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Department of Biology and Chemistry, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong Special Administrative Region, The People's Republic of China
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Zoospores of mangrove isolates of Schizochytrium mangrovei KF6, KF7, KF12 (three strains), Thraustochytrium striatum KF9 and Ulkenia sp. KF13 were examined for their chemotactic responses to amino acids, carbohydrates, ethanol, and leaf extracts using a capillary root model. Most leaf extracts of mangrove plants and a marsh grass tested were shown to induce moderate chemotactic responses in zoospores of both S. mangrovei KF6 and Ulkenia sp. KF13. Of the remaining amino acids and carbohydrates evaluated, glutamic acid and pectin induced strong attraction in zoospores of S. mangrovei KF6 and Ulkenia sp. KF13, suggesting these are the major components in leaves which may be responsible for the chemotactic response of thraustochytrid zoospores in nature. Zoospores of T. striatum KF9, in general, showed a weak chemotactic response to all the tested compounds and extracts except cellulose, which elicited a moderate response. The ecological significance of the data presented is discussed.
Key words: chemotactic response, Schizochytrium mangrovei, thraustochytrid zoospores, Thraustochytrium striatum, Ulkenia sp
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). In mangrove environments, these marine microbes are found associated with decaying mangrove leaves (Findlay et al 1986) and can also colonize, penetrate, and decompose mangrove leaves by their degradative enzymes (Bremer 1995, Raghukumar et al 1994, 1995). Reproduction in thraustochytrids is normally by the formation of biflagellate, heterokont, zoospores from zoosporangia (Moss 1986). Zoospores, the primary dispersal units of zoosporic organisms, possess flagella, which enable them to selectively accumulate at or avoid a site through the reorientation of zoospore swimming direction (Carlile 1993).
Among the various forms of tactic responses, chemotaxis has been the main focus of research. It has been intensively studied in relation to the detection and response of fungal zoospores to environmental cues for subsequent colonization and utilization of a suitable substrate (Carlile 1993). Most of the chemotactic studies have been focused on pathogenic and saprophytic species: Achlya species (Thomas and Peterson 1990), Allomyces species (Carlie and Machlis 1965, Pommerville 1977), the nematode-parastic fungus Catenaria anguillulae Sorokin (Jansson and Thiman 1992), Halophytophthora vesicula (Anastasiou & Churchl.) H. H. Ho & Jong (Leaño et al 1998), the rumen fungus Neocallimastix frontalis (Braune) Varva & Joyon ex Heath (Orpin and Bountiff 1978), Phytophthora species (Allen and Newhook 1973, Cameron and Carlile 1978, Halsall 1976, Tyler et al 1996), root infecting strains of Pythium species (Donaldson and Deacon 1993, Goldberg et al 1989, Jones et al 1991, Royle and Hickman 1964a, b), a marine chytrid Rhizophydium littoreum Amon (Muehlstein et al 1988) and fish-egg-pathogenic strains of Saprolegnia diclina Humphrey (Rand and Munden 1993). However, there are no reports on the chemotactic response of zoospores of thraustochytrids. Therefore, the aim of this study is to investigate the chemotactic response of zoospores of selected thraustochytrids to different compounds and leaf extracts in their immediate environment to enhance our understanding of the role of thraustochytrid zoospores in mangrove ecosystems.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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A modified capillary root model by Royle and Hickman (1964a) as described by Halsall (1976) was used. Capillary tubing (1 mm external diameter) was bent into uniform angular U-shape by heating, and sealed at both ends to form the assay chamber. This bent tube was placed on a glass slide and overlayed with a coverslip to form the chamber (approximately 10 mm x 10 mm x 1 mm) with one open side through which the zoospore suspension was introduced. Test compounds were dissolved in deionized double distilled water, filtered through a 0.2 µm disposable filter unit and mixed with molten 2% agar at 1:1(v/v) ratio. Final test concentrations were: amino acids and sugars = 100 mM; polysaccharides = 2.5 mg/mL; fresh leaf extracts = 100 mg/mL. One percent (1%) agar was used as a control. Capillary tubes (1 mm external diameter) were filled with the molten mixture of the test attractants up to 15–20 mm in length and allowed to solidify before use.
For ethanol, an initial concentration of 5% was used. The ethanol solution was drawn into the capillary tube following the procedure described by Morris et al (1995). One end of the capillary tube was heat-sealed, and while the tube was still hot, the tube was plunged into the ethanol solution, allowing the liquid to be drawn up into the tube as it gradually cooled. The filled tube was then used immediately for the chemotaxis assay.
The zoospore suspension introduced into the chamber was allowed to stabilize for one minute before the test attractants in the capillary tube were introduced. Ten minutes after the introduction of the test compounds, accumulation of zoospores at the mouth of the capillary tube was observed under a microscope (4x objective) and photomicrographs taken. Motile zoospores/encysted spores were scored on the photograph within an area corresponding to 0.5 mm2 on the slide near the mouth of the capillary tube. The chemotactic ratio was determined according to the formula described by Halsall (1976): Chemotactic Ratio (CR) = scores on test attractant/mean score on control.
Positive chemotactic responses were further graded into: weak (CR = 1.1–3.0), moderate (CR = 3.1–10) or strong (CR = >10.1) according to Leaño et al (1998). Chemotactic ratios of compounds were analyzed using analysis of variance (ANOVA). Significant differences among means were compared using the Student Newman-Keuls test. Glutamic acid, asparagine, pectin, and leaf extracts of Kandelia candel elicited a response in the upper moderate range of chemotactic activity from zoospores of Schizochytrium mangrovei KF6 and Ulkenia sp. KF13. These species were then selected for further threshold level determination. Concentrations of amino acids were tested from 0.1 to 100 mM while green Kandelia candel leaf extract was tested from 0.1 to 100 mg/mL. For pectin, concentrations tested were from 0.05–2.5 mg/mL.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, is a phenomenon where zoospores only approach a certain distance towards a capillary tube before being repelled because of high concentration of the compound or unfavorable pH, and form an arc around a zone free of zoospores. This phenomenon was not observed in thraustochytrid zoospores in response to test compounds, but was observed in zoospores of Oomycota (Leaño et al 1998).
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Ulkenia sp. KF13 zoospores showed moderate chemotactic response to the leaf extracts tested (CR 3.71–5.09), similar to those of S. mangrovei. The amino acids asparagine, cysteine, and glutamic acid showed moderate zoospore attraction, while a weakly positive response was observed with the remaining amino acids. Of the tested sugars, only pectin elicited a strong chemotactic response, while weak responses were observed for the saccharides (Table II and Figs. 3–7). Ethanol gave a weak response to zoospores of the five thraustochytrids (Table II).
Comparison of the chemotactic ratios of all the tested compounds using the Student-Newman-Keul's test on zoospores of the three S. mangrovei strains showed that, in general, green leaf extracts, glutamic acid, and pectin were significantly different (P < 0.05) from the remaining tested compounds (Figs. 3–7). The carbohydrate, cellulose (as CMC) was the only compound that differed significantly (P < 0.05) from the rest of the tested compounds for zoospores of T. striatum KF9. For zoospores of Ulkenia sp. KF13, only pectin showed a significant difference (P < 0.05) from the rest of the compounds.
Zoospores of S. mangrovei KF6 and Ulkenia sp. KF13 were further examined for their chemotactic response to varying concentrations of selected compounds (Figs. 8–10). Glutamic acid elicited a concentration-dependent response with the highest chemotactic response at 100 mM for both species (Fig. 8). Schizochytrium mangrovei KF6 zoospores also exhibited positive concentration-dependent response to all the tested concentrations of pectin (0.01–2.5 mg/mL) and leaf extract (0.1–100 mg/mL) with the highest response at the highest tested concentration. Zoospores of Ulkenia sp. KF6 showed a negative response at the lowest concentration of pectin and leaf extracts tested (0.1 mM) but a dose-dependent response has again been observed in the remaining tested concentrations (Figs. 9, 10). In general, zoospores of S. mangrovei KF6 were more sensitive and responsive to the lower concentrations of the test compounds than those of Ulkenia sp. KF13, but the latter elicited higher chemotactic response with higher concentrations.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Cellulose, hemicellulose, pectic substances, and proteins are the four major components of plant cell walls (Mauseth 1988). Degradation studies by Raghukumar et al (1994, 1995) indicated that carbohydrates, cellulose, hemi-cellulose, phenolic compounds, and proteins are constantly lost from decaying leaves of R. apiculata during an eight week study. Soluble fractions such as sugar, phenolic compounds, and to some extent cellulose and hemi-cellulose, were observed to leach rapidly from decaying leaves in the initial stage of degradation. In nature cellulose in particulate leaf material is made readily accessible as the result of microbial attack and the activities of animal shredders, e.g., crabs. The extent to which they might be soluble is unknown, so in our study, CMC, as a soluble form of cellulose, was used. Soluble compounds leached from leaf material in the early stage of leaf decay may contribute to the survival of organisms occurring in this environment. The chemotactic response of zoosporic organisms to leaf leachate, as illustrated by the thraustochytrids in this study, is an example.
The results demonstrated that zoospores of thraustochytrids, similar to zoospores of chytrids and Oomycetes, were able to respond chemotactically to carbohydrates, amino acids, and leaf extracts in their immediate environment (Muehlstein et al 1988). Zoospores of three strains of S. mangrovei and Ulkenia sp. KF13, in general, showed a stronger chemotactic response towards leaf extracts of mangrove plants and Phragmites communis than to most individual amino acids or carbohydrates tested (Table III). Leaño et al (1998) also demonstrated a similar chemotactic response for two strains of Halophytophthora vesicula zoospores under laboratory conditions. Thus, the results from the present study, and that of Leaño et al (1998), suggest the probable synergistic effect of a whole array of compounds released during leaching and decomposition of leaf material, which may be responsible for attracting zoospores. Furthermore, the higher chemotactic response of zoospores towards green leaf extracts of K. candel than its senescent counterpart may be explained by nutrient status. Green leaves falling onto the mangrove floor may contain a higher amount of pectic substances and amino acids than those of senescent leaves, resulting in a higher chemotactic response of thraustochytrid zoospores towards green leaves.
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). Leaño et al (1998) suggested that release of amino acids from leaf material might help to attract zoospores in nature. Indeed, glutamic acid, one of the most efficient nitrogen sources for the growth of thraustochytrids (Singh and Ward 1997), may subsequently be used for the development and growth of attracted zoospores. Ethanol, a possible by-product released during leaf decomposition under semi- or anaerobic conditions, did not elicit a strong chemotactic response from thraustochytrids, whereas zoospores of H. vesicula were strongly attracted to it (Table III).
Zoospores of T. striatum KF9 showed weak chemotactic responses to most of the test compounds and leaf extracts. This sharp contrast of behavior to leaf extracts as compared with S. mangrovei strains may be explained by their higher sensitivity to phenolics, which are common in plant leaves (Harborne 1980), and have been known to be inhibitory to microbes (Cundell et al 1979, Gonzalez-Farias and Mee 1988). The phenolic compound luteolin 7-O-ß-D-glucopyranosyl-2''-sulfate extracted from healthy Thalassia testudinum Banks ex Konig (marine angiosperm) also had an inhibitory effect on the colonization and attachment of the thraustochytrid, Schziochytrium aggregatum (Jensen et al 1998). Phenolic compounds have also been suggested as an important factor in inhibiting thrasutochytrids from colonizing living algae (Miller and Jones 1983, Sathe-Pathak et al 1993, Sharma et al 1994). Thus, phenolic compounds present in leaf extracts may lead to avoidance of zoospores of T. straitum KF9. However, Raghukumar et al (1994, 1995) suggested that some thrausochytrids could tolerate high concentrations of phenolic compounds and this played a significant role during the early (0–21 d) and late (28–60 d) stages of the mineralization and decomposition of leaves of the mangrove, Rhizophora apiculata Blume. Therefore, zoospores of S. mangrovei KF6, 7, 12 and Ulkenia sp. KF13 may be able to tolerate phenolics and consequently be attracted to leaf extracts. The overall weak chemotactic response observed in zoospores of T. striatum KF9 may be explained by the phenomenon of selective accumulation of zoospores to a specific substratum. Specific accumulation was observed in zoospores of some chytrids and Oomycetes in the colonization of chitin or cellulosic materials (Mitchell and Deacon 1986). Selective accumulation of thraustochytrid zoospores is at the ventral sulcus area of Pinus pollen grains rather than the distal areas (Clokie 1974). Such preferential accumulation may involve diffusion of compounds from the ventral sulcus areas of the pollen grains and this accounts for the response observed.
A preliminary isolation study indicated that S. mangrovei was the most commonly found thraustochytrid on senescent leaves of K. candel, followed by Ulkenia spp. from various mangrove sites in Hong Kong. (Fan, unpubl). Thraustochytrium striatum KF9 was rarely found, suggesting that this species may be an uncommon colonizer of mangrove leaves. Bremer (1974) observed that the growth of T. striatum was retarded with the formation of abnormal zoosporangia at a semi-saline medium (7%) while good growth was noticed at full strength seawater (35%). This suggests that T. striatum may be an oceanic species adapted to a highly saline environment and its chemotactic response towards various compounds and leaf extracts may have been suppressed under less saline conditions as in most mangrove habitats.
Studies on zoospore chemotaxis of chytrids and oomycetes were observed to be concentration-dependent. Zoospores of Halophytophthora vesicula were observed to elicit a higher chemotactic response with higher concentrations of glucose, fructose, glutamic acid, asparagine, pectin, and ethanol (Leaño et al 1998). Maltose, starch, and Bryopsis extract (an alga commonly found in marine coastal waters) elicited strong and concentration-dependent chemotactic responses from zoospores of the chytrid R. littoreum (Muehlstein et al 1988). Our study shows that zoospores of S. mangrovei KF6 and Ulkenia sp. KF13 displayed concentration-dependent response to glutamic acid, pectin, and green leaf extract of Kandelia candel. The ability of S. mangrovei KF6 zoospores to respond to low concentration of leaf extracts (0.1 mg/mL) suggests that thraustochytrid zoospores can respond effectively to a low level of leaf leachate that diffuses from decaying leaves in tidal inundation areas. However, the impact of water flow cannot be neglected as this has been suggested as one of the dominant factors in influencing colonization of leaves by zoospores in the tidal zone (Newell and Fell 1992). Thus, the combined effect of water flow in bringing zoospores to the vicinity of a substratum and the ability of zoospores to respond to chemical attractants diffusing from the substratum might be an effective means for thraustochytrid colonization.
Thraustochytrids are common inhabitants of water columns and can reach from >100 cells/L in Antarctic and Subantarctic regions (Bahnweg and Sparrow 1974) to more than 11 000 cells/L in coral reef lagoon waters (Raghukumar 1987). They can probably survive as bacterial feeders in their amoeboid form (Raghukumar 1992). However, the ability of thraustochytrid zoospores to respond chemotactically towards leaf extracts allows them to survive in an alternative way as degraders of leaf litter in nature.
In Hong Kong the major mangrove tree species are Kandelia candel, Aegiceras corniculatum, Excoecaria agallocha (L) Latex, and Avicennia marina (Yipp et al 1995, Tam and Wong 2000). In Mai Po mangrove alone, Kandelia candel contributes an annual primary productivity and litter production of 24 ton/ha/yr and 11 ton/ha/yr (54% leaf litter) respectively (Lee 1989, 1990). Therefore there is an abundance of substrata available for colonization by thraustochytrid zoospores which can subsequently attach, colonize, and act synergistically with other microbes, such as Halophytophthora species (Leaño et al 1998), and later with the succession ascomycetes, in the degradation of mangrove leaves.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Accepted for publication January 28, 2002.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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