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Ecological Aspects of Carbon and Nitrogen Isotope Ratios of Cyanobacteria

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Ecological Aspects of Carbon and Nitrogen Isotope Ratios of Cyanobacteria Plankton Benthos Res 7(3): 135–145, 2012 Plankton & Benthos Research © The Plankton Society of Japan Ecological aspects of carbon and nitrogen isotope ratios of cyanobacteria 1, 2 2 3 3 EITARO WADA *, KAORI OHKI , SHINYA YOSHIKAWA , PATRICK L. PARKER , CHASE VAN BAALEN , 4 1 1 GENKI I. MATSUMOTO , MAKI NOGUCHI AITA & TOSHIRO SAINO 1 Environmental Biogeochemical Cycle Research Program, Research Institute for Global Change, Japan Agency for Marine- Earth Science and Technology (JAMSTEC), 3173–25 Showa-machi, Kanazawa-ku, Yokohama, Kanagawa 236–0001, Japan 2 Department of Marine Bioscience, Fukui Prefectural University, 1–1 Gakuenncho, Obama, Fukui 917–0003, Japan 3 Marine Science Institute, The University of Texas, 750 Channel View Drive Port Aransas, TX 78373, U.S.A. 4 Department of Environmental Studies, School of Social Information Studies, Otsuma Women’s University, 2–7–1 Karakida, Tama, Tokyo 206–8540, Japan Received 5 January 2012; Accepted 28 May 2012 Abstract: Variation in the δ13C of a cultured marine cyanobacterium (Agmenellum quadruplicatum, strain PR-6) is 13 described with an emphasis on the relationships between growth rate, pCO2, and δ C. An average nitrogen isotope fractionation of 1.0017 was obtained during N2 fixation by cultured marine cyanobacteria. This result suggests that 15 nitrogen supply via N2 fixation may be characterized by a low δ N, down to ca. －2‰ in marine environments, where the average δ15N is higher (at ca. 6‰) for major inorganic nitrogenous compounds such as nitrate. The natural abun- dances of nitrogen and carbon isotope ratios for cyanobacteria collected from the McMurdo Dry Valleys, Antarctica, were characterized by extremely low δ15N and widely ranging δ13C. Summarizing these and other data obtained, an isotopic map of cyanobacteria and other plankton in aquatic ecosystems was constructed and the ecological implica- tions are discussed. Our results suggest that the δ13C of marine phytoplankton is positively correlated with sea sur- face temperature and can be a useful parameter for estimating in situ growth rates in the open ocean. Key words: Antarctica, C and N isotope ratios, cyanobacteria, marine plankton, N2 fixation 1991), depending on temperature, pH (which affects the Introduction HCO3–CO2 isotope exchange equilibrium), and carbon Stable isotope studies can be useful for understanding availability. Based on latitudinal, hemispheric, and polar nutrient cycling, as well as the physiological nature of mi- discrepancies in plankton δ13C, Rau et al. (1982) and Goer- croorganisms in aquatic ecosystems. In photosynthetic or- icke & Fry (1994) emphasized that geographic differences ganisms, carbon isotope fractionation is generally recog- in kinetic isotope effects associated with plankton biosyn- nized to occur during photosynthetic carbon fixation. In thesis and metabolism were important factors causing lati- his comprehensive review, O’Leary (1981) demonstrated tudinal variation in plankton carbon isotope abundance. that the carbon isotope effect in the C3 pathway is large In a continuous culture of Chlamydomonas reinhardtii, during the carboxylation step. However, the diffusion of Takahashi et al. (1991) found a linear relationship between CO2 into leaves is partially rate-limiting and this serves to the growth rate constant and the carbon isotope fraction- reduce in vivo fractionation, suggesting a possible correla- ation factor under light- and nitrogen-limited conditions. tion between the carbon isotope effect and the growth The same trend was also reported for nitrate-uptake pro- physiology of marine phytoplankton. The CO2 content of cesses in the marine diatom Phaeodactylum tricornutum supplied gas has a major effect on the δ13C of microalgae (Wada & Hattori 1978). Because information on the (Mizutani & Wada 1982). δ13C in marine plankton is growth physiology of phytoplankton and epibenthic algae thought to range from －9 to －30‰ (Wada & Hattori can likely be obtained by measuring their C and N stable isotope ratios, Wada & Hattori (1991) created a δ15N–δ13C * Corresponding author: Eitaro Wada; E-mail, [email protected] map of marine phytoplankton. 136 E. WADA et al. In the open ocean, the nitrogen isotope ratios of plank- Materials and Methods ton are closely correlated with the chemical forms of inor- ganic nitrogen used for primary production. The level of Cultures δ15N in Trichodesmium sp. is low compared to those of plankton commonly found in other areas, supporting the Agmenellum quadruplicatum, strain PR-6 (Synechococus idea that nitrogen is supplied to this community via molec- sp. ATCC27264/PCC7002), was kept in the laboratory of ular nitrogen fixation (Minagawa & Wada 1986, Saino & one of the authors (Van Baalen) in an axenic form. The or- Hattori 1987, Carpenter et al. 1997). The aerobic nitrogen ganism was grown in modified ASP-2 medium (Van fixation ability of Trichodesmium has been confirmed Baalen, 1962) in test tubes (100 ml) or Erlenmeyer flasks 13 using isolated strains (Ohki et al. 1986, 1988, Chen et al. (1 L) with continuous bubbling of 1% CO2 (δ C PDB= 1996, Ohki 2008, Finzi-Hart et al. 2009). However, nitro- －36.64‰) and illuminated with fluorescent lamps 10 cm gen fixation sometimes occurs at low rates relative to the from the growth apparatus (50–60 μmol photons m－2 sec－1). total nitrogen budget (Ohki et al. 1991, Capone et al. 1997). To control the growth rate, light intensity was altered using Unicellular diazotrophic cyanobacteria contribute signifi- black mesh cloth to cover the test tubes. Growth of the liq- cantly to nitrogen cycling in the ocean (Zehr et al. 2001), uid cultures was followed turbidimetrically and the spe- although δ15N data for these unicellular species are not yet cific growth rate constant (μ) was estimated using the available. method of Kratz and Myers (1955), where μ=0.301 corre- Cyanobacteria are distributed across a wide range of sponds to a generation time of 1.00 d. physicochemical conditions, such as pH, redox potential, Cells for isotopic studies were harvested at the late loga- and temperature, and play important roles as primary pro- rithmic phase or early stationary phase for test tube cul- ducers in a variety of natural ecosystems. In the McMurdo tures. In large-scale cultures, cells were harvested at inter- Dry Valleys, Victoria Land, Antarctica, there are a variety vals and collected on Whatman type-C glass fiber filters of saline lakes and ponds that host undescribed types of preheated to 400°C for 5 h. Filters with residues were cyanobacteria with the lowest known δ15N values in the treated with 0.1 N HCl and stored in a refrigerator until biosphere. In the saline lakes and ponds the cyanobacteria mass spectrometric analysis. use nitrate supplied via precipitation. Because of the very Diazotrophs low humidity in the McMurdo Dry Valleys, the precipi- tated nitrate is present as a powdered crystal of NaNO3, Trichodesmium spp. NIBB1067 was isolated and cul- which is the nitrogen source used for growth by the cyano- tured in a synthetic medium as described in Ohki & Fujita bacteria in the saline lakes and ponds in this area. The (1982) and Ohki et al. (1986). Five unicellular and one fila- 15 δ N of sodium nitrate (NaNO3), which can be as low as mentous marine cyanobacteria isolated from the sea －20‰, and nitrogen isotope fractionation during nitrate around Singapore (Ohki et al. 2008) and Crocosphaera uptake are possible causes of these low δ15N values (Wada watsonii WH8501 (Waterbury and Pippka 1989) provided et al. 1981, Matsumoto et al. 1987, Matsumoto et al. 1993). by Drs. Waterbury and Dyhman of Woods Hole Oceano- Hage et al. (2007) isotopically characterized coastal pond- graphic Institution, USA, were maintained in a liquid mod- derived organic matter in the McMurdo Dry Valleys. Re- ified Aquil medium without combined nitrogen (Ohki et al. cently, Hopkins et al. (2009) reported isotopic evidence for 1986). Two freshwater heterocystous cyanobacteria in sec- the provenance and turnover of organic carbon by soil mi- tions IV and V (Nostoc sp. PCC7120 and Fischerella croorganisms in the McMurdo Dry Valleys. sp1ATCC29114, respectively) were cultured in BG0 (Rip- In this study, we investigated the effects of cyanobacte- pka & Herdman 1992), and used as references. Cultures rial growth rate on carbon isotope fractionation in a ma- were kept under fluorescent lights (daylight type) at rine cyanobacterium (Agmenellum quadruplicatum; PR-6). 10 μmol photons m－2 sec－1 (12 : 12 L : D) at 26°C (Ohki et Marine diazotrophs were also investigated to elucidate the al. 2008). Several milligrams of cells were collected, cen- role of nitrogen isotope fractionation in molecular nitrogen trifuged at 3,000×g for 4 min at 4°C, and lyophilized for fixation by various kinds of marine cyanobacteria. Cyano- stable isotope measurements. bacteria collected from saline lakes and ponds in the Mc- Cyanobacteria from the McMurdo Dry Valleys, Ant- Murdo Dry Valleys, Antarctica, were also studied in detail, arctica with an emphasis on cyanobacterial growth physiology. Finally, we summarized the characteristics of cyanobacte- Observations of the McMurdo Dry Valleys area during ria on a δ15N vs. δ13C map and discuss some ecological im- the 1980–1981 field season were reported in detail by plications of algal isotope ratios based on our data in com- Wada et al. (1984). Lake Vanda, several ponds in the Laby- bination with previously reported data (Minagawa & Wada rinth, Lake Bonney, and other lakes were visited during 1986, Wada & Hattori 1991, Yoshioka et al. 1994, Aita et the season. Epibenthic cyanobacteria were collected from al. 2011). unnamed saline ponds in the Labyrinth, near the terminus of the Wright Upper Glacier, and from Lake Vanda and its surroundings. Samples were also collected from the Taylor C and N isotope ratios of cyanobacteria 137 Fig. 1. Locations of sampling sites in the McMurdo Dry Valleys of southern Victoria Land, Antarctica (revised from Matsu- moto et al. 1990). Dotted areas are ice-free. South side of Lake Vanda (77°31′0″S, 161°40′0″E): V1, V2, V3, V4, V5, V6, V7, V8, V9, V10, and V11.
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