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Facsimile Del Frontespizio Della Tesi Di Dottorato Alma Mater Studiorum – Università di Bologna DOTTORATO DI RICERCA IN Scienze Ambientali: tutela e gestione delle Risorse Naturali Ciclo XXVII Settore Concorsuale di afferenza: 05/A1 Settore Scientifico disciplinare: BIO/01 The harmful benthic dinoflagellate Ostreopsis cf. ovata: biotic factors affecting its growth and toxicity Presentata da: Flavio Guidi Coordinatore Dottorato Relatore Enrico Dinelli Silvana Vanucci Tutore Rossella Pistocchi Esame finale anno 2016 This thesis is dedicated to my mother and father, my inspiration 2 TABLE OF CONTENTS Introduction .......................................................................................................... 5 1. HABs: Harmful Algal Blooms ......................................................................... 5 2. Target species: Ostreopsis cf. ovata .................................................................. 7 3. Palytoxin group .............................................................................................. 12 4. Biotic factors influencing O. cf. ovata bloom dynamics with emphasis on microalgal-bacterial interactions ....................................................................... 16 4.1. Microalgal-bacterial interactions ........................................................................... 20 4.2. Main bacterial taxa found associated with toxic dinoflagellates ........................... 22 4.3. Some aspects on bacterial-viral relationships ........................................................ 29 4.3.1. Bottom-up and top-down control on bacterial communities ............................... 32 References ........................................................................................................... 33 Aims .................................................................................................................... 59 Chapter 1 ............................................................................................................ 61 (Inorganic nutrients uptake and organic phosphorus utilization by Ostreopsis cf. ovata) Chapter 2 ............................................................................................................ 72 (Phylogenetic structure of bacterial assemblages co-occurring with Ostreopsis cf. ovata bloom) Chapter 3 .......................................................................................................... 129 (Microbial dynamics along the toxic dinoflagellate Ostreopsis cf. ovata growth: bacterial phylogenetic succession and viruses top-down control) Overall conclusions .......................................................................................... 179 Acknowledgments .............................................................................................. 183 3 4 Introduction 1. HABs: Harmful Algal Blooms The acronym HABs (i.e. Harmful Algal Blooms) designate microalgae outbreaks directly or indirectly harmful for the ecosystem and the human health (Anderson, 1992; Hallegraeff, 1993). In the last years, HABs have been reported with increasing frequency and areal distribution, thus research efforts have been aimed at investigating the conditions and the factors that trigger or regulate these phenomena. Within the approximately 4000 identified marine microalgae, about 200 including diatoms, dinoflagellates, haptophytes, raphydophytes, cyanophytes and pelagophytes can generate negative events (mostly dinoflagellates), whereof about 80 synthetize toxins (Zingone and Enevoldsen, 2000; Smayda and Reynolds, 2003). In addition, the number of harmful algal species discovered is constantly growing. A noxious phytoplanktonic bloom (also known as “red tide”; Fig. 1) is characterized by a sudden increase in microalgal cell abundances, which reach high values (e.g. 104-105 cells mL-1) in a variable time span (1-3 weeks; Masò and Garcés, 2006). Blooms maybe harmful either due to the high biomass or to toxin production depending on the algal species involved; synergy of both the factors is sometimes reported. Algal species producing toxins can have severe impacts on human health (i.e. biointoxications) causing sometimes the death mainly through seafood consumption or aerosol inhalation and contact, while high biomasses can generate negative effects on the ecosystem (hypoxia/anoxia) and on the recreational activities (Garcés et al., 1999; Botana et al., 2014). 5 Fig. 1. A spectacular non-toxic “red tide” bloom of Noctiluca scintillans in New Zealand (A; photo by M. Godfrey), a toxic cyanobacterial bloom at Lake Erie (B; photo by Tom Archer/University of Michigan), and a non-toxic bloom of Noctiluca miliaris in Hong Kong (C; photo by Kin Cheung). Toxins produced by algal species encompass a wide range of organic compounds with different molecular weight (from few hundreds to more than 1.000 Da) and solubility characteristics. These molecules are mainly produced by phytoplanktonic and phytobenthic organisms but also from heterotrophic bacteria, the latter being involved in modification processes as well. Bivalve mollusks are one of the most common vectors, as they can bioaccumulate large amount of toxins in tissues by filter-feeding. A first grouping within algal biotoxins can be done between water- soluble and fat-soluble toxins (Poletti et al., 2003). For long time biotoxins have been classified on a symptomatic base as: Paralytic shellfish poisoning (PSP); Diarrhoetic shellfish poisoning (DSP); Neurotoxic shellfish poisoning (NSP); Azaspiracid poisoning (AZP); Amnesic shellfish poisoning (ASP), related to diatoms; Ciguatera fish poisoning (CFP), provoked by dinoflagellates and spread to the humans by fishes. Nowadays this classification is rather debated, as some compounds has been wrongly grouped in a cluster only because of the concomitantly presence of other known toxins, although they showed different effects and chemical structure. Therefore, it 6 has been considered more adequate to distinguish toxin based on their chemical structure as follows (Toyofuku, 2006; Tubaro et al., 2010; Botana et al., 2014): Saxitoxin group (STX); Okadaic acid group (OA); Pectenotoxin group (PTX); Yessotoxin group (YTX); Domoic acid group (DA); Brevetoxin group (BTX); Azaspiracid group (AZA); Ciguatera group; Cyclic imine group and Palytoxin group (PLTX). Toxins are secondary metabolites differing for structure, elemental composition and functional activity (Granéli and Flynn, 2006), and their synthesis rate depends on availability and utilization of primary metabolites which are precursors. In turn, primary metabolites synthesis vary in relation to nutrients availability, cell cycle and cell growth phase (Flynn and Flynn, 1995; Pistocchi et al., 2014). As general, changes in toxin cell content are related with physiological stress or with the shift from exponential to the stationary growth phase of the algae (Edvardsen et al., 1990, Anderson 1994; Flynn et al., 1994, 1996; Granéli et al., 1998; Johansson and Granéli 1999a,b; Vanucci et al., 2012a; Pezzolesi et al., 2014; Pistocchi et al., 2014). However, the abiotic and biotic factors that trigger or regulate toxin production in many algal species are still largely unknown (Katircioglu et al., 2004). 2. Target species: Ostreopsis cf. ovata Phylum Dinoflagellata Class Dinophyceae Order Peridiniales Family Ostreopsidaceae Genus Ostreopsis Species Ostreopsis cf. ovata Dinoflagellates belonging to the Ostreopsidaceae family are found in the benthic microalgal assemblage both in temperate and tropical areas (Faust et al., 1996). As for their planktonic counterparts, it is hypothesized that benthic dinoflagellates are mixotrophic and auxotrophic for at least some vitamins. Only the two species Ostreopsis siamensis and Ostreopsis cf. ovata have 7 been retrieved in the Mediterranean in the 70’s and the 90’s, respectively (Taylor, 1979; Tognetto et al., 1995), whereof O. cf. ovata (Fig. 2) is the most common and abundant species (Vila et al., 2001; Penna et al., 2005; Aligizaki and Nikolaidis, 2006; Turki et al., 2006; Battocchi et al., 2010; Totti et al., 2010; Accoroni et al., 2011; Mangialajo et al., 2011). The lack of a monitoring program for the microphytobenthic communities along the Mediterranean coasts do not allow to establish when these species have been introduced in the basin (with ballast water for instance) or whether they were already present as autochthonous at low densities. However, the increasing in Ostreopsis spp. bloom event frequencies, intensities and distribution along the Mediterranean coasts in the last decade is evident, raising the attention of the scientific community and of the environmental management authorities. As a result, taxonomical, genetic, ecological and toxicological studies intensified in this period (e.g. Vila et al., 2001; Penna et al., 2005; Turki, 2005; Aligizaki and Nikolaidis, 2006; Ciminiello et al., 2006, 2008; Riobò et al., 2006; Aligizaki et al., 2008; Ledreux et al., 2009; Guerrini et al., 2010; Vanucci et al., 2012a; Pezzolesi et al., 2012, 2014; Accoroni et al., 2015a,b; Pinna et al., 2015; Tartaglione et al., 2016). Fig. 2. Light microscopy micrograph of an O. cf. ovata culture. 8 The genus Ostreopsis was firstly designated with the species O. siamensis Schmidt (1901). Nevertheless, the genus was negligibly taken into consideration until taxonomical studies of Fukuyo allowed to describe two more species: O. ovata Fukuyo (1981) and O. lenticularis Fukuyo (1981). Six other species were successively added: O. heptagona Norris, Bomber and Balech (1985), O. mascarenensis Quod (1994),
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