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Microbial Ecology View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Electronic Publication Information Center Microbial Ecology Picoeukaryotic Plankton Diversity at the Helgoland Time Series Site as Assessed by Three Molecular Methods L.K. Medlin1, K. Metfies1, H. Mehl1, Karen Wiltshire2 and K. Valentin1 (1) Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, D-27570 Bremerhaven, Germany (2) Alfred Wegener Institute for Polar and Marine Research Biologische Anstalt Helgoland, D-27498 Helgoland, Germany Received: 8 April 2005 / Accepted: 8 July 2005 / Online publication: 19 May 2006 Abstract similar accuracy and with higher throughput for a more in-depth analysis. We analyzed picoeukaryote assemblages in the German Bight at the Helgoland time series site by sequencing cloned eukaryotic 18S rRNA genes in six genetic libraries plus one library from the Orkney Islands from a cruise of Introduction opportunity. The libraries were constructed from envi- Picoplanktons (defined operationally as cells that pass ronmental samples collected at different periods of the through a 3-mm filter) dominate the photosynthetic year. The same samples were also analyzed using a biomass in many marine ecosystems, not only in the fingerprinting technique, single-strand conformational very oligotrophic regions of the world oceans, such as the polymorphism (SSCP), and DNA microarrays with Eastern Mediterranean Sea, but also in mesotrophic class-level oligonucleotide probes. One hundred unique areas. However, picophytoplanktons are clearly not clones were analyzed from each library, thus insuring exclusively restricted to pelagic environments. In many over 85% coverage of the library. The V4 region of the coastal regions, they are present throughout the year and 18S rRNA gene was sequenced from each of these clones, constitute a Bbackground^ population, onto which thus providing the most discrimination among the episodic phenomena, such as the spring bloom, develop. clones. The nonphotosynthetic picoeukaryotic compo- In some environments, such as coastal lagoons, pico- nent dominated over the photosynthetic one and was plankton can be a major component of biomass and represented by the ciliates at 45% and group II alveolates productivity for most of the year. In addition, some at 42%. Prasinophytes dominated the photosynthetic bloom-forming picoplankters, such as Aureococcus, are group at 40%, but other picoplankton groups, such as toxic. However, to date, fewer than 30 species of bolidomonads and chrysophytes, were also present. picoeukaryotic phytoplankton have been described. A Totally novel groups were found in the cryptomonads clear proof of our poor knowledge of picoeukaryotic and in the dinoflagellates. A new algal group sister to the phytoplankton diversity is revealed by the discovery/ cryptophyte nuclear gene and the glaucocystophytes was recognition of four novel algal classes in the last 10 years also found. These three groups have been found in other described from picoeukaryotic phytoplanktonic taxa picoeukaryotic planktonic clone libraries. SSCP analyses [1, 8, 10, 18]. A fifth one will soon be published at closer time intervals suggest that clone libraries should discovered within EU PICODIV (Not, Valentin, Romari, be made at weekly intervals if succession in the Lovejoy, Massana, Vaulot, Medlin, unpublished data). picoeukaryotic plankton community is to be monitored Because so little is known about the taxonomy and accurately. A comparison of annual samples suggests systematics of picoeukaryotic phytoplankton, we have that there appears to be an annual cycle with regard to very little data to estimate the levels of its biodiversity species composition. Microarray analysis supported the under natural conditions and how picoeukaryotic phy- clone library data and offered a faster means of toplanktons are affected by environmental variability community analysis, which can be performed with linked to either anthropogenic influence or to larger- scale phenomena, such as those linked to climate change Correspondence to: L.K. Medlin; E-mail: [email protected] or global warming. As part of the EU PICODIV project, DOI: 10.1007/s00248-005-0062-x & * Springer Science+Business Media, Inc. 2006 1 2 L.K. MEDLIN ET AL.: PICOEUKARYOTIC PLANKTON DIVERSITY the biodiversity of the picoplanktonic community was flagellates have been performed on a weekly basis since assessed at three coastal sites: Roscoff in the English 1962 (see details in [29]). Samples are taken from the Channel [25], Blanes in the western Mediterranean Sea surface at a 5- to 8-m depth station. The water is not [16], and at Helgoland in the German Bight. We present fractionated, and identification is primarily confined to here the results from Helgoland with the diversity of its cells in the nanoplankton and above size range. Salinity, picoeukaryotic planktonic community assessed by three temperature, and nutrients are also measured daily. We molecular methods: environmental clone libraries, sin- sampled at a fixed location over the entire sampling gle-strand conformation polymorphisms (SSCPs), and period so that the changes that we see here can be class-level molecular probes detection with microarray interpreted as temporal changes at a single site. All trends technology (phylochips). in our data are supported by similar observations in Molecular methods are needed for the understanding bacterial and microplankton fractions for the same and describing the total diversity present in all marine period. aquatic environments, especially for the in situ picoeu- Environmental samples from which clone libraries karyotic phytoplankton diversity, and because members were made were taken at Helgoland to coincide with set of this community are small and possess few morpho- time points in the annual cycle of the phytoplankton at logical markers that can be used for identification using Helgoland: March and April 2000 (spring bloom), traditional methods. In nearly all instances where August and October 2000 (summer–fall bloom), Decem- molecular methods have been applied to answer ques- ber 2000 (shortest day length), and February 2001 tions about diversity in aquatic habitats, novel taxa and (lowest temperature). In addition to these dates, monthly hidden biodiversity have been uncovered [2, 3, 13, 14, 16, samples were taken between January 2001 and May 2002. 19, 25]. Our study of the Helgoland picoeukaryotic One sample from the Orkney Islands was also analyzed plankton community is no exception. from a cruise of opportunity. Samples were taken with a bucket just below the surface and were filtered twice through 3-mm Millipore filters to insure that no larger cells could escape the Materials and Methods filtration. The filters always showed some brownish color Sampling Site. The Helgoland time series station is even after the second round of 3-mm filtration. In located at 54-11.30N, 7-54.00E in the central German general, filters at the Helgoland site clogged faster than Bight of the North Sea (Fig. 1). Cell counts and those at Blanes or Roscoff probably because of its higher identification of diatoms, dinoflagellates, and other load with sand and mud and because of its low depth Figure 1. Location of the three coastal sites sampled in the EU PICODIV project with details of the Helgoland Times Series site in the German Bight. L.K. MEDLIN ET AL.: PICOEUKARYOTIC PLANKTON DIVERSITY 3 and comparably high turbulence. Filters were immedi- imported into ARB [14] (http://www.mikro.biologie.tu- ately stored in liquid nitrogen until processing for muenchen.de) and generally aligned automatically using molecular use. CLUSTAL-W within ARB using a secondary structure Two-hundred-microliter aliquots of unfiltered ma- model. Then all sequences were compared against Gen- terial were inoculated into 2 mL of Drebes [4] or IMR/2 Bank using a BLAST search to obtain the best hits, which [7]. Following this dilution, a fourfold serial dilution were added to the tree maintained by ARB. Phylogenetic using 200 mL was established in each of the two media. analyses were performed using Bayesian methods [9] with Flasks showing growth after several months were assessed a gamma distribution. Different nested models of DNA for purity by light microscopy and by SSCP. substitution and associated parameters were estimating using Modeltest 3.0 [23]. These parameters were used to Isolation of Genomic DNA. DNA was prepared using process the NJ and MP analysis for bootstrap analyses of chemical lysis from 0.2-mm filters with a DNA extraction 1000 replicates using PAUP*4.0b10 version [28]. Plant kit (PAN Biotechnology) to insure comparable preparation for different sampling sites and time points. Single-strand conformation polymorphism. Single-strand Typically from 200 to 300 mL of a G3-mm seawater conformation polymorphism was initially developed for fraction, enough DNA was obtained to run 10–30 18S the analysis of bacterial communities [26], and we polymerase chain reactions (PCRs). adapted it to assess the eukaryotic picoeukaryotic plank- ton community. SSCP is a PCR-based method in which a Amplification of Ribosomal RNA Genes. For subsequent fraction of the 18S gene is amplified and a single-strand cloning, 18S rDNA PCR was performed with primers product is produced by digestion of the opposite strand. of Medlin et al. [15] in an Eppendorf gradient cycler The single strands are separated in an acrylamide gel be- using standard conditions, Perkin Elmer Taq polymerase cause they assume different
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