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Ascophyllum Nodosum and Its Symbionts: XI. the Epiphyte Vertebrata Lanosa Performs Better Photosynthetically When Attached to Ascophyllum Than When Alone

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Ascophyllum Nodosum and Its Symbionts: XI. the Epiphyte Vertebrata Lanosa Performs Better Photosynthetically When Attached to Ascophyllum Than When Alone Research Article Algae 2014, 29(4): 321-331 http://dx.doi.org/10.4490/algae.2014.29.4.321 Open Access Ascophyllum nodosum and its symbionts: XI. The epiphyte Vertebrata lanosa performs better photosynthetically when attached to Ascophyllum than when alone David J. Garbary1,*, Anthony G. Miller1 and Ricardo A. Scrosati1 1Department of Biology, St. Francis Xavier University, Antigonish, NS B2G 2W5, Canada Vertebrata lanosa is an abundant and obligate red algal epiphyte of Ascophyllum nodosum that forms part of a complex and highly integrated symbiotic system that includes the ascomycete, Mycophycias ascophylli. As part of ongoing studies to resolve interactions among species in the symbiosis, we used pulse amplitude modulation fluorimetry of chlorophyll a fluorescence, from photosystem II (PSII), to measure the maximum quantum yield (Fv / Fm) of PSII [QY(II)max] and rela- tive photosynthetic electron transport rates (rETR), as a function of light intensity, in order to evaluate the photosynthetic capacity of the two algal symbionts in the field and in the laboratory under different treatments. Our primary question was ‘Is the ecological integration of these species reflected in a corresponding physiological integration involving pho- tosynthetic process?’ In the laboratory we measured changes in QY(II)max in thalli of V. lanosa and A. nodosum over one week periods when maintained together in either attached or detached treatments or when maintained separated from each other. While the QY(II)max of PSII of A. nodosum remained high and showed no significant variation among treat- ments, V. lanosa showed decreasing performance in the following conditions: V. lanosa attached to A. nodosum, V. lanosa in the same culture, but not attached to A. nodosum, and V. lanosa alone. These results are consistent with observations in which rETR was reduced in V. lanosa maintained alone versus attached to A. nodosum. Values for QY(II)max in V. lanosa measured in the field in fully submerged thalli were similar to those measured in the laboratory when V. lanosa was at- tached to it obligate host A. nodosum. Our results provide evidence of a physiological association of the epiphyte and its host that reflects the known ecology. Key Words: Ascophyllum nodosum; epiphytism; photosynthesis; quantum yield; symbiosis; Vertebrata lanosa INTRODUCTION Ascophyllum nodosum (L.) Le Jolis is the host of a four core members of a symbiosis that also involves the complex symbiotic system that includes an obligate en- obligate, but not host-specific, epiphyte, Elachista fuci- dophytic ascomycete, Mycophycias ascophylli (Cotton) cola (Velley) Areschoug (also on Fucus spp.), and the chi- Kohlmeyer & Volkmann-Kohlmeyer, and the obligate, ronomid insect, Halocladius variabilis (Staiger), which is epiphytic red alga, Vertebrata lanosa (L.) Christensen typically associated with E. fucicola (Garbary et al. 2009a, (Garbary and Deckert 2001). V. lanosa is, in turn, asso- Tarakhovskaya and Garbary 2009, Brown et al. 2013). ciated with the host-specific, red algal parasite Choreo- Considerable progress has been made in understanding colax polysiphoniae Reinsch (Irvine 1983). These are the the geographic and ecological distributions of these sym- This is an Open Access article distributed under the Received July 15, 2014, Accepted November 16, 2014 terms of the Creative Commons Attribution Non-Com- Corresponding Author mercial License (http://creativecommons.org/licenses/by-nc/3.0/) which * permits unrestricted non-commercial use, distribution, and reproduction E-mail: [email protected] in any medium, provided the original work is properly cited. Tel: +1-902-867-2164, Fax: +1-902-867-2389 Copyright © 2014 The Korean Society of Phycology 321 http://e-algae.kr pISSN: 1226-2617 eISSN: 2093-0860 Algae 2014, 29(4): 321-331 bioses across the North Atlantic Ocean, as well as the ana- of Fundy of Nova Scotia, Canada (44°36.85′ N, 65°55.56′ tomical and ultrastructural interactions of these associa- W) (Fig. 1A), and experiments were conducted during tions (e.g., Lining and Garbary 1992, Deckert and Garbary November-December 2012. Gullivers Cove is an unde- 2005a, 2005b, Garbary et al. 2005b, Longtin and Scrosati veloped area that was previously studied for algal diver- 2009, Longtin et al. 2009, Toxopeus et al. 2011, Garbary sity (Edelstein et al. 1970), and is currently used for com- and Tarakhovskaya 2013). mercial harvest of Palmaria palmata (L.) Weber & Mohr From a physiological perspective, the interactions of (Garbary et al. 2012a). Ascophyllum grew on the basalt A. nodosum and V. lanosa (hereafter referred to as Asco- bedrock characteristic of Nova Scotian shores facing the phyllum and Vertebrata, respectively) have been the lower Bay of Fundy (Garbary et al. 2012a), and where most intensively studied. Given the host specificity, it fronds typically reach 1 m long (Fig. 1B). The site has a was initially assumed that host specificity was based on continuous bed of Ascophyllum through the mid inter- a biochemical dependency, and there was considerable tidal zone from ca. 1.5 to 5 m elevation, and Vertebrata interest in the possible transfer of materials between (Fig. 1C-E) was abundant at all but the extreme upper and Vertebrata and Ascophyllum. A variety of studies showed lower portions of the Ascophyllum distribution. photosynthate and inorganic nutrient transfer between the symbionts (Citharel 1972, Harlin 1973, Penot 1974, Photosynthetic fluorescence parameters Harlin and Craigie 1975, Turner and Evans 1977, Penot et al. 1993, Ciciotte and Thomas 1997). None of these stud- We examined photosynthetic performance of Asco- ies, however, provided a strong physiological explanation phyllum and Vertebrata by measuring the maximum for the association, in that movement of materials was in quantum yield of photosystem II (PSII) [QY(II)max], a both directions, and rarely in excess of what was consid- measure of the photochemical efficiency of PSII, and the ered simple diffusion. Indeed, Pearson and Evans (1990, relative rates of photosynthetic electron transport (rETR) 1991), Garbary et al. (1991), and Longtin and Scrosati at various light intensities. Both photosynthetic param- (2009) suggested that the association had a strong eco- eters were measured as changes in the PSII chlorophyll logical basis in recruitment limitation provided by host a fluorescence emission using a portable, PAM fluorom- surface features. These included the number of settle- eter (Diving-PAM; Heinz Walz, Effeltrich, Germany). The ment sites on Ascophyllum associated with scars from QY(II)max was estimated as: receptacle abscission and herbivore surface wounds, as QY(II) = (F - F ) / F = F / F well as epidermal shedding (Garbary et al. 2009b). max m o m v m In this study, we used pulse amplitude modulation , where Fo is the minimal value of chlorophyll a fluo- (PAM) of chlorophyll a fluorescence to measure pho- rescence from PSII in dark-adapted thallus (10-15 min) tosynthetic parameters of Vertebrata and Ascophyllum when both photochemical quenching (qP) is at a maxi- when isolated from each other, or when in combina- mum (i.e., at 100%) and non-photochemical quenching tion, where the two species were either attached or not (NPQ) is at a minimum (i.e., at 0). Fm is the maximum attached to each other. We evaluated a series of hypoth- value for chlorophyll a fluorescence from PSII measured eses: 1) that Vertebrata is parasitic on Ascophyllum and from dark-adapted thalli during a non-modulated flash will have a negative impact on the photosynthetic per- of light that fully reduces PSII and is called a saturating formance of the host; 2) that the survival of Vertebrata is flash (SF).F v, the difference between Fm - Fo, is called based on exudates from Ascophyllum; and 3) that main- the variable fluorescence (Papageorgiou and Govindjee tenance of photosynthesis in Vertebrata requires it to be 2004). To obtain thalli in the dark-adapted state samples in direct contact (i.e., rhizoid penetration) with Ascophyl- were placed in the ‘dark leaf clips’ (DIVING-LC; Heinz lum so that transfer of materials can be facilitated from Walz) and dark-adapted for 10-15 min prior to taking the host to epiphyte. readings. Gain settings on the Diving-PAM were set at 1 and 4 for Ascophyllum and Vertebrata, respectively. Chlo- rophyll a fluorescence nomenclature follows Kromkamp MATERIALS AND METHODS and Forster (2003). The intensity of the monitoring beam of the PAM fluo- Study site and source of algal material rometer was 0.04 µmol photons m-2 s-1 and the intensity of the SF was 10,000 µmol photons m-2 s-1. All algal material came from Gullivers Cove in the Bay The QY(II)max measurements give information only http://dx.doi.org/10.4490/algae.2014.29.4.321 322 Garbary et al. Symbiosis of Ascophyllum and Vertebrata A B C D E F a c a d c b b d Fig. 1. (A) Field site at Gullivers Cove, Nova Scotia with mid-intertidal zone dominated by Ascophyllum nodosum. (B) Abundant thalli of Vertebrata lanosa on A. nodosum in situ. (C) Clumps of fully moistened V. lanosa exposed on surface of A. nodosum. (D) Partially dried thalli of V. lanosa after several hours of desiccation on exposed surface of A. nodosum. (E) ‘Leaf clips’ (arrows) attached to V. lanosa during dark adaptation prior to fluorescence measurement. (F) Apparatus for laboratory experiment with replicated containers of A. nodosum alone (a); V. lanosa alone (b); both species with V. lanosa detached (c); both species with V. lanosa attached (d). Scale bars represent: B & E, 50 cm; C & D, 5 cm. about the photochemical efficiency of PSII. In order to periods (10 s each) of increasing light intensity (24 to investigate the effect of treatments on the photosynthetic 1,341 µmol photons m-2 s-1). The rETR was determined electron transport capacity downstream from PSII we using the following equation: measured rETR at various light intensities using the rapid rETR = QY(II) × PAR × 0.5 light curve (RLC) option of the Diving-PAM fluorometer.
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