Novel ssDNA Viruses Detected in the Virome of Bleached, Habitat-Forming Kelp Ecklonia radiata

Beattie, Douglas T.; Lachnit, Tim; Dinsdale, Elizabeth A.; Thomas, Torsten; Steinberg, Peter D.

doi:10.3389/fmars.2017.00441

Cited by 21 publications

(15 citation statements)

References 85 publications

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“…For instance, an increase in herpes‐like viruses was reported in the coral P. compressa at elevated temperature (Vega Thurber et al ., ) and an increased frequency of algal phycodnaviruses was reported from both bleached corals (Vega Thurber et al ., ) and thermally stressed Symbiodinium cultures (Correa et al ., ; Lawrence et al ., ; Weynberg et al ., ). A shift in the viral community of the kelp Ecklonia radiata also occurs during thermal stress, including an increase in eukaryote‐infecting ssDNA viruses (Beattie et al ., ). Elevated sea temperatures increase the mortality rate of oysters infected by Herpesviruses (Petton et al ., ), and the prevalence of Densoviruses increases in sea stars affected by wasting disease under both elevated and depressed temperatures (Hewson et al ., ; Eisenlord et al ., ; Kohl et al ., ; Menge et al ., )…”

Section: Introductionmentioning

confidence: 97%

Thermal stress modifies the marine sponge virome

Laffy

Botté

Wood‐Charlson

et al. 2019

Environ Microbiol Rep

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Summary Marine sponges can form stable partnerships with a wide diversity of microbes and viruses, and this high intraspecies symbiont specificity makes them ideal models for exploring how host‐associated viromes respond to changing environmental conditions. Here we exposed the abundant Great Barrier Reef sponge Rhopaloiedes odorabile to elevated seawater temperature for 48 h and utilised a metaviromic approach to assess the response of the associated viral community. An increase in endogenous retro‐transcribing viruses within the Caulimorviridae and Retroviridae families was detected within the first 12 h of exposure to 32 °C, and a 30‐fold increase in retro‐transcribing viruses was evident after 48 h at 32 °C. Thermally stressed sponges also exhibited a complete loss of ssDNA viruses which were prevalent in field samples and sponges from the control temperature treatment. Despite these viromic changes, functional analysis failed to detect any loss or gain of auxiliary metabolic genes, indicating that viral communities are not providing a direct competitive advantage to their host under thermal stress. In contrast, endogenous sponge retro‐transcribing viruses appear to be replicating under thermal stress, and consistent with retroviral infections in other organisms, may be contributing to the previously described rapid decline in host health evident at elevated temperature.

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Section: Introductionmentioning

confidence: 97%

Thermal stress modifies the marine sponge virome

Laffy

Botté

Wood‐Charlson

et al. 2019

Environ Microbiol Rep

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“…Infection prevalence increased towards higher latitudes in both Chile and Australia, which could be due to increased population density in southern parts of Durvillaea's range, or it could be that the Maullinia pathogen is more prevalent in colder waters (Blake et al 2017), which may mean that increased temperatures could counteract the virulence of this pathogen (Blake et al 2017). However this could be offset by physiological stresses caused by higher temperatures increasing organisms' susceptibility to disease (Case et al 2011;Campbell et al 2011;Beattie et al 2018;Thomsen et al 2019). Predicting how environmental change will affect the prevalence and impacts of Maullinia on Durvillaea is, therefore, currently difficult.…”

Section: Resultsmentioning

confidence: 99%

Pathogen inferred to have dispersed thousands of kilometres at sea, infecting multiple keystone kelp species

2021

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Protistan pathogens have been found to infect populations of some large brown macroalgae. Infection could reduce the ability of macroalgae to withstand hydrodynamic pressures through weakening tissues and reducing flexibility. Widespread mortality of macroalgae if disease outbreaks were to occur could have important flow-on consequences for biodiversity and ecosystem function. Recent discoveries of the protistan pathogen Maullinia infecting the ecologically keystone southern bull kelp Durvillaea in Chile, Australia, and on Marion Island, raise the possibility that this pathogen is dispersing across ocean basins with buoyant hosts. To determine whether Maullinia also infects southern bull kelp in New Zealand, samples of gall-like tissue from Durvillaea antarctica, D. poha, and D. willana were collected from intertidal sites, and genetic analyses (sequencing of partial 18S rRNA) carried out. Maullinia infections were detected in all three species of Durvillaea. Phylogenetic analyses show a close relationship of New Zealand Maullinia to M. braseltonii previously detected in Chile and on Marion Island. Based on its genetic similarity to distant lineages and its presence on buoyant hosts that have been shown to drift long distances at seas, we infer that Maullinia has dispersed across the Southern Ocean through rafting of infected bull kelp. Understanding the capacity of pathogens to disperse across oceans is critical part of forecasting and managing ecosystem responses to environmental change.

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“…Several previous metagenomic studies have identified many novel genomes similar to ssDNA circular viruses through data-mining of public marine metagenomes [79,80], but with no hints about their putative hosts. Previously described CRESS viral hosts range from plants [81] (Geminiviridae, Nanoviridae), bleached kelp macroalgae [82], vertebrates [83] (Circoviridae), fungi, insects (Genomoviridae) [84] and crustaceans [85]. In protists, CRESS viruses were discovered in SAGs targeting Picobiliphytes [31] and in Bacillariophyceae diatoms, where they have been isolated and their lytic effect could be demonstrated [86].…”

Section: Discussionmentioning

confidence: 99%

Single cell ecogenomics reveals mating types of individual cells and ssDNA viral infections in the smallest photosynthetic eukaryotes

Benites

Poulton

Labadie

et al. 2019

Phil. Trans. R. Soc. B

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Planktonic photosynthetic organisms of the class Mamiellophyceae include the smallest eukaryotes (less than 2 µm), are globally distributed and form the basis of coastal marine ecosystems. Eight complete fully annotated 13–22 Mb genomes from three genera, Ostreococcus , Bathycoccus and Micromonas , are available from previously isolated clonal cultured strains and provide an ideal resource to explore the scope and challenges of analysing single cell amplified genomes (SAGs) isolated from a natural environment. We assembled data from 12 SAGs sampled during the Tara Oceans expedition to gain biological insights about their in situ ecology, which might be lost by isolation and strain culture. Although the assembled nuclear genomes were incomplete, they were large enough to infer the mating types of four Ostreococcus SAGs. The systematic occurrence of sequences from the mitochondria and chloroplast, representing less than 3% of the total cell's DNA, intimates that SAGs provide suitable substrates for detection of non-target sequences, such as those of virions. Analysis of the non-Mamiellophyceae assemblies, following filtering out cross-contaminations during the sequencing process, revealed two novel 1.6 and 1.8 kb circular DNA viruses, and the presence of specific Bacterial and Oomycete sequences suggests that these organisms might co-occur with the Mamiellales. This article is part of a discussion meeting issue ‘Single cell ecology’.

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Novel ssDNA Viruses Detected in the Virome of Bleached, Habitat-Forming Kelp Ecklonia radiata

Cited by 21 publications

References 85 publications

Thermal stress modifies the marine sponge virome

Thermal stress modifies the marine sponge virome

Pathogen inferred to have dispersed thousands of kilometres at sea, infecting multiple keystone kelp species

Single cell ecogenomics reveals mating types of individual cells and ssDNA viral infections in the smallest photosynthetic eukaryotes

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