Photosynthetic properties of three Brazilian seaweeds

Propriedades fotossintéticas de três macroalgas marinhas brasileiras

SCIENTIFIC NOTE

Photosynthetic properties of three Brazilian seaweeds

Propriedades fotossintéticas de três macroalgas marinhas brasileiras

Ricardo M. Chaloub^I,1; Fernanda Reinert^II; Cristina A. G. Nassar^III; Beatriz G. Fleury^IV; Dulce G. Mantuano^V; Anthony W. D. Larkum^VI

^IUniversidade Federal do Rio de Janeiro, Departamento de Bioquímica. Av. Athos da Silveira Ramos, 149, Bloco A do Centro de Tecnologia, Ilha do Fundão, 21941-909 Rio de Janeiro, RJ, Brazil

^IIUniversidade Federal do Rio de Janeiro, Departamento de Biologia Vegetal. Av. Carlos Chagas Filho, 373, Bloco A do Centro de Ciências da Saúde, Ilha do Fundão, 21941-902 Rio de Janeiro, RJ, Brazil

^IIIUniversidade Federal do Rio de Janeiro, Departamento de Biologia Marinha. Av. Carlos Chagas Filho, 373, Bloco A do Centro de Ciências da Saúde, Ilha do Fundão, 21941-902 Rio de Janeiro, RJ, Brazil

^IVUniversidade do Estado do Rio de Janeiro, Departamento de Ecologia. Rua São Francisco Xavier, 524 – PHLC, Maracanã, 20559-900 Rio de Janeiro, RJ, Brazil

^VInstituto de Pesquisas Jardim Botânico do Rio de Janeiro, Departamento de Botânica Estrutural. Rua Jardim Botânico, 1008, Jardim Botânico, 22460-070 Rio de Janeiro, RJ, Brazil

^VIUniversity of Sydney, School of Biological Sciences (A08), New South Wales 2006, Sydney, Australia

ABSTRACT

Photosynthetic performance of distinct marine macroalgae, Ulva fasciata Delile (green alga), Lobophora variegata (J. V. Lamouroux) Womersley ex E. C. Oliveira (brown alga), and Plocamium brasiliensis (Greville) M. A. Howe & W. R. Taylor (red alga), were compared using a pulse amplitude-modulated fluorometer. The maximum quantum yield (F_v/F_m) ranged from 0.80 to 0.51, and the lowest value was found in P. brasiliensis. Under 400 µmol photons m^-2 s^-1 irradiance, the highest value of photochemical quenching (qP = 0.92 ± 0.13) was observed for U. fasciata. The red alga P. brasiliensis dissipated high amounts of excitation energy (qN = 0.56 ± 0.09), resulting in relatively low values for the effective quantum yield of PS-II (0.23 ± 0.04), as well as for the relative electron transport rate (3.3 ± 0.7). The high photosynthetic potential found for U. fasciata partially explains the species ability for rapid growth and high productivity.

Key words: Chlorophyll fluorescence, Lobophora variegata, Plocamium brasiliensis, Ulva fasciata

RESUMO

O desempenho fotossintético de três grupos distintos de macroalgas marinhas, Ulva fasciata Delile (alga verde), Lobophora variegata (J. V. Lamouroux) Womersley ex E. C. Oliveira (alga parda) e Plocamium brasiliensis (Greville) M. A. Howe & W. R. Taylor (alga vermelha), foi comparado com auxílio de um fluorímetro de pulso e amplitude modulada. O potencial fotoquímico máximo do PS II (F_v/F_m) variou de 0,80 a 0,51, sendo que os menores valores foram observados em P. brasiliensis. Sob a irradiância de 400 µmol fótons m^-2 s^-1, o maior valor de dissipação fotoquímica (qP = 0,92 ± 0,13) foi observado para U. fasciata. A alga vermelha P. brasiliensis dissipou elevada quantidade de energia de excitação (qN = 0,56 ± 0,09), resultando em valores baixos de potencial fotoquímico efetivo do PS II (0,23 ± 0,04), e também de taxa relativa de transporte de elétrons (3,3 ± 0,7). O elevado potencial fotossintético encontrado para U. fasciata explica, parcialmente, a capacidade da espécie de crescimento rápido e de alta produtividade.

Palavras-chave: fluorescência da clorofila, Lobophora variegata, Plocamium brasiliensis, Ulva fasciata

Introduction

Chlorophyll fluorescence analysis allows noninvasive and fast measurements of key aspects of photosynthetic light capture and electron transport. For biological systems at room temperature, the overall chlorophyll fluorescence yield is usually low and most of the fluorescence emission originates from PSII antenna pigments (Krause & Weis 1991). Although PSII fluorescence is a minor pathway for excitation dissipation, it competes with the quantitatively more important energy dissipation routes of PSII photochemistry, such as excitation transfer to PSI and heat dissipation. Therefore, changes in photochemistry or in the two nonphotochemical routes (energy and heat emission) cause changes in the fluorescence yield from PSII (Krause & Weis 1991; Bolhàr-Nordenkampf & Öquist 1993).

Pulse amplitude-modulated (PAM) fluorescence measuring systems, originally developed for higher plants, have been used to measure chlorophyll fluorescence from algae and cyanobacteria (Schreiber et al. 1986, Büchel & Wilhelm 1993, Schreiber et al. 1995, Mouget & Tremblin 2002, Molina-Montenegro et al. 2005), as well as from photosymbiont-containing invertebrates such as corals (Yellowlees et al. 2003) and sponges (Beer & Ilan 1998). In this study, a pulse amplitude-modulated fluorometer was used to assess photosynthetic properties of three tropical seaweeds (green, brown and red algae). Lobophora variegata (J.V. Lamouroux) Womersley ex E. C. Oliveira (Heterokontophyta) and Ulva fasciata Delile (Chlorophyta) are widely distributed along the Brazilian coast from shallow waters up to depths of 26 and 13 m, respectively (Horta 2000). In contrast, Plocamium brasiliensis (Greville) M. A. Howe & W. R. Taylor (Rhodophyta) is restricted to the southern and southeastern coast of Brazil, growing from the intertidal zone to depths of 22 m (Horta 2000). The thalli of the first two species are foliose and expanded while P. brasiliensis thallus is foliose and abundantly branched. Comparative studies on the photosynthetic responses of different groups of tropical seaweeds are scarce (Necchi Júnior 2004), and this study was initiated as a contribution to reduce this gap.

Material and methods

Algal material – Specimens of the green alga Ulva fasciata, the brown alga Lobophora variegata and the red alga Plocamium brasiliensis were collected from Praia do Forno (Búzios, Rio de Janeiro State, Brazil – 22º46' S, 42º53' W) in March 2006. U. fasciata occurred in the intertidal and upper sub-littoral zone of rocky shores, while L. variegata and P. brasiliensis were found in the upper sub-littoral zone of the beach. Samples were collected from the rocky shore at 1 m depth and immediately placed in a vessel with seawater at 22 ºC (ambient seawater temperature). The vessel was maintained in darkness for at least 20 minutes prior to fluorescence measurements. Three thalli of each species were used for measurements.

Chlorophyll-a fluorescence measurements – Chlorophyll fluorescence parameters were measured using a submersible diving-PAM system (Walz, Effeltrich, Germany), equipped with a blue LED (470 nm). The minimal fluorescence level in the dark-adapted state (F_o) was elicited by a weak probe of modulated light, whereas the maximum fluorescence level (F_m) was detected after a saturating pulse of actinic light (10,000 µmol photons m^-2 s^-1), which is sufficient to close all reaction centers and drive photochemical quenching to zero. Variable fluorescence of dark-adapted samples (F_v) was calculated from F_m-F_o, and the maximum quantum efficiency of PS-II photochemistry was obtained from the ratio F_v/F_m. Samples were also exposed to 400 µmol photons m^-2 s^-1 until steady-state fluorescence emission (F_s) was obtained, and maximum fluorescence signal (F_m') of light-adapted samples was determined after a saturating pulse of actinic light. The effective quantum efficiency of PS-II (Φ_PS-II = F_m'-F_s / F_m') was obtained from light-adapted samples. The proportion of open PSII reaction centers under actinic light was determined by the photochemical quenching coefficient, qP = (F_m'-F_s)/(F_m'-F_o), and the nonphotochemical quenching coefficient calculated from qN = (F_m-F_m')/(F_m-F_o). The relative electron transport rate (rETR) was computed by using the equation ETR = PAR 0.5 Φ_PS-II 0.84 (Genty et al. 1989).

Statistics – Mean values were compared using Kruskal Wallis non-parametric ANOVA at 5% significance level (P < 0,05), using the software GraphPadInStat 3.01 (GraphPad Software Inc.).

Results and discussion

The three seaweed species showed significantly different responses in fluorescence parameters, although they occurred at similar positions on the boulders, and were, therefore, exposed to similar irradiances. Maximum quantum efficiency (F_v/F_m of dark-adapted samples) was significantly lower in P. brasiliensis and higher in U. fasciata than in L. variegata (figure 1A), suggesting that the red alga was photoinhibited at the highest light levels around noontime. In addition, the highest values observed in U. fasciata (0.80-0.83), seem to indicate an increased PSII function in comparison with the other two species.

The values for qP were not significantly different among the three species (figure 1B). Given that qP reflects the proportion of the PSII reaction centers in the open state, high values of qP can result either from high rates of electron transfer around PSII (high rates of Q_A re-oxidation) or from the occurrence of high nonphotochemical quenching processes. As qN describes any nonphotochemical process that reduces the yield of variable fluorescence, the lowest values for this parameter in U. fasciata (figure 1B) confirm that this alga efficiently utilizes trapped light energy. This is in agreement with high values of both photochemical yield of electron transport around PSII (F_PS-II, figure 1C) and relative electron transport rate (rETR, figure 1D) observed for this species. In contrast, it is evident in figure 1B that a higher amount of excitation energy is dissipated by nonphotochemical processes in P. brasiliensis than in the other two species, resulting in low values of Φ_PS-II and rETR (figure 1C and 1D). These results suggest that P. brasiliensis is a shade adapted species in accordance with the results found for another red alga Palmaria palmata (Linnaeus) Kuntze from the French coastline (Mouget & Trembling 2002). Under light intensities ranging from 10 to 150 µmol m^-2 s^-1, P. palmata exhibited the lowest Φ_PS-II and qP values, as well as the highest level of energy dissipation through nonphotochemical quenching, in comparison to Ulva sp. and the brown alga Fucus serratus Linnaeus (Mouget & Trembling 2002). Previous studies with freshwater algae also showed that the rhodophytes were typically shade-adapted plants and some of them can tolerate high irradiances due to the presence of high nonphotochemical quenching (Necchi Júnior 2005). Since the fluorescence parameters found in L. variegata were close to those found in the green alga, an efficient photosynthetic apparatus is also assumed to occur in this Dictyotales. Similar results were previously observed in L. variegata sampled from deep-water near Bermuda (Peckol & Ramus 1992).

Our results support the view of rapid growth potential and high net primary productivity of the opportunistic macroalgae U. fasciata as previously reported (Littler & Littler 1980, Mouget & Tremblin 2002). The sampling site can be subjected to drastic changes in water temperature during the summer, due to the upwelling phenomenon that occurs in the proximity (Valentin et al. 1978). High solar irradiation allied to cold water can change photosynthetic rates and increase photoinhibition (Gomez et al. 2001). Such conditions represent a natural laboratory for studies in the tropics and a better understanding of the photosynthetic responses of the macroalgal community is of major importance in the present scenario of potential global weather changes.

Acknowledgement – We are indebted to Dr. Marcia Creed for organizing a workshop on chlorophyll fluorescence with the presence of Dr. Anthony W. D. Larkum funded by CNPq.

(received: June 03, 2009; accepted: March 11, 2010)

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Publication Dates

• Publication in this collection
  01 Sept 2010
• Date of issue
  June 2010

History

• Received
  03 June 2009
• Accepted
  11 Mar 2010