Viruses of a key coral symbiont exhibit temperature-driven productivity across a reefscape

Howe‐Kerr, Lauren I.; Grupstra, Carsten G. B.; Rabbitt, Kristen M.; Conetta, Dennis; Coy, Samantha R; Klinges, J. Grace; Maher, Rebecca L.; McConnell, Kaitlin; Meiling, Sonora S.; Messyasz, Adriana; Schmeltzer, Emily R.; Seabrook, Sarah; Sims, J.; Veglia, Alex; Thurber, Andrew R.; Thurber, Rebecca Vega; Correa, Adrienne M. S.

doi:10.21203/rs.3.rs-1899377/v1

Cited by 6 publications

(25 citation statements)

References 78 publications

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“…Targeted gene sequencing is increasingly being applied to explore spatiotemporal patterns of viral diversity (Adriaenssens & Cowan, 2014;Finke & Suttle, 2019;Frantzen & Holo, 2019;Gustavsen & Suttle, 2021;Howe-Kerr et al, 2022;Y. Li et al, 2018;Montalvo-Proaño et al, 2017;Prodinger et al, 2020;Short et al, 2010;Tong et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

“…Dinoflagellate-infecting RNA viruses (dinoRNAVs) are positive-sense, single-stranded RNA viruses hypothesized to infect the dinoflagellate symbionts (Family Symbiodiniaceae) that live in the tissues of reef-building stony corals (Correa et al, 2013;Veglia et al, 2022). Although dinoRNAVs can be prevalent in coral colonies Howe-Kerr et al, 2022;Montalvo-Proaño et al, 2017;Veglia et al, 2022), it is unclear how dinoRNAVs (or Symbiodiniaceae infected by dinoRNAVs) are transmitted among colonies. Recent work has shown that corallivorous (coral-eating) fishes disperse 100s of millions of live Symbiodiniaceae cells across reefscapes in their feces each day (Grupstra et al, 2021).…”

Section: Rna Virus Study Descriptionmentioning

confidence: 99%

“…To assess the extent to which corallivorous fish feces disperse dinoRNAVs in their feces (as in , we characterized the presence and diversity of dinoRNAVs in various environmental reservoirs using amplicon sequencing of the dinoRNAV major capsid protein (mcp ) gene. Given that dinoRNAV communities can vary across coral species and colonies Howe-Kerr, 2022;Montalvo-Proaño et al, 2017) and that corallivorous fish actively 'sample' corals while feeding (Grupstra et al, 2021), we hypothesized that corallivorous fish feces are a reservoir of dinoRNAVs and that fish feces-associated dinoRNAV communities exhibit higher alpha diversity than coral colony-associated dinoRNAV communities. We generated 19 dinoR-NAV mcp amplicon sequencing libraries from coral colony biopsies (Acroporahyacinthus , n=8; Pocillopora species complex, n=5), as well as the feces of corallivorous fishes (Chaetodon reticulatus , n=4; Chaetodon ornatissimus, n=2).…”

Section: Rna Virus Study Descriptionmentioning

confidence: 99%

“…All samples were collected from reefs off the north shore of Moorea, French Polynesia (South Pacific). Methods for sampling and sample processing to generate virus amplicon sequencing libraries are described in Grupstra et al (2021 and Howe-Kerr et al (2022). DinoRNAV mcp amplicon libraries were processed and analyzed using vAMPirus (see doi.org/10.5281/zenodo.7574173).…”

Section: Rna Virus Study Descriptionmentioning

confidence: 99%

“…Amplicon sequencing is a targeted, polymerase chain reaction (PCR)-based HTS approach that allows deep characterization of genetic variants within virus populations (Short et al 2010). The targeted nature of amplicon sequencing reduces the economic and computational investment required for spatiotemporal investigations of virus communities at ecologically relevant scales (see Finke & Suttle, 2019;Frantzen & Holo, 2019;Gustavsen & Suttle, 2021;Howe-Kerr et al, 2022;Montalvo-Proaño et al, 2017). The number of studies leveraging virus amplicon sequencing has increased rapidly over the last two decades (e.g., 16 peer-reviewed publications in 1998 compared to 127 in 2021 based on a Web of Science search of 'virus amplicon sequencing', November 2022).…”

Section: Introductionmentioning

confidence: 99%

See 4 more Smart Citations

vAMPirus: A versatile amplicon processing and analysis program for studying viruses

Veglia

Rivera‐Vicéns

Grupstra

et al. 2023

Preprint

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Amplicon sequencing is an effective and increasingly applied method for studying viral communities in the environment. Here, we present vAMPirus, a user-friendly, comprehensive, and versatile DNA and RNA virus amplicon sequence analysis program, designed to support investigators in exploring virus amplicon sequencing data and running informed, reproducible analyses. vAMPirus intakes raw virus amplicon libraries and, by default, performs nucleotide- and protein-based analyses to produce results such as sequence abundance information, taxonomic classifications, phylogenies, and community diversity metrics. The vAMPirus pipelines additionally include optional approaches that can increase the biological signal-to-noise ratio in results by leveraging tools not yet commonly applied to virus amplicon data analyses. In this paper, we validate the vAMPirus analytical framework and illustrate its implementation into the general virus amplicon sequencing workflow by recapitulating findings from two previously published double-stranded DNA virus datasets. As a case study, we also apply the program to explore the diversity and distribution of a coral reef-associated RNA virus. vAMPirus is incorporated with the Nextflow workflow manager, offering straightforward scalability, standardization, and communication of virus lineage-specific analyses. The vAMPirus framework itself is also designed to be adaptable; community-driven analytical standards will continue to be incorporated as the field advances. vAMPirus supports researchers in revealing patterns of virus diversity and population dynamics in nature, while promoting study reproducibility and comparability.

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Section: Discussionmentioning

confidence: 99%

Section: Rna Virus Study Descriptionmentioning

confidence: 99%

Section: Rna Virus Study Descriptionmentioning

confidence: 99%

Section: Rna Virus Study Descriptionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

vAMPirus: A versatile amplicon processing and analysis program for studying viruses

Veglia

Rivera‐Vicéns

Grupstra

et al. 2023

Preprint

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Filamentous virus-like particles are present in coral dinoflagellates across genera and ocean basins

Howe-Kerr,

Knochel,

Meyer

et al. 2023

The ISME Journal

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Filamentous viruses are hypothesized to play a role in stony coral tissue loss disease (SCTLD) through infection of the endosymbiotic dinoflagellates (Family Symbiodiniaceae) of corals. To evaluate this hypothesis, it is critical to understand the global distribution of filamentous virus infections across the genetic diversity of Symbiodiniaceae hosts. Using transmission electron microscopy, we demonstrate that filamentous virus-like particles (VLPs) are present in over 60% of Symbiodiniaceae cells (genus Cladocopium) within Pacific corals (Acropora hyacinthus, Porites c.f. lobata); these VLPs are more prevalent in Symbiodiniaceae of in situ colonies experiencing heat stress. Symbiodiniaceae expelled from A. hyacinthus also contain filamentous VLPs, and these cells are more degraded than their in hospite counterparts. Similar to VLPs reported from SCTLD-affected Caribbean reefs, VLPs range from ~150 to 1500 nm in length and 16–37 nm in diameter and appear to constitute various stages in a replication cycle. Finally, we demonstrate that SCTLD-affected corals containing filamentous VLPs are dominated by diverse Symbiodiniaceae lineages from the genera Breviolum, Cladocopium, and Durusdinium. Although this study cannot definitively confirm or refute the role of filamentous VLPs in SCTLD, it demonstrates that filamentous VLPs are not solely observed in SCTLD-affected corals or reef regions, nor are they solely associated with corals dominated by members of a particular Symbiodiniaceae genus. We hypothesize that filamentous viruses are a widespread, common group that infects Symbiodiniaceae. Genomic characterization of these viruses and empirical tests of the impacts of filamentous virus infection on Symbiodiniaceae and coral colonies should be prioritized.

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Widespread occurrence and diverse origins of polintoviruses influence lineage-specific genome dynamics in stony corals

Stephens,

Faghihi,

Moniruzzaman

2024

Virus Evolution

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Stony corals (Order Scleractinia) are central to vital marine habitats known as coral reefs. Numerous stressors in the Anthropocene are contributing to the ongoing decline in coral reef health and coverage. While viruses are established modulators of marine microbial dynamics, their interactions within the coral holobiont and impact on coral health and physiology remain unclear. To address this key knowledge gap, we investigated diverse stony coral genomes for ‘endogenous’ viruses. Our study uncovered a remarkable number of integrated viral elements recognized as ‘Polintoviruses’ (Class Polintoviricetes) in 30 Scleractinia genomes; with several species harboring hundreds to thousands of polintoviruses. We reveal massive paralogous expansion of polintoviruses in stony coral genomes, alongside presence of integrated elements closely related to Polinton-like viruses (PLVs), a group of viruses that exist as free virions. These results suggest multiple integrations of polintoviruses and PLV-relatives, along with paralogous expansions, shaped stony coral genomes. Re-analysis of existing gene expression data reveals all polintovirus structural and non-structural hallmark genes are expressed, providing support for free virion production from polintoviruses. Our results, revealing a significant diversity of polintovirus across the Scleractinia order, open a new research avenue into polintovirus and their possible roles in disease, genomic plasticity, and environmental adaptation in this key group of organisms.

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Viruses of a key coral symbiont exhibit temperature-driven productivity across a reefscape

Cited by 6 publications

References 78 publications

vAMPirus: A versatile amplicon processing and analysis program for studying viruses

vAMPirus: A versatile amplicon processing and analysis program for studying viruses

Filamentous virus-like particles are present in coral dinoflagellates across genera and ocean basins

Widespread occurrence and diverse origins of polintoviruses influence lineage-specific genome dynamics in stony corals

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