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Phospholipid-Derived Fatty Acids As Chemotaxonomic Markers for Phytoplankton: Application for Inferring Phytoplankton Composition

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Phospholipid-Derived Fatty Acids As Chemotaxonomic Markers for Phytoplankton: Application for Inferring Phytoplankton Composition MARINE ECOLOGY PROGRESS SERIES Vol. 324: 113–125, 2006 Published October 23 Mar Ecol Prog Ser Phospholipid-derived fatty acids as chemotaxonomic markers for phytoplankton: application for inferring phytoplankton composition Nicole A. Dijkman*, Jacco C. Kromkamp Centre for Estuarine and Marine Ecology, Netherlands Institute of Ecology (NIOO-KNAW), PO Box 140, 4400 AC Yerseke, The Netherlands ABSTRACT: Phospholipid-derived fatty acids (PLFA) are widely used as chemotaxonomic markers in microbial ecology. In this paper we explore the use of PLFA as chemotaxonomic markers for phyto- plankton species. The PLFA composition was determined for 23 species relevant to estuarine phyto- plankton. The taxonomic groups investigated were Chlorophyceae, Trebouxiophyceae, Prasi- nophyceae, Bacillariophyceae, Dinophyceae, Cryptophyceae, Rhodophyceae, Pavlovophyceae and Prymnesiophyceae. Most of these taxonomic groups have a characteristic PLFA composition, although a few contain truly unique PLFA biomarkers. The PLFA composition was used to derive spe- cies composition and abundance of the phytoplankton in the Scheldt estuary (border region between Belgium and the Netherlands) in April, July and October 2003, using the matrix factorization pro- gram CHEMTAX. The results agree well with results from HPLC-derived pigment analysis of the same samples. The advantages of using PLFA instead of pigments, or rather in addition to pigments, are that (1) information on bacteria can be derived in addition to information on photosynthetic taxa, (2) in some cases more or different taxa can be distinguished and (3) the isotopic composition of PLFA can be measured relatively easily, allowing the measurement of group-specific primary production. KEY WORDS: Phytoplankton composition · Phospholipid-derived fatty acids · PLFA · Scheldt estuary · Biomarkers · CHEMTAX Resale or republication not permitted without written consent of the publisher INTRODUCTION standing of species richness and distribution, but the ‘paradox of the plankton’ as posed by Hutchinson Phytoplankton play an important role in aquatic (1961) has still not been fully explained. Probably one ecosystems, supplying food and oxygen to other mem- of the main reasons why species richness and dynam- bers of the ecosystem. Diverse taxonomic groups, vary- ics are not yet well understood is the fact that most ing in shape, pigmentation, ecological characteristics measurements are made on bulk samples and that and evolutionary origin, contribute to the phytoplank- physiological measurements at the level of a single ton community. The composition and abundance of species or functional groups have been hampered by phytoplankton depend on environmental parameters lack of proper methodology. such as irradiance, temperature, salinity and nutrient Microscopy has been an important tool in the study availability (e.g. Underwood & Kromkamp 1999, Bady- of species richness and abundance ever since the lak & Phlips 2004). Patterns of phytoplankton distribu- invention of the microscope. Microscopic analysis tion are the subject of ongoing research (e.g. Badylak allows a precise and elaborate determination of the & Phlips 2004). Progress has been made in the under- species present in a water sample. However, accurate *Email: [email protected] © Inter-Research 2006 · www.int-res.com 114 Mar Ecol Prog Ser 324: 113–125, 2006 microscopic enumerations require a trained micro- phytoplankton species relevant to estuarine phyto- scopist and are time-consuming. Furthermore, in most plankton and used these data to derive group composi- cases, the algae have to be stored and therefore fixed tion and abundance in the Scheldt estuary (border before analysis and not all taxa withstand fixation well region between Belgium and the Netherlands) from (Gieskes & Kraay 1983). Often, cell numbers are diffi- the PLFA composition of particulate suspended matter. cult to compare due to large differences in cell size and The results from this PLFA analysis are compared to volume and cell numbers have to be converted to similar data derived from the pigment composition of biovolume (e.g. Hillebrand et al. 1999) or carbon the same samples. In a later paper we will determine (Menden-Deuer & Lessard 2000), a tedious procedure. the photosynthetic activity of several taxonomic groups The use of chemotaxonomic markers provides an by measuring the rate of 13C-labeling of individual alternative method for determining phytoplankton PLFA (Dijkman et al. unpubl.). composition. Photosynthetic pigments are the best known chemotaxonomic markers for phytoplankton. As HPLC technology advances, more and more pig- MATERIALS AND METHODS ments can be routinely measured, allowing an increas- ing number of taxa to be distinguished (e.g. Zapata et Organisms and culture conditions. PLFA composi- al. 2004, Jeffrey & Wright 2006). In recent years, tion was determined for a number of species from tax- several studies have compared cell numbers and pig- onomic groups relevant to estuarine phytoplankton. ments, and in general a good agreement is found Most of these species are regularly observed in the between these 2 methods both in freshwater and Scheldt estuary (e.g. Koeman et al. 2004) and some marine ecosystems (e.g. Garibotti et al. 2003, Marinho were isolated from the Scheldt estuary. Other species & Rodrigues 2003). Even groups lacking specific were obtained from culture collections. Isolated spe- pigments can be detected with the help of pigment cies were identified to at least the genus level by ratios using matrix factorization programs such as sequence analysis of the 18S rRNA. Table 1 lists the CHEMTAX (Mackey et al. 1996, Schlüter & Møh- species, strain number and source (where available), lenberg 2003). and the media in which the species were cultured. Of Bacteria are also an important constituent of aquatic 23 species examined, 9 were axenic (Table 1). In the ecosystems. Suitable pigment biomarkers are lacking non-axenic species, bacterial abundance was low and for bacteria, and phospholipid-derived fatty acids is considered negligible. The algae were grown at a (PLFA) have become well-established chemotaxono- temperature of 15°C and a light intensity of 40 µmol mic markers (Pinkart et al. 2002, Boschker 2004). Phos- photons m–2 s–1 with a light:dark cycle of 14:10 h. The pholipids are the main cellular membrane lipids to algae were harvested during the exponential growth which a large diversity of fatty acids can be esterified. phase. We also investigated the PLFA content of a Phospholipids are rapidly degraded following cell number of cyanobacteria, but these were not included death, and therefore PLFA are representative of viable in this study because cyanobacteria were hardly ever organisms (Pinkart et al. 2002, Drenovsky et al. 2004). encountered in the phytoplankton samples. Since all known organisms contain phospholipids, this Study area and sampling. Field measurements were method can be used to derive information on other tax- done in the Scheldt estuary, a well-mixed tidal system onomic groups as well. A substantial amount of infor- in the border region between Belgium and The mation can be found in the literature on the fatty acid Netherlands (Fig. 1). Samples of surface water (0 to composition of phytoplankton groups (Volkman et al. 1 m) were taken using a Niskin sampler on board the 1989, Viso & Marty 1993, Brown et al. 1996, Renaud et RV ‘Luctor’. We sampled 5 stations, with nominal salin- al. 2002). However, this comprises nearly exclusively ities of 0, 2, 8, 18 and 28 PSU respectively, which cov- information on total fatty acids, including fatty acids ers the full salinity gradient of the estuary. The approx- derived from neutral lipids and glycolipids in addition imate locations of the sampling stations are indicated to PLFA. A limited number of papers have used PLFA on the map. The measurements were done in April, composition (Boschker et al. 2005) or total lipid derived July and October 2003. Each month, the 5 stations fatty acid composition (Shin et al. 2000, Reuss & were sampled within 3 consecutive days. Poulsen 2002) to describe phytoplankton community Sample treatment. Samples from cultured material structure, usually by looking at individual biomarker were filtered onto precombusted (400oC) GF/F filters PLFA or ratios of PLFA. (Whatman); field samples were filtered onto precom- The objective of the present study was to elaborate busted GF6 filters (Schleicher & Schuell). Samples were and refine the use of PLFA to determine phytoplankton frozen immediately in liquid nitrogen. Samples for pig- composition and abundance in natural samples. We ment analysis were stored at –80°C until extraction; have determined the PLFA composition of a number of PLFA extraction was started immediately. Samples for Dijkman & Kromkamp: PLFA as phytoplankton biomarker 115 Table 1. Species, growth medium and strain code of algae for which phospho- microscopic analysis were preserved lipid-derived fatty acids (PLFA) and pigment composition were determined. F/2: with 2% formaldehyde and stored in artificial seawater enriched with F/2 nutrients (Guillard & Ryther, 1962); F/2-Si: the dark at 5°C. Filters for the analysis identical to F/2, but Si omitted; F/20-FF: Frisian Front filter-sterilized water en- riched with F/20 nutrients; BG11: blue-green freshwater medium (Stanier et al. of particulate organic carbon (POC) 1971); CCMP: Provasoli-Guillard National Center for Culture of Marine Phyto- content were stored at –20°C and were plankton; PCC:
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