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MALDI-TOF MS) for the Identification of Freshwater Zooplankton: a Pilot Study with Three Eudiaptomus (Copepoda: Diaptomidae) Species

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MALDI-TOF MS) for the Identification of Freshwater Zooplankton: a Pilot Study with Three Eudiaptomus (Copepoda: Diaptomidae) Species JOURNAL OF PLANKTON RESEARCH j VOLUME 34 j NUMBER 6 j PAGES 484–492 j 2012 Potential of matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) for the identification of freshwater zooplankton: a pilot study with three Eudiaptomus (Copepoda: Diaptomidae) species NICOLETTA RICCARDI1, LARA LUCINI2, CINZIA BENAGLI2, MARTIN WELKER3, BARBARA WICHT2 AND MAURO TONOLLA2,4* 1 2 CNR-INSTITUTE OF ECOSYSTEM STUDY, 28922 VERBANIA PALLANZA, ITALY, CANTONAL INSTITUTE OF MICROBIOLOGY, VIA MIRASOLE 22A, CH-6500 3 4 BELLINZONA, SWITZERLAND, ANAGNOSTEC GMBH, AM MU¨ HLENBERG 11, 14476 POTSDAM-GOLM, GERMANY AND MICROBIAL ECOLOGY, MICROBIOLOGY UNIT, BIVEG DEPARTMENT, UNIVERSITY OF GENEVA, 30, QUAI ERNEST ANSERMET, 3000 GENEVA, SWITZERLAND *CORRESPONDING AUTHOR: [email protected] Received October 7, 2011; accepted in principle March 2, 2012; accepted for publication March 6, 2012 Corresponding editor: Beatrix E. Beisner The accurate identification of individuals in zooplankton samples is a crucial step in many plankton studies. Up to now, this has been done primarily by microscopic analysis of morphological characters, and new molecular methodologies are still relatively rarely applied. Another promising technology is matrix-assisted laser de- sorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS), which has had a major impact in applied and systematic microbiology, where it is used for routine high throughput identification of bacteria and fungi. For the present study, we developed a protocol for the rapid acquisition of mass spectra from whole individual copepods. The final protocol enabled us to obtain mass spectra with more than 100 distinct peaks in the mass range of 2000–20 000 Da. A com- parison of the mass spectra of three species of Eudiaptomus showed that they could all be clearly discriminated, whereas the mass spectra of different developmental stages and sexes of each particular species were highly similar. Further, a discrim- ination of con-specific individuals from different habitats was achieved, at least partly, even without extensive optimization of the analytical and statistical proce- dures. These results indicate the feasibility of identifying copepods by a rapid and simple MALDI-TOF MS analysis, e.g. for population ecology studies. KEYWORDS: Eudiaptomus; MALDI-TOF MS; identification INTRODUCTION and laborious, and requires considerable experience The taxonomic discrimination of zooplankton species (Mauchline, 1998; Thum and Derry, 2008; Jagadeesan relies on subtle morphological characteristics, which et al., 2009). For example, copepod species identification makes routine identification of individuals very difficult generally involves careful dissection and examination of doi:10.1093/plankt/fbs022, available online at www.plankt.oxfordjournals.org. Advance Access publication April 6, 2012 # The Author 2012. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected] N. RICCARDI ET AL. j IDENTIFICATION OF EUDIAPTOMUS SP.USING MALDI-TOF MS minute morphological characters located on different zooplankton specimens could be the use of matrix- parts of the male or the female, such as the female assisted laser desorption/ionization time-of-flight mass genital somite and the male mating appendages in cala- spectrometry (MALDI-TOF MS), a technology that has noid families/genera (Ranga Reddy, 1994; Dussart and had a major impact in many fields of the life sciences Defaye, 1995), and/or the fourth leg coxa and the fifth over the last two decades (Duncan et al., 2008; Karr, pair of legs in cyclopoids and poecilostomatoids (Einsle, 2008; Seng et al., 2010; Welker, 2011). 1996; Karaytug, 1999; Bo¨ttger-Schnack and Schnack, MALDI-TOF MS of whole cells has been recently 2009). Depending on which morphological feature applied to the identification of bacteria and fungi in proves most useful for species discrimination, taxonomic clinical, plant and veterinary microbiology (Seng et al., keys to species within each genus are frequently based 2009; Kallow et al., 2010, Rezzonico et al., 2010). This on either male or female characters, while equally technology takes advantage of the fact that whole cells detailed descriptions of both sexes are rarely provided can be analyzed after a simple single-step extraction (Mauchline, 1998). For instance, taxonomic keys for the procedure without any further preparation steps. The identification of Eudiaptomus species are generally based resulting mass spectra display peak patterns that have on the morphology of males due to the lack of unam- been shown to be phylogenetic markers in a mass range biguous morphological differences between females of 2–20 kDa (Wynne et al., 2009). For bacteria, or pro- (Kiefer, 1968; Petkowski, 1983; Stella, 1984). This con- karyotes in general, it has been shown that the peaks tributes to a recurring problem in routine zooplankton recorded in MALDI-TOF mass spectra can be assigned analysis, matching the females to the males of each to ribosomal proteins (Teramoto, 2009; Kallow et al., species. Moreover, immature copepod stages cannot 2010), thus representing biomarkers that can be used in generally be identified to species (or even genus) level taxonomic studies (Kroppenstedt et al., 2005) and also (MacManus and Katz, 2009; Bucklin et al., 2010) and for routine identification (Freiwald and Sauer, 2009). are pooled under more or less generic categories that Among eukaryotes, it is primarily yeasts and moulds can even include the total number of copepod nauplii of importance in medical and food safety that have or copepodites in multi-species copepod assemblages. been analyzed by MALDI-TOF MS (Erhard et al., Studies of zooplankton assemblages are therefore 2008; Marinach-Patrice et al., 2009). An equal potential often limited by the impossibility of assessing the actual for species discrimination and identification has been abundance of each species population, which affects recognized, although the identity of the compounds biodiversity and ecological assessment. This applies to detected (mostly proteins) is not fully understood: along all groups of holozooplankton, including calanoid cope- with ribosomal proteins, it is mostly cell-wall-associated pods, for which species identification is further compli- proteins that seem to be recorded (Hettick et al., 2008). cated by the existence of several groups of closely The excellent results obtained with microorganisms related sibling species that can be difficult or impossible have prompted a number of studies to assess the poten- to distinguish using morphological characters (Thum tial of MALDI-TOF MS for discriminating species of and Derry, 2008). Since accurate taxonomic species metazoa. The outcome of these studies is equally prom- identification at all life stages is critical for ecological ising, as they have shown that species discrimination studies, the use of molecular methods complementary based on mass spectral pattern is possible for nematodes to traditional morphological analysis is rapidly growing (Perera et al., 2005a), various insect taxa (Perera et al., (MacManus and Katz, 2009). Molecular approaches, in- 2005b; Feltens et al., 2010; Kaufmann et al., 2011), cluding DNA barcoding and community metagenomics, bivalves (Lopez et al., 2005) and fish (Mazzeo et al., can assess species diversity (Bucklin et al., 2010; 2008; Volta et al., 2012). Radulovici et al., 2010), reveal cryptic and new species In this context, MALDI-TOF MS analysis appears to (Belyaeva and Taylor, 2009), elucidate phylogenetic rela- be a promising tool for plankton ecology studies. Its po- tionships (Bucklin and Frost, 2009) and identify species tential in limnological studies has already been shown, from diapausing eggs (Briski et al., 2011). However, most for example, by the clonal typing of Microcystis of these methods are applied in ecological studies with (Cyanobacteria) colonies based on metabolomic profiles a focus on evolutionary questions (Selkoe and Toonen, (Welker et al., 2007). In the present pilot study, we 2006; Costa and Carvalho, 2010; Yebra et al., 2011). For sought to explore the potential of mass spectral analysis the rapid identification of individuals, techniques based for the taxonomic identification of zooplankton. We on nucleotide sequences (still) have the disadvantage of chose diaptomid copepods (Copepoda: Calanoida: requiring a number of steps, i.e. DNA extraction, poly- Diaptomidae), the most diverse group of freshwater merase chain reaction, gel electrophoresis, etc. Another calanoids, with over 400 species in more than 50 approach for fast, high throughput identification of genera (for a complete list of species, see http://www 485 JOURNAL OF PLANKTON RESEARCH j VOLUME 34 j NUMBER 6 j PAGES 484–492 j 2012 .nmnh.si.edu/iz/copepod). We focused on three of the padanus are almost indistinguishable, we considered only five species of Eudiaptomus recorded in Italian waters copepodites of the third Eudiaptomus species (Eudiaptomus (Stoch, 2005) which are most representative of the cala- intermedius), which never co-occur with the other two noid assemblages of the Northern Italian water bodies species (Tavernini et al., 2003). Males, females and cope- (Stella, 1984; Tavernini et al., 2003; Riccardi and podites of Mixodiaptomus tatricus were obtained from dif- Rossetti, 2007). ferent collections, analyzed and used as an outgroup. The aims of the study were, first, to develop a simple and straightforward protocol for mass spectral analysis
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