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Contrasting Diversity of Phycodnavirus Signature Genes in Two Large and Deep Western European Lakes

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Contrasting Diversity of Phycodnavirus Signature Genes in Two Large and Deep Western European Lakes bs_bs_banner Environmental Microbiology (2014) 16(3), 759–773 doi:10.1111/1462-2920.12201 Contrasting diversity of phycodnavirus signature genes in two large and deep western European lakes Xu Zhong and Stéphan Jacquet* (Weinbauer, 2004; Danovaro et al., 2008), and so there are INRA, UMR CARRTEL, 75 Avenue de Corzent, 74203 little data on viruses that infect eukaryotic phytoplankton. Thonon-les-Bains cx, France. Indeed, there is a paucity of studies dealing with all aspects of algal virus ecology, including ‘species’ diversity and distribution, community dynamics and their role as mortal- Summary ity agents and conductors of biogeochemical cycling of Little is known about Phycodnavirus (or double- elements (Brussaard, 2004; Brussaard et al., 2008). stranded DNA algal virus) diversity in aquatic ecosys- Viruses infecting eukaryotic algal viruses are primarily tems, and virtually, no information has been provided double-stranded DNA (dsDNA) viruses. It has been sug- for European lakes. We therefore conducted a 1-year gested that they are a very diverse group (Suttle, 2005; survey of the surface waters of France’s two largest Dunigan et al., 2006; Bench et al., 2007), and research has lakes, Annecy and Bourget, which are characterized shown that they play a role in the control and regulation of by different trophic states and phytoplanktonic com- phytoplankton, typically for blooming species in marine munities. We found complementary and contrasting coastal waters (Bratbak et al., 1993; Jacquet et al., 2002; diversity of phycodnavirus in the lakes based on two Tomaru et al., 2008). genetic markers, the B family DNA polymerase- The Phycodnaviridae infect a variety of eukaryotic encoding gene (polB) and the major capsid pro- microalgae, including Chlorophyta, Dinophyta, Hapto- tein-encoding gene (mcp). These two core genes phyta and Heterokonta. They belong to the nucleo- have already been used, albeit separately, to infer cytoplasmic large DNA viruses, which are characterized by phylogenetic relationships and genetic diversity having a polyhedral capsid, no tail or envelope, and large among members of the phycodnavirus family and to dsDNA genomes ranging from 160 to 560 kb (Van Etten determine the occurrence and diversity of these genes and Meints, 1999; Van Etten et al., 2002; Iyer et al., 2006; in natural viral communities. While polB yielded Wilson et al., 2009). Currently, the Phycodnaviridae prasinovirus-like sequences, the mcp primers yielded consist of six genera named after the hosts they infect: sequences for prasinoviruses, chloroviruses, pry- Chlorovirus, Coccolithovirus, Prasinovirus, Prymne- mnesioviruses and other groups not known from avail- siovirus, Phaeovirus and Raphidovirus (Dunigan et al., able databases. There was no significant difference in 2006; Wilson et al., 2009). So far, the characterization of phycodnavirus populations between the two lakes phycodnaviruses has been limited to only a few individuals. when the sequences were pooled over the full year However, as mortality agents of eukaryotic algae and of investigation. By comparing Lakes Annecy and vehicles of gene transfer, we know that they play a crucial Bourget with data for other aquatic environments role in host community structuring, population succession, around the world, we show that these alpine lakes are resistance phenomena and the cycling of carbon in aquatic clearly distinct from both other freshwater ecosys- environments (Brussaard, 2004; Larsen et al., 2004; tems (lakes and rivers) and marine environments, sug- Suttle, 2005; Monier et al., 2008; Tomaru et al., 2008; gesting the influence of unique biogeographic factors. Thomas et al., 2012). Until now, the diversity of phycodnaviruses has been estimated using two molecular markers, the polB and mcp Introduction genes, which encode for DNA polymerase and their major Viruses are the most abundant biological entities in aquatic capsid protein respectively. Primers that target these ecosystems and exhibit the greatest genetic diversity of genes have already provided varying results regarding any group on Earth (Suttle, 2005; Angly et al., 2006). Most phycodnavirus occurrence and diversity (Schroeder et al., studies have focused on viruses that infect prokaryotes 2003; Short, 2012). Investigations using polB have revealed a very diverse and wide distribution of Received 5 February, 2013; revised 14 May, 2013; accepted 22 June, 2013. *For correspondence. E-mail [email protected]; phycodnaviruses in marine environments (Chen et al., Tel. (+33) 4 5026 7812; Fax (+33) 4 5026 0760. 1996; Short and Suttle, 2002; 2003; Bellec et al., 2009; © 2013 Society for Applied Microbiology and John Wiley & Sons Ltd 760 X. Zhong and S. Jacquet Park et al., 2011), rivers (Short and Short, 2008; Gimenes Chatfield Reservoir, Cuieiras River and Solimões River), et al., 2012) and lakes (Short and Short, 2008; Clasen and with only three sequences from Lake Bourget or Lake Suttle, 2009). In these studies, carried out in various Ontario, six from Lake 239 and two from Lake 240 (Fig. 2). marine and freshwater locations, all or almost all of the In Freshwater Cluster I, all of the sequences originated polB sequences obtained were closely related to from lakes. Freshwater Cluster III contained sequences prasinoviruses. While Larsen et al. (2008) developed uni- from both rivers and lakes. The Marine and Freshwater versal primers that target mcp, this marker has only been Cluster comprised all of the polB sequences recruited from used twice: once in Norwegian fjords (Larsen et al., 2008) GOS, and also sequences from both lakes and rivers. and once in the coastal waters of Korea (Park et al., 2011). These sequences were closely related to the marine MpV, These studies revealed that mcp may, in fact, be a useful OtV and OlV prasinovirus groups. The Marine BpV Cluster genetic marker for inferring phylogenetic relationships and contained sequences exclusively from marine environ- genetic diversity among members of the phycodnavirus ments and was closely related to the marine prasinovirus family in natural viral communities. BpV group. To the best of our knowledge, only a limited number of In total, 81.6% of polB sequences obtained from Lake freshwater lakes have, so far, been investigated for Annecy and Bourget belonged to Freshwater Cluster I, phycodnaviruses (Short, 2012). Studies have generally 17.2% to the Marine and Freshwater Cluster and only 1.2% focused on one ecosystem and used only one molecular to Freshwater Cluster II. No sequences belonged to the marker, typically polB. Our study is unique in that we use Freshwater Cluster III and Marine BpV Cluster (Fig. 2). An primers that target both mcp and polB and examine two examination of the colour ring in the phylogenetic tree large and deep lakes located in the same eco-area but shows that the distribution of sequences from either Lake characterized by different trophic states (oligotrophic vs. Annecy or Lake Bourget is clearly separated from the oligo-mesotrophic) and phytoplanktonic communities others (Fig. 2). A similar clustering pattern was observed (Jacquet et al., in press). By collecting samples every 3–4 for the majority of the sequences obtained. No clade was weeks, our investigation also provides new insights into privileged by sequences from either lake. Based on the phycodnavirus community structure and diversity in alpine pooled 1-year polB sequences, the Unifrac analysis lakes. revealed no significant differences between Lake Annecy and Lake Bourget (Fig. 3, P = 1). The polB sequences Results originating from marine environments seemed different from those obtained in freshwater, as revealed by the Diversity of phycodnaviruses as estimated from polB principal component analysis (PCA) (Fig. 3, P = 0). From the excised 48 visibly different bands, we obtained a total of 163 non-redundant sequences from 665 to 683 bp, Diversity of phycodnaviruses as estimated from mcp with nucleotide similarity ranging from 37.7% to 99.4%. The phylogenetic analysis of these sequences with From the excised 60 visibly different representative bands, phycodnavirus culture representatives showed that all of we obtained 115 non-redundant sequences for both lakes, the obtained polB sequences were grouped within marine varying from 362 to 527 bp, and with nucleotide similarity prasinoviruses and apart from other phycodnavirus groups varying between 29.5% and 98.5%. After phylogenetic (Fig. 1A). When we conducted the metaphylogene- analysis, the obtained sequences from Lake Annecy and tic analysis by introducing all prasinovirus-like polB Bourget were clustered into several phycodnavirus sequences from other published studies (Table 1) and from groups: Prymnesiovirus, Prasinovirus and Clusters the GOS (Global Ocean Survey) metagenome database, number 4, 6, 7 and 9 (Fig. 1B). In general, the clustering we discerned five clades (Fig. 2). Three of them were pattern matched the results of the metaphylogenetic analy- initially identified by Short and Short (2008): Freshwater sis when we included sequences observed in other envi- Cluster I, Freshwater Cluster II and Marine and Fresh- ronments (Table 1) and from the GOS and Antarctica- water Cluster [with Micromonas pusilla virus (MpV), Aquatic metagenome databases, while keeping both Ostreococcus tauri virus (OtV) and Ostreococcus maximum likelihood (ML) bootstrap and Bayesian infer- lucimarinus virus (OlV)]. The other two clades were Fresh- ence (BI) clade credibility values ≥ 50 (Fig. 4). Very differ- water Cluster III and
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