinal rows (Fig. 2, Tab. 2). While in
mature thalli, the cells were less regular in shape 25–48 × 19–31
μm, and the rows were not as distinct as those in young thalli.
An interesting nding was the presence of numerous calcium
carbonate crystals on the surface of the mature thalli cells.
Cells of the Ulva exuosa subsp. pilifera thalli were arranged
in longitudinal and transverse rows. e cells in the specimens
collected from a pond in sampling site Kuciny were slightly
narrower (the lower limits of the width range) compared
to cells of thalli from other localities. Chloroplasts in Ulva
exuosa subsp. pilifera cells, from the Malta Reservoir were
similar to the thalli described from other freshwater sites, and
contained up to four pyrenoids. In our study of Ulva exuosa
subsp. pilifera thalli from the freshwater reservoir, pyrenoids
Fig. 1
Collection sites of Ulva exuosa subsp. pilifera specimens
from Poland.
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Messyasz et al. / Studies on Ulva exuosa subsp. pilifera from Poland
in the upper parts were more distinct than those in the lower
(basal) part. e young cells are thinner compared to mature
cells, therefore their structural feature, in particular pyrenoids,
are easier to focus on.
Electron microscopy
e cell walls were multilayered and had a complex structure
(Fig. 3, Fig. 4). e transverse sections of the outer cell wall
showed from three to six distinct layers enclosed by common
wall layers. Each layer was composed of highly irregular electron
dense brillar network, and limited by thick electron dense lines.
ese layers were of variable thickness, and in most cases were
parallel to each other. e inner cell wall layer, and outer cell
wall layer were very similar in appearance. Outer cell wall layer
was usually thicker than inner cell wall layer, and the structure
of both these layers was less distinct and electron dense than
(Fig. 5a,b). In the Fig. 3a,d and Fig. 5c,d, bacteria embedded in
mucilage either within or outside the cell wall were observed.
Discussion
Of the ve Ulva species, which have been recorded in inland
Polish waters, Ulva exuosa subsp. pilifera is the rarest. Intense
development of this species in the Malta Reservoir was cor-
related with the abundant availability of nutrients in particular
N [9]. ese ndings were consistent with other studies previ-
ously published [510]. When Ulva exuosa subsp. pilifera
was observed for the rst time in 2009 [9], the highest values
of nutrient concentrations in water were twice as high as the
values reported in 2011. e nutrients may have an inuence
on the seasonal uctuation in size of Ulva specimens collected.
Using morphological and ultrastructural analyses, we identi-
ed and examined Ulva exuosa subsp. pilifera occurring in
the Malta Reservoir in Poland. Our results demonstrated the
complexity of the ultrastructure of Ulva exuosa subsp. pilifera
cell wall. However, the function of such a thick cell wall structure
is debatable. One possible explanation is that the thick cell wall
All thalli (n = 120) Young thalli (n = 60) Mature thalli (n = 60)
Lenght of thalli
(cm)
Width of thalli
(cm)
Lenght of cells
(μm)
Width of cells
(μm)
Lenght of cells
(μm)
Width of cells
(μm)
Minimum 10.10 0.20 32.21 20.24 25.09 18.90
Maximum 65.10 2.00 55.81 35.12 47.66 31.56
Average 29.09 0.72 41.99 26.40 35.89 24.66
Standard deviation 10.42 0.42 6.06 3.94 5.01 3.55
Tab. 1 Morphometry of Ulva exuosa subsp. pilifera thalli and cells from the Malta Reservoir.
Fig. 2
a Phase contrast light microscopy of mature cells. b Cells radially arranged around crystals in mature thalli of Ulva exuosa subsp. pilifera.
Factors (mg l
−1
)
Sampling site N-NO
3
N-NH
4
NaCl P-PO
4
PO
4
−3
Cl
Malta Reservoir 0.002 0.10 120 0.10 0.03 73
Tab. 2 Chemical characteristics of the water in the Malta Reservoir (environmental data comes from 2011).
160
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Messyasz et al. / Studies on Ulva exuosa subsp. pilifera from Poland
Fig. 3
Transverse and tangential section of Ulva exuosa subsp. pilifera. a Transverse section of cell wall with bacterium (B) entering cell wall,
electron dense material (Ed). b Tangential section of cell wall layers showing the cell lumen (Cl – inside cell), and appearing more homogenous
cell wall brillar material. c Transverse section of cell wall layers displaying part of cell wall in the process of sheding. d Transverse section of
cell wall layers showing bacterial cells (B) deeply inside the cell wall. Scale bars: 10 µm.
Fig. 4 TEM micrographs of Ulva exuosa subsp. pilifera. a Transverse section showing primary cell wall (Pc), and details of brillar mate-
rial (Mf). b Transverse section of cell wall layers with bacterium (B) inside the cavity in the cell wall, and the electron dense material (Ed).
c Transverse section of inner cell wall layer (Ic), brillar material (Mf). Scale bars: 10 µm.
161
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Messyasz et al. / Studies on Ulva exuosa subsp. pilifera from Poland
may protect the freshwater macroalga against environmental
pollution. Interestingly, abundant calcium carbonate crystals
were recorded on older U. exuosa subsp. pilifera thalli. We
suggest that the crystals of calcium carbonate forming on the
surface of Ulva thalli may have had an inuence on the change
of cells arrangement. As shown in Fig. 2 and Fig. 6, the cells
were oen focused radially around the crystals and interjected
between longitudinal rows. On the other hand, it was suggested
[34] that radially arranged cells can be also found without the
presence of crystals. e occurrence of small radially arranged
cell clusters has previously been noted as a typical feature of
Ulva exuosa subsp. pilifera mature specimens [13,25]. It may
be argued that, the thalli age may correlate with the formation
of folds on the thalli surface, as well as with an increase in thalii
coarseness, a process that can also involve creation of non-
linearly arranged cell clusters. However, further work on the
formation of the large number of calcium carbonate crystals,
and their possible eects on cell arrangement, is still required.
e fact that the cells from the Malta Reservoir were shorter
(at the lower limits of the length range) in comparison to those
observed by Sitkowska [7] from the pond in Kuciny, could be
related to the varied chemical water composition and/or the
availability of nutrient components. e chloroplasts in Ulva
cells, from our samples were similar to the chloroplasts in the
thalli from other freshwater sites, which have been found by
other authors to contain up to four pyrenoids. e number
of pyrenoids per cell has been treated as a distinctive feature
for identication by Griths [17] and Teng et al. [35]. e
applicability of this criterion, however, appears to be rather
limited on account of the diculty with which the pyrenoid
can be eectively investigated with a light microscope (i.e. the
apex cells are usually too small to allow a clear observation of
the pyrenoid). Nevertheless, our observation of the pyrenoid
number per cell (2–4) in mature thalli of U. exuosa subsp.
pilifera appears to be in good agreement with previous studies
[13,25].
e ultrastructure of Ulva exuosa subsp. pilifera cell wall in
general showed similarities to the cell wall of Enteromorpha in-
testinalis [18]. McArthur and Moss [18] studied the early stages
of cell wall formation noting the brillar material in the small
vesicles, and suggested that this material was subsequently used
for the cell wall formation. Such vesicles could not be observed
in our material, which is most likely because of the fact that the
samples contained only adult and/or ageing cells. e layering
in the junction between the outside cell wall and the inner cell
wall shown in a previous study [18] was also present in our
material. Contrary to very regular cell wall stratication with
no visible details within the strata as described for the marine
species Enteromorpha intestinalis by McArthur and Moss [18],
our material revealed highly complex and intricate structures,
shown in Fig. 3Fig. 5. Relatively little information regarding
the cell wall chemistry of freshwater Ulvaceae is available, which
hinders interpretation of the observed structures. Majority of
studies concerning the cell wall of Ulvaceae refer to marine
Fig. 5 TEM micrographs of Ulva exuosa subsp. pilifera. a,b Transverse section of cell wall layers (Cl), the inner cell wall layer (Ic), and outer
cell wall layers (Oc). b Transverse section of the cell wall showing side cell wall (Sc), cell wall network (Cn). c Transverse section of the cell wall
with bacteria (B) embedded in mucilage (Mu) outside the cell. d Transverse section of the cell wall with bacteria (B) inside the cell wall and the
electron dense lines (Ed) which probably delineate the places where the cell wall layers are shed. Scale bars: a–c 5 µm; d 10 µm.
162
© The Author(s) 2013 Published by Polish Botanical Society
Messyasz et al. / Studies on Ulva exuosa subsp. pilifera from Poland
habitats. e chemical composition and structure of the glucan
in the alkali-insoluble cell-wall polysaccharides from the marine
green seaweed Ulva lactuca includes: α-cellulose composed of
glucose, xylose, rhamnose, uronic acid, and sulfate. e last
three components do not appear to be part of the glucan as
they were partially removed by methylmorpholine N-oxide
treatment [36]. e chemical composition of the freshwater U.
exuosa subsp. pilifera cell wall is yet to be determined.
Waite and Mitchell [37] suggested that there is an apparent
close benevolent relationship between Ulva and its surface
microora, although an antagonistic bacterial population also
exists on Ulva surfaces. ese bacteria were found to be capable
of degrading Ulva cell walls, and invading the plant cells. Waite
and Mitchell [37] also postulated that the antagonistic bacterial
population is opportunistic and proliferates when the plant is
placed under stress. ese ndings are in agreement with our
observations, in which the bacteria were found both on the cell
wall surface, and inside the cell wall between the stratication
lines. Spoerner et al. [38] studied the morphology of U. mutabilis
depending on its microbial ora. Certain isolated bacterial
species recovered in combination the morphogenesis of axenic
algal cultures (callus-like morphotype) mediated by specic
regulatory factors excreted. Spoerner et al. [38] argues that
some of those beneciary bacteria might be located in the cell
wall as well. However, each isolated bacterium alone induced
the development of Ulva into thalli composed of cells with
characteristic deciencies. Matsuo et al. [39] isolated, (from
an epiphytic marine bacterium), and characterized a causative
factor for the induction of normal thallus germination and
morphogenesis. Lahaye and Ray [40] found the sugar sequences
in the water soluble polysaccharides from Ulvaceae, also Ray
and Lahaye [41] as well as Robic et al. [42] studied the cell wall
polysaccharides of this group using mid-infrared spectroscopy
combined with chemometric techniques.
Our results present the cell wall ultrastructure in more
details than so far published by other investigators. Although
we did not study the cell wall chemistry, the high complexity
and structural details well corresponds with the cell wall multi
ingredients composition, conrmed by other authors. e fact
that Ulva exuosa subsp. pilifera exists both in freshwater and
marine environment, implies high ecological plasticity of this
species. erefore it would be of interest to continue studies
on its ultrastructure.
Acknowledgments
We are grateful to Prof. Elliot Schubert (Natural History
Museum, London, England) for helpful comments and critical
reading of manuscript. Prof. Beata Zagórska-Marek (University
of Wrocław) for advice on previous dra of this paper. We are
also indebted to both anonymous reviewers for their valuable
comments that signicantly improved the submitted manu-
script. e project was supported by funding from the Polish
Ministry of Science, grant No. NN 304 013 437 and partially
funded by the project GDWB-07/ 2011.
Authors’ contributions
e following declarations about author’s contributions to
the research have been made: wrote the paper: JCM, BM, BU;
eld research: AR, LS, MP; electron microscope analysis: JCM,
AM; english verication: JCM, BM, BU.
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... M. J. Wynne [17] is regularly encountered in freshwaters, but is equally well represented in brackish waters. In Europe, this species was reported from two distinct areas: a salt marsh in the Czech Republic [12] and from ponds and pools with increased salinity in Poland [18,19], Sweden [15], Slovakia [20], Germany [21], Hungary [12], and the United Kingdom [1]. U. pilifera has not until now been observed in Montenegro, although, Kapetanović et al. [22] and Kosanić et al. [23] found two marine ulvalean species U. lactuca and U. intestinalis in the Adriatic Sea. ...
... Molecular analysis confirmed that all of the freshwater and marine specimens occurring for the four sites from Montenegro were indeed U. pilifera. The specimens of the same species Ulva from freshwater habitats in Poland [18] were compared with the specimens from the similar habitats in Montenegro. The neighbour joining (NJ) and parsimony analysis (MP), as presented in Figures 5 and 6, were congruent with maximum likelihood (ML), considering bootstrap proportions (BP) from ML, NJ, and MP demonstrated at the nodes. ...
... Morphological characteristics of Ulva pilifera from Montenegro and Poland[18]. ...
Article
Full-text available
The paper presents four new sites where bright green Ulva thalli were found inhabiting freshwater (a river, a ditch, the Milet Canal) and marine (on the rocky shore of the Adriatic Sea) habitats in Montenegro. The aims of this study were to determine, for the first time, whether specimens of Ulva pilifera collected in Montenegro are phylogenetically and morphologically the same species as the one occurring in Europe. Using total reflection X-ray fluorescence (TXRF) and wavelength dispersive X-ray fluorescence (WDXRF) techniques it assessed the elemental composition of their thalli and its influence to colonise new habitats. Elements: Al, As, Ba, Br, Ca, Cl, Cr, Cu, Fe, Hf, I, K, Mg, Mn, Na, Ni, P, Pb, Rb, S, Si, Sr, Ti, V, and Zn were determined. The highest elemental concentrations were found for Ca = 16.3% (using WDXRF) and for Sr = 292 ppm (using TXRF) in the Ulva thalli. Ulva pilifera analysed from Montenegro, based on classical morphological methods and molecular techniques, are closely related to the same species from inland and coastal waters throughout Europe. The analysis of trace elements showed that the metal content in Ulva thalli is correlated with the trace elements in water and sediments. Ulva pilifera fits numerous features that make it one of the bioindicators of marine pollution, thanks to its worldwide distribution and capacity to accumulate trace elements.
... In recent study on young and mature thalli of E. flexuosa the shape of cells and their arrangement was found to be different. In young thalli they were rectangular in shape and their rows were distinct whereas, in mature thalli the cells were less regular and the rows were not distinct (Messayasz et al., 2013). ...
... In recent study on young and mature thalli of E. flexuosa the shape of cells and their arrangement was found to be different. In young thalli they were rectangular in shape and their rows were distinct whereas, in mature thalli the cells were less regular and the rows were not distinct (Messayasz et al., 2013). ...
... Ulva flexuosa ssp. pilifera, a fresh-water variant, was also reported to occur in a region of high nutrient concentration (Messyasz et al., 2013). ...
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Invasive alien species, on successful establishment, can displace native species. The threat of invasive species arises in view of their ability to outcompete and destabilize native biodiversity. Invasive species are found across all taxonomic groups of plants, animals and microorganisms. The green macroalga Ulva flexuosa has a potential to become invasive and this species was investigated for its hitchhiking potential under laboratory conditions. Zoospores of U. flexuosa were maintained at 4°C for nearly 10 months in the dark. Recruitment potential of zoospores after dark stress was tested in a modified Provasoli medium under optimal laboratory conditions. The success rate of zoospore recruitment was 61%. The paper describes the transfer potential through shipping activities by correlating the Ulva zoospores recruitment potential and survivability.
... U. flexuosa belongs to Ulvophyceae, with thalli composed of uninucleate cells, and is difficult to be set apart from species among Ulva spp., since the latter is often sheet like in external morphology [5]. Furthermore, the vegetative cells arrangement of the mature thalli show tendency towards distortions determined by the calcium carbonate crystals which increase the difficulty for identification [6,7]. Then, the rRNA ITS region, 5S and partial rbcL gene sequences are applied to demonstrate sequence variation within species or even subspecies [2,8]. ...
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Ulva flexuosa, one kind of green tide algae, has outbroken in the Yellow Sea of China during the past ten years. In the present study, we sequenced the chloroplast genome of U. flexuosa followed by annotation and comparative analysis. It indicated that the chloroplast genomes had high conservation among Ulva spp., and high rearrangement outside them. Though U. flexuosa was closer to U. linza than U. fasciata in phylogenetic tree, the average Ka/Ks between U. flexuosa and U. linza assessed by 67 protein-coding genes was higher than those between U. flexuosa and other species in Ulva spp., due to the variation of psbZ, psbM and ycf20. Our results laid the foundation for the future studies on the evolution of chloroplast genomes of Ulva, as well as the molecular identification of U. flexuosa varieties.
... For these reasons, taxonomically Ulva is complicated macroalgal group and usually confused with Enteromorpha genus; they are used as synonyms. If the differentiation of both genus is required, it would be necessary genetic and/or ultrastructure studies [8]. ...
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Use of seaweed by humans is an ancient practice. In Asian countries, the use of them in human and animal feed, traditional medicine, and compost in agriculture is well documented. Since the twenty-first century begins, the scientific interest for seaweed had increased in Occidental countries. Ulva or Enteromorpha is a green macroalgae genus that raises and cultivates around the world. It has salinity tolerance and growth with diverse nitrogen ratios, be able to farm them in aquaculture systems. Scientific studies seen in this genus an interesting profile of chemical compounds: The protein is similar in quantity and quality to soy or some animal products; dietetic fiber percentage is elevated (>40%), being around 40% soluble fiber of them. In addition, fiber fraction presents Ulvan, a complex sulfated polysaccharide that presents antiviral, antihyperlipidemic, and antidiabetic effect in animal assays. Moreover, antioxidant and phytochemical profile has not being totally elucidated, giving important opportunities to scientific community for explode consciously this biological resource.
... Indeed, bacteria were recently identified by TEM in Ulva flexuosa subsp. pilifera ( Messyasz et al., 2013). Rhizoid cells have to attach to the substratum by an adhesive polyglycoprotein ( Callow and Callow, 2006) for the formation and maintenance of this cross-kingdom assembly. ...
... Also, marine species of Enteromorpha genus, especially E. intestinalis were reported in inland athalassic salty lakes (Savage 1964, Taft 1964, Pfiester et al. 1976, Conner et al. 1978, Hammer 1981, Reinke 1981, Hammer & Heseltine 1988, Eimanifar & Mohebbi 2007, Kaštovský et al. 2010, Gheorghievici et al. 2015, Messyasz et al. 2013, hypersaline springs and rivers (Velasco et al. 2006, Millán et al. 2011, streams and lagoons receiving effluents from salt mines (John & Rindi 2015). However, based on literature review, the most widespread species of Enteromorpha genus in inland waters is E. intestinalis. ...
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Three new sites of Enteromorpha intestinalis have been found in the drainage basin of the Slănic River located in the Subcarpathians region, salt Meledic Plateau. E. intestinalis is a cosmopolitan macro green alga species with tubular thali that is primarily found in the coastal zone, including the Romanian Black Sea coast. Due to its salt tolerance this alga it was found in some inland waters, both fresh and saline waters courses and limnic waters that are often positively correlated with cultural eutrophication. These new reported localities of E. intestinalis in inland waters from this saline region contribute new and essential information about the distribution of this originally marine species on the inland area of Romania.
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As a biocompatible polymer, ulvan has applications in countless fields. Therefore, the following study intends to extract ulvan from Ulva fasciata, emphasizing its use for biomedical and industrial applications in the manufacture of nanofibrous webs. The extracted ulvan was characterized using FT-IR, DSC, XRD, GPC, and NMR. The extracted ulvan's FT-IR spectra confirmed that it is a sulfated polysaccharide. The HPLC analysis showed that the extracted ulvan is composed of rhamnose, xylose, glucose and glucuronic acid. NMR showed that the proton chemical shifts at 1.3 are due to methyl protons of rhamnose 3-sulfate in the ulvan samples. The X-ray diffractograms suggested that the extracted ulvan is semi-crystalline polymer with major crystalline reflection at 2θ of 29.4°. Deionized water has been successfully used to produce ulvan/polyvinyl alcohol (ulvan/PVA) nanofibers as an eco-friendly solvent. It was found that the ulvan-to-PVA (1:2) ratio results in nanofiber that is well handled and smooth. In addition to pretreated ones, the ulvan extracted without organic solvent pretreatment showed bead free nanofibers. It is concluded that pretreatment with organic solvent in ulvan extraction, particularly in the manufacture of nanofibers, is not recommended. In addition, the resulting nanofibrous mat has sufficient mechanical properties for various applications to be incorporated.
Chapter
The eutrophication, or nutrient enrichment, of coastal waters as a result of man’s activities is now widely recognized as a major, world-wide pollution threat. Essentially, the increased anthropogenic source of inorganic plant nutrients interferes with the natural annual nutrient cycles and can artifically enhance primary production during periods when activity is normally low. This can have quite considerable ecological consequences for both pelagic and benthic organisms. For example, phytoplankton activity will be increased (Hoogweg et al. 1991) and, although this can be generally beneficial by increasing fisheries (Raymont 1947; Fonselius 1978; Elmgren 1989), there is some evidence that it has resulted in the occurrence of some phytoplankton blooms, both toxic and non-toxic, which have had serious effects on local fisheries and leisure activities (Braarud 1945; Ruud 1968; O’Sullivan 1971; Zou and Dong 1983; Rosenberg 1985; Kimor 1991). One such bloom occurred in the northern Adriatic in 1988 when large quantities of mucilaginous material was washed up on many tourist beaches (Degobbis 1989; Vukadin 1991). A number of authors have similarly speculated on the possible relationship between eutrophication and the occurrence of toxic blooms of microalgae in the North Sea (Cole 1972).