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Photosynthetic Pigment Composition of Marine Angiosperms: Preliminary Characterization of Mediterranean Seagrasses

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Photosynthetic Pigment Composition of Marine Angiosperms: Preliminary Characterization of Mediterranean Seagrasses BULLETIN OF MARINE SCIENCE, 71(3): 1171–1181, 2002 PHOTOSYNTHETIC PIGMENT COMPOSITION OF MARINE ANGIOSPERMS: PRELIMINARY CHARACTERIZATION OF MEDITERRANEAN SEAGRASSES Gianna Casazza and Lucia Mazzella ABSTRACT Pigments were investigated in the Mediterranean marine angiosperms Posidonia oceanica, Cymodocea nodosa, Zostera noltii and Halophila stipulacea. Samples were collected and analyzed from shallow and deep water habitats. Acetone extracts of leaves were analyzed by absorption spectroscopy, high performance liquid chromatography (HPLC) and thin layer chromatography (TLC). The marine angiosperms examined pos- sessed: β,β-carotene, lutein, zeaxanthin, violaxanthin, neoxanthin and other minor pig- ments. Two unidentified pigments with the same retention time as two “siphonaxanthin- type” pigments were isolated from the green alga Flabella petiolata and are relatively abundant in the species P. oceanica and H. stipulacea. Pigment data indicate a possible biochemical adaptation to different light regimes in seagrass species that can colonize deeper habitats. Seagrasses represent an outstanding example of adaptation of angiosperms to the ma- rine environment (Waycott and Les, 1996). They possess many specialized characteris- tics, such as hydrophilous pollination, morphological adaptations to submergence, nutri- ent assimilation by leaves and physiological adaptation to root anoxia (Den Hartog, 1970; Smith et al., 1988; Cox et al., 1992; Kraemer et al., 1997). Among the characteristics of shallow water marine environments where seagrasses grow, the variable and extremely reduced light regimes play a fundamental role. Seagrasses respond to these light reduced environments in a variety of morphological and physiological ways that have recently received considerable attention (Abal et al., 1994; Enriquez et al., 1995). Previous work has focused on growth and biomass measurements, morphological alterations, carbon balance and analysis of various photosynthetic parameters (Dennison and Alberte, 1986; Mazzella and Alberte, 1987; West, 1990; Zimmerman et al., 1994, 1995; Buia et al., 1992). The photosynthetic capabilities of plants are closely related to the structure of their photosynthetic apparatus. Chlorophyll a is common to all oxygen-producing photosyn- thetic organisms. Among all the photosynthetic organisms known, the greatest diversity of pigments is found in plants inhabiting the aquatic environments and particularly among the different groups of marine algae (Rowan, 1989). The role of the pigments in the depth distribution of algae, popularly known as ‘chromatic adaptation’ has been a controversial and greatly discussed topic for long time (Ramus et al., 1976; Ramus, 1983; Dring, 1981). Photosynthesis is strongly influenced by light quantity and quality. Although different photosynthetic performance of organisms can be ascribed to characteristics other than pigments, the light quality definitely plays a role in growth and development in deep water (Dring, 1981; Senger and Bauer, 1987). Seagrasses generally occur in shallow waters (Larkum and den Hartog, 1989) although reports indicate a wide range of depth limits for different species (Duarte, 1991). P. oceanica typically extends to 40 m depth in the Mediterranean Sea (Colantoni et al., 1982) while 1171 1172 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 3, 2002 Halophila engelmannii has been reported to 90 m depth in the Coral Sea (Duarte, 1991). Studies of marine angiosperms have shown that different seagrass species respond to changes in light availability over different time scales, reflecting variations in plant growth strategy and architecture (Abal et al., 1994; Duarte, 1991; Buia et al., 1992). Pigment adaptation plays a fundamental role in the success of submerged angiosperms in shaded aquatic environments (Dennison and Alberte, 1982; Frost-Christensen and Sand- Jensen, 1992) but data on the phosynthetic pigment composition of marine angiosperms are sparse and incomplete. Preliminary work (Ikemori and Arasaki, 1977) on Zostera marina and H. ovalis indicated that the pigment composition of seagrasses was identical to those of terrestrial vascular plants. Later studies of photosynthetic pigments focused on chlorophyll a/b contents and ratios (Drew, 1978; Wiginton and McMillan, 1979). More recently unidentified and putative UV blocking pigments have been reported (Trocine et al., 1981, 1982; Abal et al., 1994; Dawson and Dennison, 1996). To our knowledge, no other information on the photosynthetic pigments of marine angiosperms is available. The present work examines the pigment composition of four Mediterranean seagrasses: P. oceanica, Cymodocea nodosa, Z. noltii and H stipulacea, which represent different depth distributions. The aim was a comparison of the pigment composition of four seagrass species with: (1) a terrestrial plant, (2) two macroalgae inhabiting the same marine envi- ronment and (3) eventually a comparison of deep and shallow seagrass beds to ascertain whether pigment composition plays a role in the ability of some species to grow at lower light regimes hence colonizing greater depths. MATERIALS AND METHODS SAMPLE COLLECTION.—Leaf samples of P. oceanica, C. nodosa, Z. noltii were collected using SCUBA, from different locations around the Island of Ischia (Gulf of Naples). H. stipulacea was collected in the Levante Bay of Vulcano Island (Eolian Islands, Sicily). For comparison, material of the Chlorophyceae Flabella petiolata and Chaetomorpha aerea and of the terrestrial plant Spinacia olearacea, as one of the most used species in photosynthetic pigment studies, was obtained. All samples were collected in shallow waters, at depths ranging between 3 and 5 m. Z. noltii and the macroalga C. aerea are limited to these depths; C. nodosa, H. stipulacea P. oceanica and the macroalga F. petiolata were also collected at the maximum depth observed, for these species, in the investigated areas. C. nodosa was found at a maximum depth of 13 m, H. stipulacea at 27 m and P. oceanica at a depth of 37 m. The epiphytes were manually removed from the leaves and thalli with a razor blade; tissues were either weighed and processed immediately for pigment extraction, or frozen at −20°C for further analyses. Three samples from each species and depth were pooled together. Tissues were repeatedly cold extracted with 100% acetone using an Ultra Turrax homogenizer. Acetone extracts were transferred to diethyl ether 1:1, with the addition of 10% cold NaCl, according to Jeffrey (1968). Samples were concentrated by drying under a stream of nitrogen gas in reduced light to minimize photoxidation. PIGMENT CHARACTERIZATION.—The pigment composition of all samples was analysed by High Performance Liquid Cromatography (HPLC), Thin Layer Chromatography (TLC) and absorption spectroscopy. A Beckman ultrasphere RP18 column (ODS 5µm , 250 × 4.6 mm, IP) HPLC system was used with a two solvent mixture for separation: A) methanol:water:P solution (80:10:10) and B) methanol:ethyl acetate (80:20), as specified in Brunet et al. (1993). Pigments were detected both spectrophotometrically (440 nm, with Beckman Gold system, model 166) and fluorometrically (excitation 345 to 510 nm, emission 610 to 650 nm, with a Gilson, Model 121). Sigma chl a, chl b, β,β-carotene and “V.K.I. - Water Quality Institute - International Agency for 14C Determination”, CASAZZA AND MAZZELLA: PHOTOSYNTHETIC PIGMENT COMPOSITION 1173 Denmark, were used as standard pigments. Carotenoid quantification was obtained as relative amounts of total carotenoids, based on integrated peak areas of the chromatographs, from three separated pigment determination. Thin layer chromatography was used to separate pigments. The chromatographic systems used were: I) precoated silica gel plates (Sigma), with two developing solvent systems, a) n-propanol (4−10%) in petroleum ether (40°−60°) and b) 30% acetone in petroleum ether (Sherma and Lippstone, 1969); II) high performance, reverse phase, TLC plate (HPTLC Merck, RP-8), with developing system 90% methanol (Vesk and Jeffrey, 1987). For the identification of the isolated pigments, the pigmented zones were scraped from the plate with a razor blade and eluted into ethanol (100%, v/v) for carotenoids and acetone (100%, v/v) for chlorophylls. The absorption spectra of the pigments were analysed; some carotenoid spectra were examined after reactions with NaBH4, for the presence of specific chemical structure, i.e. conju- gated ketogroups (Walton et al., 1970). Absorption spectra of the acetone extracts of the macrophytes and the carotenoid ethanol ex- tracts of the separated pigments were obtained using a UV-VIS Varian CARY 1E spectrophotom- eter. RESULTS SPECTROPHOTOMETRIC ANALYSES.—Absorption spectra of acetone extracts of the four seagrasses, collected in the same depth range (3−5 m), are shown in Figure 1. All spectra were normalized to the chl a absorption maximum at long wavelength. Differences are evident in the blue portion of the spectrum (400−600 nm), where the Soret band of chl b and the carotenoids absorb (Jeffrey et al. 1997). In particular the P. oceanica and H. stipulacea extracts reveal an enhanced absorption in the Soret band for chl b (ca 450 nm) and a red shift in the Soret peak from 451 nm to 456 nm in H. stipulacea. This shift is most likely due to a change in the carotenoids composition. Figure 1. Absorption spectra of acetone (100%) extracts of four seagrass species: Posidonia oceanica, Cymodocea nodosa, Zostera noltii and Halophila stipulacea from shallow waters (3−5 m). Spectra
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