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Uptake Kinetics and Storage Capacity of Dissolved Inorganic Phosphorus

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Uptake Kinetics and Storage Capacity of Dissolved Inorganic Phosphorus J. Phycol. *, ***–*** (2019) © 2019 The Authors. Journal of Phycology published by Wiley Periodicals, Inc. on behalf of Phycological Society of America This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. DOI: 10.1111/jpy.12844 UPTAKE KINETICS AND STORAGE CAPACITY OF DISSOLVED INORGANIC PHOSPHORUS AND CORRESPONDING DISSOLVED INORGANIC NITRATE UPTAKE IN SACCHARINA LATISSIMA AND LAMINARIA DIGITATA (PHAEOPHYCEAE)1 Alexander Lubsch 2 NIOZ Royal Netherlands Institute for Sea Research, Department of Estuarine and Delta Systems, Utrecht University, PO Box 140, 4401 NT Yerseke, the Netherlands Department Ocean Ecosystems, University of Groningen, PO Box 72, 9700 AB Groningen, the Netherlands and Klaas R. Timmermans NIOZ Royal Netherlands Institute for Sea Research, Department of Estuarine and Delta Systems, Utrecht University, PO Box 140, 4401 NT Yerseke, the Netherlands Uptake rates of dissolved inorganic phosphorus and Abbreviations: DIN, Dissolved inorganic nitrate; dissolved inorganic nitrogen under unsaturated and DIP, Dissolved inorganic phosphate; DW, Dry saturated conditions were studied in young sporo weight; Fv/Fm,Fv refers to variable fluorescence; Fm phytes of the seaweeds Saccharina latissima and Lami refers to maximum fluorescence; FW, Fresh weight; naria digitata (Phaeophyceae) using a “pulse-and- IMTA, Integrated multitrophic aquaculture; ISC, chase” assay under fully controlled laboratory condi Internal storage capacity; NIOZ, Royal Netherlands tions. In a subsequent second “pulse-and-chase” assay, Institute for Sea Research; PAM (fluorometry), internal storage capacity (ISC) was calculated based on Pulse-amplitude-modulation (fluorometry); SA, Sur- VM and the parameter for photosynthetic efficiency face area; T, Nutrient concentration; Ve, Externally F /F .SporophytesofS. latissima showed a V of controlled uptake; VM, Maintenance uptake rate; VS, v m À À S 0.80 Æ 0.03 lmol Á cm 2 Á d 1 and a V of 0.30 Æ 0. Surge uptake rate; V, Uptake rate À À M 09 lmol Á cm 2 Á d 1 for dissolved inorganic phos phate (DIP), whereas V for DIN was 11.26 Æ 0.56 À À S lmol Á cm 2 Á d 1 and V was 3.94 Æ 0.67 Dissolved inorganic phosphorus (DIP) and dis- À À M lmol Á cm 2 Á d 1.InL. digitata, uptake kinetics for solved inorganic nitrogen (DIN) are essential DIP and DIN were substantially lower: V for DIP did macronutrients for maintaining the metabolism À SÀ not exceed 0.38 Æ 0.03 lmol Á cm 2 Á d 1 while V and growth of seaweeds. Phosphorus (P) and À À M for DIP was 0.22 Æ 0.01 lmol Á cm 2 Á d 1.V for Nitrogen (N) are key components of nucleic acids, À À S DIN was 3.92 Æ 0.08 lmol Á cm 2 Á d 1 and the V phospholipids, adenosine triphosphate (ATP) and À À M for DIN was 1.81 Æ 0.38 lmol Á cm 2 Á d 1. Accord are also involved in controlling enzyme reactions ingly, S. latissima exhibited a larger ISC for DIP and in the regulation of metabolic pathways. After À À (27 lmol Á cm 2) than L. digitata (10 lmol Á cm 2), N, P is the second most frequently limiting and was able to maintain high growth rates for a longer macronutrient in seaweed growth. Nutrient limita- period under limiting DIP conditions. Our stan- tion and shifts in limitation from one element to dardized data add to the physiological under another can significantly affect the internal compo- standing of S. latissima and L. digitata,thushelpingto sition, physiology, and growth of seaweeds (Peder- identify potential locations for their cultivation. This son and Borum 1996, Gevaert et al. 2001). These could further contribute to the development and processes can reflect natural fluctuations, but can modification of applications in a bio-based economy, also be driven by anthropogenic emissions. For example, agricultural run-off waters contain consid- for example, in evaluating the potential for biore- À erable amounts of inorganic phosphate (PO 3 ) mediation in integrated multitrophic aquacultures that 4 À produce biomass simultaneously for use in the food, and nitrogenous compounds, like nitrate (NO3 ) + feed, and energy industries. and ammonium (NH4 ; Sharpley et al. 1992, Rabal- ais et al. 2009). Anthropogenic discharge can also Key index words: Laminaria digitata; nitrate uptake; generate nutrient concentration gradients, which phosphate uptake; Saccharina latissima; uptake kinetics are often observed along coastal zones due to the proximity of nutrient sources. This can not only 1Received 5 June 2018. Accepted 4 January 2019. First Published Online 7 February 2019. lead to alterations in the type and magnitude of 2Author for correspondence: e-mail [email protected] nutrient limitations, but may also cause effects of Editorial Responsibility: A. Buschmann (Associate Editor) 1 2 ALEXANDER LUBSCH AND KLAAS R. TIMMERMANS eutrophication. In the North Sea, measures against Pederson et al. 2010), there is relatively little informa- eutrophication were first installed in the mid tion available about the DIP uptake kinetics, as well 1980s, when its dramatic effects on marine flora as DIP and DIN management in relation to the inter- and fauna became evident (Westernhagen and nal storage capacity (ISC), the maximal internal dura- Dethlefsen 1983, Malta and Verschuure 1997, Lyn- tion for growth under external limiting conditions gby et al. 1999). Recently it showed, that the de- (Pederson et al. 2010). This important information, eutrophication efforts have led to a large imbal- as it allows an estimation of ecological effects on ance in the N:P stoichiometry of coastal waters of nutrient availability and can contribute to develop- the North Sea in north-western Europe (Burson ment and modification of cultivation sites. A lot of et al. 2016). Increasing N:P ratios, which outpace studies related to uptake kinetics for DIN and DIP in the Redfield ratio of 16:1 were observed (Radach Saccharina latissima and Laminaria digitata have been and P€atsch 2007, Grizzetti et al. 2012) and a pro- conducted under field conditions with weekly to nounced P-limitation can be effective in coastal monthly sampling intervals (Bolton and Luning€ regions of the southern North Sea. 1982, Schaffelke and Luning€ 1994, Reid et al. 2013, This can have notable effects on the ecosystem Marinho et al. 2015) and the majority of studies communities and growth and functioning of pri- under laboratory conditions have focused on uptake À + mary producers. It has been reported that N avail- of nitrogenous compounds, as NO3 and NH4 ,in ability mediates the ability of primary producers to S. latissima and L. digitata (Chapman et al. 1978, access P, as shown for the brown seaweed Fucus Conolly and Drew 1985, Harrison et al. 1986). Often vesiculosus Linnaeus (Perini and Bracken 2014). DIN and DIP uptake is tested independently in short The perennial brown seaweeds (Phaeophyceae) Sac- term experiments, usually ranging from minutes to charina latissima and Laminaria digitata are commonly hours (e.g., Runcie et al. 2003, Martınez and Rico found on the lower shores of the north Atlantic 2004, Luo et al. 2012). Long-term responses to DIN around the northern North American and European and DIP availability remain unknown. coastlines, including the North Sea. Saccharina latissima Nutrient uptake by seaweed can be split into is also distributed along the shores of the north Pacific. three distinct phases, referred to as surge uptake As ecosystem engineers, S. latissima and L. digitata can (VS), metabolic or internally controlled uptake affect sedimentation and erosion by reducing water (VM), and externally controlled uptake (Ve; Conway currents (Jones et al. 1994, Bouma et al. 2005) and et al. 1976, Harrison et al. 1989). VS refers to the offer shelter, feedstock, and nursery habitats to various filling of internal nutrient pools, uncoupled from fauna, thus enhancing the diversity of their habitat growth (Conway et al. 1976), and has often been (Jørgensen and Christie 2003). Both seaweeds are rich described for nutrient-starved seaweeds (e.g., Fujita sources of nutrients and contain large amounts of car- 1985, Harrison et al. 1989, Dy and Yap 2001). The bohydrates in the form of structural, storage, and func- uptake rates gradually decrease as internal nutrient tional polysaccharides, as well as considerable amounts pools in cytoplasm and vacuoles are filled (Rosen- of proteins (Holdt and Kraan 2011). Aside from the berg et al. 1984, Fujita 1985). When internal nutri- direct use of S. latissima and L. digitata for culinary and ent concentrations are constant and relative uptake medicinal purposes, there is great interest in the rates of nutrients remain relatively stable over time, refinement, extraction, and application of carbohy- VM, which is considered equal to the rate of assimi- drates and proteins in the energy and animal feed lation, is attained (Taylor and Rees 1999, Barr et al. industries, as well as the extraction of important food 2004). The previously filled nutrient pools can be hydrocolloids, including carrageenan and alginates utilized at times of low external nutrient availability (McHugh 2003, Troell et al. 2006, Holdt and Kraan (Probyn and Chapman 1982, Pederson and Borum 2011). However, the content of these compounds var- 1996). The ISC and temporal duration of the filled ies, depending on nutrient availability, temperature, nutrient pools under external nutrient depletion light, and hydrodynamics, alternating in accordance to conditions has hardly been focused on in seaweeds season and area of cultivation (Murata and Nakazoe (Fujita 1985). 2001, Connan et al. 2004). Experimental studies under controlled conditions The vast range of possibilities for using seaweed, are critical to further understand the role of nutri- especially Saccharina latissima and Laminaria digitata, ents and shifts in nutrient ratios, and will strengthen has resulted in an enormous surge in interest over the understanding of nutrient demand and strate- the last decades (McLachlan 1985), hence stimulat- gies by seaweeds.
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