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Metagenomic Characterisation of Viral Communities in Corals: Mining Biological Signal from Methodological Noise1

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Metagenomic Characterisation of Viral Communities in Corals: Mining Biological Signal from Methodological Noise1 Metagenomic characterisation of viral communities in corals: Mining biological signal from methodological noise1 Running title: Methodological biases in coral viromics Elisha M. Wood-Charlson1,4,5, Karen D. Weynberg1, Curtis A. Suttle2, Simon Roux3,5, Madeleine J. H. van Oppen1 1 Australian Institute of Marine Science, Townsville, QLD, Australia 2 Departments of Earth, Ocean & Atmospheric Sciences, Microbiology & Immunology, Botany and the Canadian Institute for Advanced Research, University of British Columbia, Vancouver, British Columbia, Canada 3 LaboratoireArticle Micro-organismes: Genome and Environment, Université Blaise Pascal, Clermont Université, France 4 Correspondence: Elisha M. Wood-Charlson Australian Institute of Marine Science PMB 3 Townsville MC Townsville, QLD 4810, Australia E-mail: [email protected] 5 Current affiliations: Wood-Charlson, Center for Microbial Oceanography: Research and Education, University of Hawai’i at Manoa, Honolulu, HI, USA; Roux, Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, USA This article has been accepted for publication and undergone full peer review but has not been through the copyediting,Accepted typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/1462-2920.12803 1 This article is protected by copyright. All rights reserved. Summary Reef-building corals form close associations with organisms from all three domains of life and therefore have many potential viral hosts. Yet, knowledge of viral communities associated with corals is barely explored. This complexity presents a number of challenges in terms of the metagenomic assessments of coral viral communities, and requires specialised methods for purification and amplification of viral nucleic acids, as well as virome annotation. In this mini-review, we conduct a meta-analysis of the limited number of existing coral virome studies, as well as available coral transcriptome and metagenome data, to identify trends and potential complications inherent in different methods. The Article analysis shows that the method used for viral nucleic acid isolation drastically affects the observed viral assemblage and interpretation of the results. Further, the small number of viral reference genomes available, coupled with short sequence read lengths might cause errors in virus identification. Despite these limitations and potential biases, the data show that viral communities associated with corals are diverse, with double- and single-stranded DNA and RNA viruses. The identified viruses are dominated by dsDNA-tailed bacteriophages, but there are also viruses that infect eukaryote hosts, likely the endosymbiotic dinoflagellates, Symbiodinium spp., host coral, and other eukaryotes in close association. Keywords: coral, Symbiodinium, metagenome, virome, virus, methodological biases Accepted 2 This article is protected by copyright. All rights reserved. Introduction Scleractinian (stony) corals deposit calcium carbonate during colony growth and build the three-dimensional structures that constitute coral reefs. This structural framework provides important habitat for a wide taxonomic diversity of macroscopic and microscopic reef organisms. The coral itself hosts a collective of organisms, referred to as the coral holobiont, that spans the three domains of life, as well as the viruses that infect them. Of all the components in the coral holobiont, viruses are the least studied. Transmission electron microscopy (TEM) was used in earlier publications to describe virus-like particles (VLPs) in corals (Wilson et al., 2001; 2005; Davy and Patten, 2006; Patten et al., 2008). With the development of next-generation sequencing, a metagenomics approach to viral community Article characterisation is now also available (Edwards and Rohwer, 2005; Kristensen et al., 2010; Rosario and Breitbart, 2011). However, there are inherent challenges to the purification of viruses and viral genomes. The small size of virus particles and their genomes, combined with losses during purification typically results in low amounts of nucleic acids, on which whole genome amplification (WGA) is often used to obtain enough material for sequencing; this can introduce quantitative biases in the data (Angly et al., 2006; Duhaime et al., 2012). Moreover, the diverse genome chemistry of viruses (single stranded (ss)RNA, double stranded (ds)RNA, ssDNA, or dsDNA) complicates nucleic acid isolation from mixed communities (Andrews-Pfannkoch et al., 2010; Weynberg et al., 2014). Viral metagenomes prepared from coral tissues require careful post-sequencing processing. Most marine viruses lack representation in sequence databases, with coral-associated viruses being particularly scant. While there have been some phage therapy trials for bacteriaAccepted associated with coral disease (Atad et al., 2012; Cohen et al., 2013), cultured 3 This article is protected by copyright. All rights reserved. viruses associated with a healthy coral holobiont have not been reported. The paucity of representative viral sequences in databases results in many unidentified sequences in marine viral metagenomes (Breitbart et al., 2002; Angly et al., 2006; Wegley et al., 2007; Dinsdale et al., 2008; Vega Thurber et al., 2008; Williamson et al., 2008; Correa et al., 2013). Further, sequences with similarity to cellular genes are often present in viral metagenomes (Roux et al., 2013a), which may be the result of host contamination, horizontal gene transfer (HGT) between viruses and their hosts, or gene transfer agents (GTAs) (Canchaya et al., 2003; Monier et al., 2009; Liu et al., 2011; Lang et al., 2012; Roux et al., 2013a). All of these factors are likely important in the coral holobiont, given its wide diversity of organisms that live in close association. Article In spite of these caveats, holobiont metagenome and transcriptome sequence data can provide qualitative information about viruses associated with various members of the coral holobiont. Regardless of whether the focus of these studies is the coral host tissue, the algal symbiont, or the prokaryotes, it is difficult to separate the host organisms from the associated viral community. Therefore, raw sequence data from non-viral fractions will likely contain viral sequences. In this contribution, publically available coral transcriptomes, as well as prokaryote and viral metagenomes isolated from corals, were interrogated for viral sequences and analysed comparatively. The data sets Coral, prokaryotic, and viral metagenome and meta-transcriptome data sets were downloaded from publically available sequence archives and uploaded to Metavir (Roux et al., 2011),Accepted an online tool for analysing viral genomic data. Sequences from 11 coral species 4 This article is protected by copyright. All rights reserved. (Supplementary Table 1) were added to Metavir as “Coral-associated viruses” for this study. In this analysis, we also included “P. compressa” (Vega Thurber et al., 2008), “Coral Atoll” (Dinsdale et al., 2008), and several data sets from the “Coral virus – generating metagenomes” (Weynberg et al., 2014; Supplementary Table 1). Metagenomes were analysed using Metavir’s BLAST-based comparison (e-value ≤ 10-5) to the 2014-09-10 NCBI viral refseq database and normalized to genome length using the built-in Genome-relative Abundance and Average Size (GAAS) normalization tool (Angly et al., 2009). Metavir assigns taxonomy to a viral sequence using this BLAST-based comparison to sequences that are annotated in the NCBI viral refseq database. Article Methodological biases: Purification and amplification techniques select for certain viral groups Coral-associated data sets were screened for the presence of viruses identified to a viral family, where possible (Table 1). All data sets contained dsDNA viruses, but were variable for ssDNA, dsRNA, ssRNA, and retrotranscribing (RT) viral families, depending on the holobiont fraction targeted for sequencing. Coral transcriptomes (Supplementary Table 1) were generated from extracted holobiont RNA, and they produced viral assemblages dominated by RNA viruses (36-78%). While this may be expected, since transcriptomes target RNA sequences (Supplementary Table 2), it is possible that they may also contain DNA viruses, if the sample was undergoing an active DNA virus replication event. RNA viral assemblages from coral transcriptomes contained ssRNA viruses (1-13% of identified virus), a dsRNA virus (2-31%), and ssRNA and dsDNA RT viruses (29-71%). Prokaryote metagenomes (Supplementary Table 1) targeted the prokaryotic community through Percoll fractionationAccepted (Supplementary Table 2) to remove coral host and Symbiodinium cells. The 5 This article is protected by copyright. All rights reserved. prokaryote-containing fractions were extracted for DNA and amplified through a Phi29 DNA polymerase-based rolling circle WGA method to obtain enough material for sequencing (Littman et al., 2011; Wegley et al., 2007). The resulting viral assemblages were surprisingly depleted for dsDNA viruses (2-8% of identified viruses), and had a notably larger representation of ssDNA viruses (31-96%). In fact, the Porites astreoides prokaryotic data set (Wegley et al., 2007) was dominated by hits to a single ssDNA virus, an unclassified Dragonfly-associated microphage (48%). With almost half of the viral assemblage from this prokaryotic metagenome annotating to a single ssDNA virus, it is
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