The occurrence of
(Ectocarpaceae, Phaeophyceae), as epi-endophyte of
(Rhodymeniales, Rhodophyta), described from Santa Isabel, Rawson, Argentina.
grows in the host tissues forming epi-endophytic relationship in the epidermal, cortical and medullar layers. Epiphytic thalli of
were unbranched filaments emerging from hostis surface. Reproductive structures of
on the host were absent. On the contrary, free cultured individuals formed different reproductive structures. Macrozoosporangia containing a single large motile zoospore originated from vegetative cells, they were conical to cylindrical in shape, 30-50 μm in length and 18-20 μm in wide. Uniseriate plurilocular zoosporangia were cylindrical shape, 40 μm in length and 10-13 μm in wide. Sexual fusion was not seen. In mixed cultures of
infected the host, grew as in natural host and, formed macrosporangia between host subcortical cells. Gametophytes of
were filaments with diffuse growth, branched with a branch pattern alternate or opposite. Gametangia were plurilocular, uni or biseriate and lateral. When mature they contained 2 to 6 isogametes. The presence
could be defined as an epi-endophytic relationship. The percentage of infection of
was 34%.A25% of the infected thalli presented a low, non-symptomatic level infection, whereas a 62% and a 13% of them exhibited respectively moderate and high indexes of infection.
Greville includes species with traditional used in human nutrition in Ireland and Brittany and more recently marketed as a health food (Le Gall
(L.) Kuntze contains as much as 35% proteins and is a rich source of vitamins and eicosapentanoic acid (Mishra
. 1993) and was identified as one of the three red algal species with the best potential for seaweed cultivation in the northeastern United States and Canada (Cheney 1999). Due to its high protein content (Morgan
. 1980; Fleurence 1999),
sp. was considered as a good food source for abalone aquaculture (Evans and Langdon 2000; Rosen
(Lamouroux) Silva is an important species of tidal and subtidal algal communities in the southern coasts of Argentina (Mendoza and Nizovoy 2000). Its fronds are flattened, fan-shaped, rather stiff, light brownish ? red fronds, with long or short stipes arising from a discoid base. Fronds are repeatedly dichotomously lobed, with axils wide, apices rounded and margins smooth.
This study is a part of a more general study in which we are focused on the identification of the most common epiphytes infecting the host
on southern coasts of Argentina. We found the occurrence of
Kawai & Tokuyama.
was first described on
Areschoug from Japan (Kawai and Tokuyama 1995) and it is known in Europe only from Helgoland (Peters and Ellertsdottir 1996).
Algal species growing on or within other algae has been widely reported (Goff 1982; Ducker and Knox 1984; Correa
. 1988, 1993; Correa 1990; Correa and McLachlan 1991, 1992, 1994). Are goals of the present paper to assess the kind the symbiosis interactions and the relative abundance including the estimation of the severity index of infection of
. It was also a goal to study the biology of
under both nature and culture conditions.
MATERIALS AND METHODS
fronds were obtained from subtidal populations from the coast of Santa Isabel, (43°18’S-65°06’W) in the province of Chubut, Argentina during December, 2004. A collection of 30 randomly selected fronds was used for the present research.
- Estimation of the severity index of infection
Host thalli of
) were divided in apical, intermediate and basal sections for their examination. Size, presence and position of individuals of
and severity degree of infection were registered for each frond. In order to evaluate the severity degree of infection, a qualitative scale was used (Peters and Schaffelke 1996). This scale resulted from the visual categorization of a dissection observed by light microscopy. Prevalence (i.e., percentage of thalli that were infected) and severity of infection (i.e., mean abundance of
on each host thallus) were then estimated. A ‘severity index’ was based on a semi-quantitative estimation of L. elsbetiae cover on host thallus using four categories, where 0 = a total absence of epiphytes, 1 = 1-30% cover, 2 = 31-70% cover, and 3 = 71-100% cover. The severity degree of infection was categorized as low when the percentage of host thalli colonized by L. elsbetiae ranged from 1% to 10% (i.e., no visible signs of endophytic infection were observed). The severity degree of infection was categorized as moderate when the percentage of colonized thalli varied from 11% to 70% (i.e., moderate alterations, such as brown spots on the lamina, were observed). Finally, the severity degree of infection was categorized as high in those cases in which thalli exhibited a colonized area percentage higher than 71% (i.e., strongly invaded thalli were observed). The distinction between the categories was arbitrary. Only those thalli under the categories ‘moderate’and ‘high’were considered diseased.
- Isolation ofLaminarionema elsbetiaeand unialgal cultures
After being collected, fronds were kept on ice, retained in labeled plastic bags until they were examined in the laboratory, usually within 5 h after collection. Fronds were brushed and rinsed under running tap water. Small portions of infected fronds were sectioned, then immersed in fresh 0.5% solution of sodium hypochlorite for 30 s, and finally rinsed three times, 5 min each, in sterile seawater. A 2-min sonication was subsequently applied to 5 mm x 5 mm portions in sterile seawater, renewing the seawater after each burst. This cleaning procedure was followed in order to remove diatoms as well as other epiphytes.
crude cultures were initiated by inoculating portions of cleaned fronds in plastic Petri dishes containing Provasoli enriched seawater (PES) medium (Provasoli 1968). Cultures were maintained at 21 ± 1℃ with an illumination regime of 12 : 12 h light-dark (LD), with a photon flux density of 15 μmol m
. Germlings were obtained either from swarmers or from outgrowths of the endophytes from infected thalli. They were subsequently segregated into unialgal cultures and maintained under the above-mentioned conditions with weekly changes of the medium. A 2.5% germanium dioxide solution (Across Organics, Gell, Belgium) dissolved in water was added to avoid diatom contamination (Lewin 1966; Christensen 1982).
by selected isolates of
initially established from swarmers were experimentally carried out. Eight to ten 1-1.5 cm long fragments of fronds of the host were placed into plastic Petri dishes. Two replicates of each isolate were incubated under laboratory conditions during a period from 2 to 3 weeks.
- Morphological studies and semi-thin sections
Cytomorphometry was carried out using a stereoscop-ic microscope Wild-Herbrugg and an inverted micro-scope Nikon Eclipse TE 300, with anoptral phase contrast and differential interference contras) and with an incor-porated camera Nikon FDX 35. Either the presence or absence of epi-endophyte filaments was determined under light microscopy in semi-thin sections of thalli of
. In order to obtain semithin sections, thalli were fixed in 2.5% glutaraldehyde (Fisher Bioreagents, Fair Lawn, Ny, USA) in seawater for 2 hr at 4°C, and postfixed in 1% (OsO
) Osmium tetroxide (Across Organics, Gell, Belgium) in sea water for 2 hr at 4°C. The material was dehydrated in a graded acetone series (Merck, Darmstadt, Germany) and embedded in Spurr’s low viscosity resin (SPi Supplies Divisi, of Strutur pProe, Inc., West Chester, PA, USA). Sections were obtained with glass knives on a Reicher Ultracut OM U2 ultramicrotome (Reicher, Vienna, Austria). The resin was removed using a metallic sodium, benzene and methyl alcohol solution (Hayat 1986). Sections were stained with a combination of colorants, namely haematoxiline (Biopur, Rosario, Argentina) - malachite green (Biopack, Buenos Aires, Argentina) - basic fucsine (Britania, Buenos Aires, Argentina) (1 : 1 : 1) (Berkowitz
- Chromosome counts
Chromosome counts were made using unialgal cultures of
. Thalli were fixed either in 1 : 3 mixture glacial acetic acid (Cicarelli Laboratorios, San Lorenzo, Argentina) /absolute ethanol (Cicarelli Laboratorios) or in 6 : 3 : 1 mixture formaldehyde (Cicarelli Laboratorios) - absolute ethanol (Cicarelli Laboratorios) - glacial acetic acid (Cicarelli Laboratorios) at 5℃ during a period of 2 to 24 h. Postfixation was carried out with 70% ethylic alcohol (Cicarelli Laboratorios). The material was subsequently hydrolyzed for 30 min in 1 N hydrochloric acid (HCL) (Cicarelli Laboratorios) at room temperature, stained with Schiff stain in darkness for 2 h (Johansen 1940), bleached during 20 min in a 1 : 3 : 3 mixture of sodium metasulphite (Cicarelli Laboratorios): 1 N HCL: distilled water, washed with distilled water for 30 min, and finally mounted in a drop of a 2% acetic acid solution of ferric haematoxylin (Biopur) with added iron acetate (Biopur) (Nunez 1968).
- Scanning electron microscopy
filaments were fixed in 2.5% glutaraldehide (Fisher Bioreagents)-seawater at 5℃ in cacodilate buffer (Biopur) for 2 h. They were subsequently mounted on slides covered with 0.5% poly-D-lysine and dehydrated in a graded acetone series. Samples were finally critical point dried during 1 h, coated with gold, and observed with a Jeol 35 CF scanning electron microscope (Jeol, Tokyo, Japan).
Prevalence, severity index and localization of infection ofR. pseudopalmatathalli byL. elsbetiae
Prevalence, severity index and localization of infection of R. pseudopalmata thalli by L. elsbetiae
- Prevalence and severity index infections
The percentage of infection of
was 34%. A 25% of the infected thalli presented a low, non-symptomatic level infection, whereas a 62% and a 13% of them exhibited respectively moderate and high indexes of infection and presented dark patches on the host’s surface as a visible symptom of the presence of dense bushes of L.
A 41% of the infected fronds
individuals in the basal region, whereas a 21% and a 38% of them exhibited them in the median and the apical regions respectively
- Morphology ofLaminarionema elsbetiaeindividuals growing onRhodymenia pseudopalmatathalli both in nature and after experimental infections
Vegetative filaments of
thalli were uniseriate. Those growing on the cuticle (
) were postrate, regularly arranged with thick cellular walls and in some sectors observed in 2 or 3 levels (
). Also erect filaments were observed formed by few cells (
). Those developing amid epidermic cells of the host (
) also formed a fine net flanked by both cortical and medullar cells (
). In both areas, cortical and medullar, vegetative filaments did not penetrate into the host’s cells. Filaments were irregularly branched and showed apical growth (
). They were formed by cylindrical cells (Fig. 7) 50-60 μm in long and 7-13 μm in diameter. These cells contained 1 or 2 discoid or irregularly elongated chloroplasts with a single pyrenoid. Filaments invaded the host tissues penetrating through intercellular spaces of the cortical region (
) up to the medulla (
). Reproductive structures of L. elsbetiae on the host were absent. Under scanning electron microscope the cells of L. elsbetiae exhibited delicate surface ornamentation on the walls (
Rhodymenia pseudopalmata. Thallus recollected from the nature.
Semi-thin section of R. pseudopalmata thallus, showing both epiphytic monostromatic (arrow white) and endophytic (arrow black) L. elsbetiae filaments.
Semi-thin section of R. pseudopalmata thallus, with 2 or 3 layers of L. elsbetiae cells on your surface.
Epiphytic L. elsbetiae thallus with erect filaments formed with few cells.
Laminarionema elsbetiae on host thalli.
Detail of L. elsbetiae thalli. Epiphytic filaments showing the pyrenoids (arrows).
Transversal section of R. pseudopalmata showing endophytic filament of L. elsbetiae between both cortical and medullar regions (arrows).
Endophytic filaments L. elsbetiae irregularly branched (arrow), penetrating directly crossing cortical region to medullar area.
Endophytic filament L. elsbetiae, formed by short, curved filaments formed by two cells (arrows).
Photomicrograph under scanning electron microscopy (SEM) showing shorten filamentepiphytic L. elsbetiae on R. pseudopalmata’s surface.
Detail of wall cell of epiphytic filament L. elsbetiae under SEM.
- Development and morphology of free thalli ofLaminarionema elsbetiaein culture conditions
After a week of growth, sporophytes exhibited a postrate basal system and also a less developed erect system
. Both system presented diffuse growth. Cells of the first system were ovoid with a length of 10-20 μm (12.6 ± 2.5 μm, n = 30) and a wide of 7-13 μm (10 ± 1.5 μm, n = 30). These cells presented various parietal, discoid or ribbon-shaped plastids with pyrenoids
. The second system were formed by cylindrical cells, 5.4-21 μm (11 ± 33 μm) (n = 30) in length, 7.7-13 μm (8.7 ± 1.4 μm, n = 30) in wide. Macrozoosporangia originated from vegetative cells of the postrate system were observed
. They were both intercalar and terminal, presented an ovoid shape and a length of 30-50 μm and a wide of 18-20 μm
. In each macrosporangium a single macrozoospore was formed
, which was released through an apical aperture. Macrozoospores presented positive phototaxis. They were pyriform, 18-20 μm in length and 10-13 μm in wide and exhibited two plastids and stigma
. Flagella were of equal lengths and were laterally inserted adjacent to the stigma.
In most of the thalli uniseriate plurilocular zoosporangia were observed
. They were sessile with ovoid to cylindrical shape and they presented ca. 40 μm in length and 10-13 μm in wide. These zoosporangia were formed in terminal vegetative cells. In them unispores or microzoospores were observed
. The unispores were released from loci through an apical pore
they presented an ovoid chloroplast with a stigma in its anterior end (Fig. 20). They were biflagellate and 4-8 μm in wide. More of 18 microspores per every unilocular sporangium were formed
. These microspores were smaller than macrospores and presented a faster motion. Macrosporangia and uniseriate plurilocular zoosporangia were formed in different thalli.
Sporophytic filaments L. elsbetiae constituted by both basal system with postrate cells and erect system.
Detail de cells showing plastid (arrow black) and pyrenoid (arrow white).
L. elsbetiae thalli arising macrosporangium (arrow) in its postrate system.
Detail of macrosporangium.
Unilocular sporangium showin unispores inside.
Release of unispores through an apical pore.
L. elsbetiae gametophytic thalli formed by microscopic branched filaments.
Detail of cells of gametophytic thalli.
L. elsbetiae plurilocular biseriate gametangia of lateral position.
L. elsbetiae plurilocular uniseriate gametangia of lateral position, with apical pore.
Photomicrograph showing gametophytic thalli under SEM.
Metaphasic plate with 10 chromosomes.
Representation of Fig. 26.
Metaphasic plate with 5 chromosomes.
Representation of Fig. 28.
were filaments with diffuse grow, branched with a branch pattern alternate or opposite
. Basal cells were 8-26 μm (11.7 ± 4 μm, n = 50) in length and 3.7-11 μm (9.6 ± 3.7 μm, n = 50) μm in wide. Distal cells were 3.7-43.6 μm (15.2 ± 3.5 μm, n = 50) in length and 3.7-25.9 μm (8.9 ± 1.7 μm, n = 50) in wide
. Both type of cells had two or three plastids with pyrenoids
Gametangia were plurilocular, uni or biseriate and lateral. They were 31.4 μm (15-46 μm) in length and 12.9 μm (7.7-25 μm) in wide
. Gametangia loci were 5- 6 μm in length and 7-8 μm in wide. When mature they contained 2 to 6 isogametes with a size 4-6 x 4-6 μm. Gametes presented 1 or 2 plastids and stigma. They were released from a pore located in the apical end of gametangia
. Gametes showed positive phototaxis.
- Chromosome counts
Chromosomes were ovoid. L. elsbetiae’s sporophytes presented a number 2n = 10 (Figs 26, 27) and gametophytes n = 5 (Figs 28, 29).
Kawai and Tokuyama (1995) considered L. elsbetiae a representative of the order Ectocarpales because of its morphology and plastid type. Peters and Ellertsdottir’s (1996) observations of sexuality, a slightly heteromorphic life history and isogamy are congruent with this criterion.
This work represents the first report of
in America, since this species only had been reported for Japan (Kawai and Tokuyama 1995) and Germany (Peters and Ellerrsdottir 1996). In 1995, Kawai and Tokuyama described
as a new endophyte kelp of northern Japan. In Europe
was detected infecting
(Linnaeus) Lamouroux with high prevalences (Ellertsdottir and Peters 1997). In Muroran, Japan,
is common in adult Laminaria sporophytes, although they were not found in Costaria Greville and Undaria Suringar, which also grow in the same locality (Kawai and Tokuyama 1995).
Kawai and Tokuyama (1995) observed under culture condition that
also infected sporophytes of
Bachelot de la Pylaie, which is less related to
, and suggested that probably
did not show high host specificity and was potentially able to infect many other Laminarialean species in nature. The presence of
confirmed their predictions of low specificity of this species, not only by its capacity of infection to Laminarialean species, but also to seaweeds of different algal classes. Nevertheless here, in Argentina
was never observed on
(Harvey) Suringar sporophytes whose fronds, in turn, were infected by another brown endophyte,
(Rosenvinge) Peters (Gauna
infection is widespread throughout different populations of
from Argentina (Gauna 2005). In this particular Patagonian population, the infection levels observed did not reach the high intensities reported by Peters and Ellertsdottir (1996) in populations
, with prevalences there of ca. 93% in the 53% of the population. In fact, here only a 13% of the
population presented the highest level of prevalence.
We found here differences with the representatives of
of Japan (Kawai and Tokuyama 1995) and Germany (Peters and Ellertsdottir 1996). Given the great plasticity of members of Ectocarpales (Muller 1967) we considered them inside a normal intraspecific variability. Vegetative cells of sporophytes of
(Peters and Ellertsdottir 1996) were a little shorter than those of the Patagonian isolates and their cellular features are in agreement with those described by Kawai and Tokuyama’s (1995) in Japan. On the contrary, when comparing reproductive structures we found conspicuous differences, i.e., unilocular sporangia of
were decidedly smaller than those of
from Helgoland (Peters and Ellertsdottir 1996) and Japan (Kawai and Toyuyama 1995). In addition, in the sporangia from the Argentinian sporophytes not more than 18 microspores were observed, while in sporophytes from
(Peters and Ellertsdottir 1996) zoospores are more than 68. And finally, macrosporangia of thalli isolated from
are smaller than those observed by Kawai and Tokuyama (1995) and consequently macrozoids of the Patagonian thalli were shorter than those observed in Japan. With relation to the cellular dimensions of gametophytes, they are in agreement with the dimensions of central cells of the thalli of Patagonian
. The loculi of the gametangia observed in our samples were larger than those observed in
We have not observed the formation of reproductive structures of
in nature during summer. No fertile structures were also observed during summer and other seasons (winter and autumn) by Peters and Ellertsdottir (1996). These authors observed the formation during May (spring in the North hemisphere) of macrosporangia that protruded slighty from the meristoderm of the host and they hypothesize that during this season
rapidly spreads in the host population by means of direct reproduction of sporophytes.
Despite that we did not observe fusion of gametes, by means of chromosome counts we could find out in the present populations of
the presence of two heteromorphyc generations with both haploid and diploid levels of ploidy indicative of a diplobiontic life cycle. Gametophytes were not clearly observed in the field but they were experimentally isolated from hosts’ fronds. The firm adherence of them to the substrate and the fact that they never developed from isolates started with filaments from internal tissues of infected hostsmay indicate that the idea of Peters and Ellertsdottir (1996) in the sense that gametophytes of
has epilithic or epiphytic but not endophytic growth habit is correct.
Field and experimental observations indicate that the infection of
is transferred from one frond of
to another by spore discharge into the surrounding medium. Collected material, on which recently settled zoospores and germlings were found, the subsequent development of the infection in areas of the fronds took place. As Heesch and Peters (1999) did, we observed that
successfully enter into the host and developed as interstitial filaments, but the mode of entry into the host tissue has not been accurately verified.
The nature of interactions between
remains to be undoubtedly established. In some instances
caused little perturbation of the
tissues. In other cases we have noted the complete replacement of the host cortical tissue. Similar distortions of host have been observed especially by species of
(Andrews 1976; Yoshida and Akiyama 1979). Epiphytes are usually defined as organisms that grow on plants, but do not derive nutrients from their hosts (Linskens 1976). Linskens (1963) named two kings of epiphytes: holo-epiphytes, organisms attached to the outer layers of the host and amphi-epiphytes, organisms deeply anchored in the tissues of their hosts. Also, Linskens (1963) suggested that the type of anatomical contact is highly variable and that it is determined by the nature of the partners. Endophytism has been defined as the type of symbiosis in which an organism lives within the tissues of a plant host (Correa
. 1988). Other authors, such as Lewis (1973); Starr (1975); Goff (1982); Lewin (1982); Smith and Douglas (1987) and Douglas and Smith (1989) have also used the term endophytism in the same sense. A wide variety of algae that infect other algae from an anatomical point of view are a continuum between epiphytes and endophytes. Therefore they are named epi-endophytes. In general, epi-endophytes are pigmented algae photosynthetically independent with almost no metabolic relation with their hosts. For that reason many of them can be isolated from their hosts and subsequently be cultivated under laboratory conditions (White and Boney 1969, 1970; Boney 1972; Garbary 1979; Nielsen 1987; Gauna
. 2009). In this sense the presence
could be defined as an epi-endophytic relationship.
MCG has a fellowship of the Consejo Nacional de Investigaciones Cientificas y Tecnicas de la Republica Argentina (CONICET). ERP is Research Member of the Consejo Nacional de Investigaciones Cientificas y Tecnicas de la Republica Argentina (CONICET). EJC is Research Member of the Comision de Investigaciones Cientificas de la Provincia de Buenos Aires, Republica Argentina (CIC). The Secretary of Science and Technology of the Universidad Nacional del Sur provided funds by grant PGI CSU-24 B/145 to ERP.
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