Molecular phylogenetic analysis in ecogenotoxicological studies. D. Davolos*,V. Iannilli**, E. De Matthaeis**, B. Pietrangeli*

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1 Vol. 1, no. 3-4, Molecular phylogenetic analysis in ecogenotoxicological studies D. Davolos*,V. Iannilli**, E. De Matthaeis**, B. Pietrangeli* * ISPESL, Department of Production Plants and Environmental Interaction, Rome ** University of Rome La Sapienza, Department of Animal and Human Biology ABSTRACT The usefulness of taxa belonging to the Amphipoda (Crustacea) in environmental toxicology is welldocumented in literature and a growing number of studies are addressing this line of research. However, as with most ecotoxicology studies, this research is rarely supported by analyses of the genetic structure and evolutionary history of the taxa under examination.the availability of such information becomes crucial when research is being carried out on the effects, such as genotoxic ones, of exposure to particular substances. In this work, two crustaceans (Orchestia garbinii and Gammarus aequicauda;amphipoda) from aquatic habitats and with different ecological characteristics were chosen as potential candidates for ecogenotoxicological assessment for water, as well as for sediments in toto. Data are presented on the genetic structure and on the relationships among populations of these Crustaceans, inferred by using sequences of mitochondrial genes. Furthermore, various methods are discussed, which are helpful in assessing genotoxicity in tissues of organisms exposed in the laboratory and in populations taken from contaminated sites. 69 (Key words: ecogenotoxicology, molecular phylogeny,amphipoda) BOW PO/base indexing: EUOSHA - OSH: Genetic toxicology (26601D), Environmental pollution (05481D), Measurement and assessment (12561D) CIS: Ecogenetics (Wopg), Ecotoxicology (Sepe), Crustacea (Fidu),Water pollution (Bubue), Sampling and analysis (Qe) Reviewed and accepted: 20/02/2006 by Giovanni Alfredo Zapponi; 17/03/2006 by Laura Mancini - National Institute of Health (ISS)

2 INTRODUCTION 70 The development of Community and national norms on the subject of water protection, geared initially towards the protection of drinking water, bathing water and of the consumption of edible aquatic organisms, is currently geared towards an approach of integrated protection, taking into account the necessity to safeguard the entire aquatic ecosystem. In fact, defence of the whole hydric environment from pollution caused by the introduction of dangerous substances from specific and widespread sources is necessary in order to ensure the protection of human health (e.g. from risks deriving from the transfer of contaminants through processes of bioaccumulation and biomagnification). Criteria for toxicity and ecotoxicity are therefore extremely useful for defining environmental quality standards that are necessary to achieve a good chemical state in bodies of water 1-2. The usefulness of determined taxa in environmental toxicology is well-documented in scientific literature 3-5. However, ecotoxicology studies are rarely supported by analyses of the genetic structure or the evolutionary history of the taxa under examination.the availability of this information 6-14 turns out to be indispensable when research is being carried out on the effects (e.g. the genotoxic effects) from exposure to particular substances Two Crustaceans belonging to Amphipoda and linked to aquatic environments were chosen for this study, as potential candidates for ecogenotoxicological assessment (direct, indirect and long-term effects) both for water and for sediments in toto.analyses were carried out on the talitrid, Orchestia garbinii (Fig. 1), a semiterrestrial species found along the banks of lakes and rivers in Europe, and the gammarid, Gammarus aequicauda (Fig. 2), found in salt water and the lagoon systems of the Mediterranean. Figure 1 - Orchestia garbinii (Crustacea,Amphipoda,Talitridae): adult male, 20 mm Figure 2 - Gammarus aequicauda (Crustacea,Amphipoda, Gammaridae): adult male, 15 mm In this paper, we present phylogenetic results on those crustaceans with the focus on gene sequences of mitochondrial DNA (mtdna). We will also discuss various methods that are helpful for evaluating genotoxicity and mutagenesis in tissues of organisms exposed in the laboratory and in populations taken from contaminated sites.

3 1. MATERIALS AND METHODS The sampling sites of O. garbinii were: Lake Garda (Verona ) and Lake Bracciano (Rome) (Fig. 3a,b).The samples of G. aequicauda were taken from the following sites: Lake Patria (Caserta); the mouth of the River Ombrone (Grosseto); the mouth of the River Mignone (Viterbo); the mouth of the River Candeloro, Manfredonia (Foggia). Figure 3 - Sampling sites of Orchestia garbinii: (a) Lake Garda and (b) Lake Bracciano Lake Garda (a) 71 Lake Bolsena Lake Vico Lake Bracciano (b)

4 The methods used for amplification by Polymerase Chain Reaction (PCR) and the sequencing of mitochondrial genes of the subunits I and II of the cytochrome oxidase (COI and COII) 23-5 and of 16S ribosomal RNA (16S rrna) are shown in 14, Homologous sequences of the mtdna of talitrids 14 (one sequence is deposited in GenBank, NCBI, with access number AY555730), of gammarids 28,29 and of other Crustacea (extracted from GenBank) were used to carry out phylogenetic analyses by the Neighbour- Joining and Maximum Parsimony methods 14. Molecular phylogenetic inferences were carried out by using nucleotidic sequences (examining both transitions and transversions) and the deduced amino acid sequences (with Poisson correction) 14. From 500 to 0 bootstrap replications were calculated for each phylogenetic reconstruction RESULTS 72 Mitochondrial regions encoding protein and ribosomal RNA of O. garbinii and of G. aequicauda were amplified through the PCR method and then sequenced.the alignments with homologous sequences of Crustacea generally resulted as unambiguous.the gene trna LeuUUR was found between the genes for the subunits I and II of the cytochrome oxidase (COI and COII) in G. aequicauda, while COI-NC-COII 14 rearrangement was found in O. garbinii. Inferences on the evolutionary relationships of O. garbinii and G. aequicauda (potential candidates for ecogenotoxicological assessment for water as well as for sediments) were obtained through phylogenetic reconstruction using mitochondrial sequences. Figs. 4 and 5 show some results of a phylogenetic analysis of the two Amphipods examined and of other Crustacea, based on sequences of nucleotides and amino acids encoded by the COI and COII genes. Fig. 6 shows a phylogenetic study of O. garbinii and G. aequicauda based on nucleotide sequences of ribosomal RNA of the large subunit (16S rrna). Figure 4 - Molecular phylogeny of O. garbinii, talitrids and other Crustacea (sequences extracted from GenBank) obtained through (a) Neighbour-Joining on 121 amino acids (Poisson correction) encoded by a region of the COI gene and (b) Maximum Parsimony (consensus tree) on 367 nucleotides of the COI gene Panulirus japonicus Pagurus longicarpus Penaeus monodon Orchestia gammarellus (I. Cumbrae) Orchestia gammarellus (I.Wight) Orchestia mediterranea (I.Wight) Talorchestia deshayesii (I.Wight) Talitrus saltator (I.Wight) Talitrus ssltator (I. Cumbrae) Orchestia stephenseni Orchestia garbinii (L. Garda) Orchestia garbinii (L. Bracciano) Parhjale hawaiiensis Triops cancriformis Daphnia pulex Artemia francescana Tigriopus japonicus Hyalidae Talitridae Talitroidea 0,05 (a)

5 66 Triops cancriformis Daphnia pulex Artemia francescana Panulirus japonicus Penaeus monodon Pagurus longicarpus Parhyale hawaiiensis Hyalidae Orchestia garbinii (L. Garda) Orchestia garbinii (L. Bracciano) Orchestia gammarellus (I. Cumbrae) Orchestia gammarellus (I.Wight) Orchestia mediterranea (I.Wight) Orchestia stephenseni (AY555730) Talitrus saltator (I.Wight) Talitrus saltator (I. Cumbrae) Talorchestia deshayesii (I.Wight) Talitridae Talitroidea (b) Figure 5 - Molecular phylogeny of O. garbinii, of G. aequicauda and other Crustacea (sequences extracted from Genbank) obtained through Maximum Parsimony (consensus tree) on 114 amino acids encoded by regions of the COI and COII genes Daphnia pulex Triops cancriformis Pagurus longicarpus Penaeus monodon Gammarus aequicauda (Mignone) Gammarus aequicauda (L. Patria) Gammarus aequicauda (Ombrone) Gammarus aequicauda (Candeloro) Parhyale hawaiiensis Hyalidae Orchestia garbinii (L. Bracciano) Orchestia garbinii (L. Garda) Talitrus saltator (I.Wight) Talitrus saltator (I. Cumbrae) Talorchestia deshayesii (I.Wight) Orchestia gammarellus (I.Wight) Orchestia gammarellus (I. Cumbrae) Orchestia mediterranea (I.Wight) Gammaridae Talitridae Talitroidea 73 Figure 6 - Molecular phylogeny of O. garbinii, of G. aequicauda and of other Crustacea (sequences extracted from GenBank) obtained through Maximum Parsimony (consensus tree) on 246 nucleotides of the 16S rrna gene (500 bootstrap replications) Pagurus longicarpus Penaeus monodon Gammarus locusta Gammarus aequicauda (Black Sea) Gammarus aequicauda (L. Patria) Gammarus aequicauda (Mignone) Gammarus balcanicus Gammarus fasciatus Gammarus mucronatus Gammarus annulatus Gammarus oceanicus Gammarus elvirae Gammarus lacustris (L. Hovsgol) Chaetogammarus marinus Orchestia garbinii (L. Garda) Orchestia garbinii (L. Bracciano) Orchestia cavimana (AY744911) Parhyale hawaiiensis Hyalidae Gammaridae Talitridae Talitroidea

6 3. DISCUSSION 74 Many human activities (in the industrial, urban, agricultural sectors, etc.) have caused an increase in the environmental concentration of particular pollutants including heavy metals, mutagenic substances, etc.the negative effects (direct and indirect) of xenobiotic agents can be significant in natural populations 12-30, with a potential risk of exposure and repercussions on human health 31. In recent years, many research projects have focussed attention on the identification of species that are useful in ecogenotoxicological assessments on different types of matrices. However, the lack of phylogenetic analyses of the taxa under examination may entail a margin of error in the interpretation of the research results, e.g. environmental-genotoxicological 16,17,21,22. Low levels of genetic divergence found among the populations of O. garbinii validate this organism as a suitable subject for ecotoxicological investigation on various geographical scales It should be noted that our research group is involved in further molecular studies to examine populations of O. garbinii and G. aequicauda sampled in other geographical areas, analysing especially the control region of mtdna which generally presents hypervariable portions 36 and non-coding mitochondrial segments 14,37,38. Furthermore, studies into genotoxicology 39 and mutagenesis (Fig. 7) are underway on organisms exposed in the laboratory. Figure 7 - Nucleotidic mutation in the COI gene highlighted by sequencing of mtdna. (Davolos, study pending).the chromatograms are visualized with Chromas software version

7 4. CONCLUSIONS Due to their biological characteristics and the ease with which they may be grown in the laboratory 22,40, the O. garbinii and G. aequicauda species analyzed here are particularly suited to experiments on genotoxicological exposures. In literature, we can find various molecular protocols that are used to assess the levels of genotoxicity 18,31,41. Among these, the electrophoretic analysis of DNA samples in agarose gel is useful for the identification and quantification of the kind of damage caused at DNA level 39, In addition, using in vivo and in vitro methods followed in DNA sequencing analysis, it is possible to identify any nucleotidic mutations induced 21,22,45. Nevertheless, the information on the genetic structure of the populations examined is absolutely necessary for the interpretation of the results of environmental-genotoxicological studies REFERENCES 1. Italia. Decreto Legislativo 11 maggio 1999, n. 152.Testo aggiornato del decreto legislativo 11 maggio 1999, n. 152, recante: Disposizioni sulla tutela delle acque dall inquinamento e recepimento della direttiva 91/271/CEE concernente il trattamento delle acque reflue urbane e della direttiva 91/676/CEE relativa alla protezione delle acque dall inquinamento provocato dai nitrati provenienti da fonti agricole, a seguito delle disposizioni correttive ed integrative di cui al decreto legislativo18 agosto 2000, n Gazzetta Ufficiale n. 246, Supplemento Ordinario n. 172, 20 ottobre Unione Europea. Direttiva 2000/60/CE del Parlamento Europeo e del Consiglio del 23 ottobre 2000 che istituisce un quadro per l azione comunitaria in materia di acque. Gazzetta ufficiale delle Comunità europee L327/1-72, 22 dicembre Schulz R. Using a freshwater amphipod in situ bioassay as a sensitive tool to detect pesticide effects in the field. Environ Toxicol Chem 2003;22: Schill RO, Kohler HR. Does the environment or the source of the population define stress status and energy supply in the freshwater amphipod Gammarus fossarum? Ecotoxicology 2004;13: Borgmann U, Couillard Y, Doyle P, Dixon DG.Toxicity of sixty-three metals and metalloids to Hyalella azteca at two levels of water hardness. Environ Toxicol Chem 2005;24: Meyran JC, Monnerot M,Taberlet P.Taxonomic status and phylogenetic relationships of some species of the genus Gammarus (Amphipoda) from mtdna sequences. Mol Phylogenet Evol 1997;8: Meyran JC, Gielly L,Taberlet P. Environmental Ca and mtdna polymorphism among populations of Gammarus fossarum (Amphipoda). Mol Ecol 1998;7: Meyran JC, Taberlet P. mtdna polymorphism among alpine populations of Gammarus lacustris (Amphipoda). Freshw Biol 1998;39: Müller J. Mitochondrial DNA variation and the evolutionary history of cryptic Gammarus fossarum types. Mol Phylogenet Evol 2000;15: De Matthaeis E, Davolos D, Cobolli M Genetic divergence between populations and species of talitrids from Aegean islands. J Hered 2000;89: De Matthaeis E, Davolos D, Cobolli M, Ketmaier V. Isolation by distance in equilibrium and non equilibrium populations of four talitrid amphipod species in the Mediterranean sea. Evolution 2000;54: Davolos D, Ketmaier V, Cobolli M, De Matthaeis E. Struttura genetica e livelli di differenziamento tra popolazioni e specie di Orchestia (Amphipoda, Talitridae) del Mediterraneo. Biogeographia 2002;23:

8 Iannilli V, Ketmaier V, Ruffo S, De Matthaeis E. Multidisciplinary approach to the systematics of the Italian freshwater Gammarus (Amphipoda). In: Proceedings of the 4th European Crustacean Conference. Lodz (Poland); Abstracts, p Davolos D, Maclean N. Mitochondrial COI-NC-COII sequences of talitrid amphipods (Crustacea). Heredity 2005;94: Hogg ID, Larose C, de Lafontaine Y, Doe KG. Genetic evidence for a Hyalella species complex within the Great Lakes - St. Lawrence River drainage basin: implications for ecotoxicology and conservation biology. Can J Zool 1998;76: Stanton JL, Schizas NV, Chandler GT, Coull BC, Quattro JM. Ecotoxicology and population genetics: the emergence of phylogepgraphic and evolutionary ecotoxicology. Ecotoxicology 2001;10: Theodorakis CW. Integration of genotoxic and population genetic endpoints in biomonitoring and risk assessment. Ecotoxicology 2001;10: Perkins EJ, Lotufo GR. Playing in the mud-using gene expression to assess contaminant effects on sediment dwelling invertebrates. Ecotoxicology 2003;12: Whitehead A, Anderson SL, Kuivila KM, Roach JL, May B. Genetic variation among interconnected populations of Catostomus occidentalis: implications for distinguishing impacts of contaminants from biogeographical structuring. Mol Ecol 2003;12: Snape JR, Maund SJ, Pickford DB, Hutchinson TH. Ecotoxicogenomics: the challenge of integrating genomics into aquatic and terrestrial ecotoxicology.aquat Toxicol 2004;67: Davolos D, Pietrangeli B, Maclean N. Mitochondrial DNA sequence analysis and molecular phylogeny of Orchestia cavimana (Crustacea) in freshwater genotoxicological studies. In: Proceedings of the 34th Annual Meeting of the European Environmental Mutagen society (EEMS 2004). Maastricht, the Netherlands: University of Maastricht; 2004.Abstracts PW Davolos D, Maclean N, Pietrangeli B. A molecular phylogenetic study of the freshwater Orchestia cavimana (Crustacea). Riv Biol 2004;97: Capaldi RA.The complexity of a respiratory complex. Nature Struct Biol 1996;3: Saraste M. Oxidative Phosphorylation at the fin de siècle. Science 1999;283: Tsukihara T,Aoyama H,Yamashita E,Tomizaki T,Yamaguchi H, Shinzawa-Itoh, et al. Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 Å. Science 1995;269: Davolos D, Maclean N. Evolutionary relationships among supralittoral talitrid amphipods (Crustacea) inferred from mitochondrial sequence analysis. In: Proceedings of the XXI Giornata dell Ambiente. Aree costiere. Roma, Italy:Accademia Nazionale dei Lincei. [2004];205: Müller JC, Schramm S, Seitz A. Genetic and morphological differentiation of Dikerogammarus invaders and their invasion history in Central Europe. Fresh Biol 2002;47: Macdonald KS III,Yampolsky L Duffy JE. Molecular and morphological evolution of the amphipod radiation of Lake Baikal. Mol Phylogenet Evol 2005;35: Iannilli V, De Matthaeis E. Genetic divergence within Gammarus aequicauda (Martynov, 1931) based on 16S mitochondrial DNA. In: Proceedings of The Sixth International Crustacean Congress. Glasgow, Scotland UK: University of Glasgow; Wurgler FE, Kramers PG. Environmental effects of genotoxins (eco-genotoxicology). Mutagenesis 1992;7: Jha AN. Genotoxicological studies in aquatic organisms: an overview. Mutat Res 2004;552: Sato H, Aoki Y. Mutagenesis by environmental pollutants and bio-monitoring of environmental mutagens. Curr Drug Metab 2002;3:311-9.

9 33. De Matthaeis E, Ketmaier V, Latella L, Ruffo S, Scapini F,Tarocco M. Multidisciplinary approach to the study of a terrestrial Amphipod: the case of Orchestia cavimana. In: Proceedings of the IV European Crustacean Conference. Lodz, Poland; Abstracts Ketmaier V,Amendola D, Scapini F, De Matthaeis E. Large scale phylogeography of the landhopper Orchestia cavimana: combining allozymes and mtdna. In: Proceedings of the XIth International Colloquium on Amphipoda.Tunis; Fialkowski W, Rainbow PS, Smith BD, Zmudzinski L. Seasonal variation in trace metal concentrations in three talitrid amphipods from the Gulf of Gdansk, Poland. J Exp Mar Biol Ecol 2003;288: Chu KH, Li CP,Tam YK, Lavery S.Application of mitochondrial control region in population genetic studies of the shrimp Penaeus. Mol Ecol Notes 2003;3: Davolos D, Iannilli V, De Matthaeis E.Analysis on the mitochondrial region between the COI and COII genes in Crustacea. In: Proceedings of The Sixth International Crustacean Congress. Glasgow, Scotland UK: University of Glasgow; Davolos D, Iannilli V, De Matthaeis E. Molecular analysis on the mitochondrial COI-tRNALeuUUR- COII region in Gammarus aequicauda (Amphipoda, Gammaridae). In: Proceedings of the First Congress of Italian Evolutionary Biologists. Ferrara, Italy: University of Ferrara; Setini A, Iannilli V. DNA strand breakage come biomarker di esposizione ai metalli. In: Proceedings of the 66th Annual Congress of the U.Z.I Sept Roma, Italy: Hecker A, Quennedey B,Testeniere O, Quennedey A, Graf F, Luquet G. Orchestin, a calcium-binding phosphoprotein, is a matrix component of two successive transitory calcified biomineralizations elaborated by a terrestrial crustacean. J Struct Biol 2004;146: Lee RF, Steinert S. Use of the single cell gel electrophoresis/comet assay for detecting DNA damage in aquatic (marine and freshwater) animals. Mutat Res 2003;544: Costa FO, Neuparth T, Costa MH,Theodorakis CW, Shugart LR. Detection of DNA strand breakage in a marine amphipod by agarose gel electrophoresis: exposure to X-rays and copper. Biomarkers 2002;7: Dixon DR, Pruski AM, Dixon LR, Jha AN. Marine invertebrate eco-genotoxicology: a methodological overview. Mutagenesis 2002;17: Park S, Imlay JA. High levels of intracellular cysteine promote oxidative DNA damage by driving the fenton reaction. J Bacteriol 2003;185: Braman J (ed.). In Vitro Mutagenesis Protocols. 2nd Edn.Totowa NJ: Humana Press;

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