Increases and decreases in marine disease reports in an era of global change

Tracy, Allison M.; Pielmeier, Madeline L.; Yoshioka, Reyn; Heron, Scott F.; Harvell, C. Drew

doi:10.1098/rspb.2019.1718

Cited by 76 publications

(61 citation statements)

References 46 publications

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“…The temporal rapidity and geographic heterogeneity of the 2013 sea star wasting disease outbreak made it difficult to narrow down the range of factors, causes, and mechanisms involved at the time. Similar to other multitaxon pandemics (e.g., “white nose” syndrome in bats, chytrid fungi for amphibians, morbillivirus in dolphins) SSWD was elusive in the early stages of study (Hewson et al, 2018; Miner et al, 2018), which is a concern as mass mortalities are increasing in frequency with global change in some taxa (Fey et al, 2015; Tracy, Pielmeier, Yoshioka, Heron, & Harvell, 2019) and require more rapid assessment. Given the central role of asteroid predators in community ecology (Gravem & Morgan, 2017; Menge, 1983; Paine, 1974), as the focal organisms in the 2013 wasting pandemic, and wasting's intermittent recurrence (albeit with different intensity and taxonomic breadth) we desperately need to better understand risk factors.…”

Section: Discussionmentioning

confidence: 99%

An initial comparative genomic autopsy of wasting disease in sea stars

et al. 2020

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Beginning in 2013, sea stars throughout the Eastern North Pacific were decimated by wasting disease, also known as “asteroid idiopathic wasting syndrome” (AIWS) due to its elusive aetiology. The geographic extent and taxonomic scale of AIWS meant events leading up to the outbreak were heterogeneous, multifaceted, and oftentimes unobserved; progression from morbidity to death was rapid, leaving few tell‐tale symptoms. Here, we take a forensic genomic approach to discover candidate genes that may help explain sea star wasting syndrome. We report the first genome and annotation for Pisaster ochraceus, along with differential gene expression (DGE) analyses in four size classes, three tissue types, and in symptomatic and asymptomatic individuals. We integrate nucleotide polymorphisms associated with survivors of the wasting disease outbreak, DGE associated with temperature treatments in P. ochraceus, and DGE associated with wasting in another asteroid Pycnopodia helianthoides. In P. ochraceus, we found DGE across all tissues, among size classes, and between asymptomatic and symptomatic individuals; the strongest wasting‐associated DGE signal was in pyloric caecum. We also found previously identified outlier loci co‐occur with differentially expressed genes. In cross‐species comparisons of symptomatic and asymptomatic individuals, consistent responses distinguish genes associated with invertebrate innate immunity and chemical defence, consistent with context‐dependent stress responses, defensive apoptosis, and tissue degradation. Our analyses thus highlight genomic constituents that may link suspected environmental drivers (elevated temperature) with intrinsic differences among individuals (age/size, alleles associated with susceptibility) that elicit organismal responses (e.g., coelomocyte proliferation) and manifest as sea star wasting mass mortality.

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Section: Discussionmentioning

confidence: 99%

An initial comparative genomic autopsy of wasting disease in sea stars

et al. 2020

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“…This has resulted in them being classed as threatened (US Endangered Species Act; ESA), and critically endangered (IUCN). The primary cause of this decline is disease [2][3][4] and this is particularly worrying for these species as climate change and anthropogenic stressors are now being implicated in increasing disease prevalence, frequency, and severity [5][6][7][8][9][10]. While these two species are now being heavily used in restoration activities in the Caribbean, their disease susceptibility requires a more thorough understanding of the disease dynamics within the remnant populations.…”

Section: Introductionmentioning

confidence: 99%

Innate immune gene expression in Acropora palmata is consistent despite variance in yearly disease events

et al. 2020

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Coral disease outbreaks are expected to increase in prevalence, frequency and severity due to climate change and other anthropogenic stressors. This is especially worrying for the Caribbean branching coral Acropora palmata which has already seen an 80% decrease in cover primarily due to disease. Despite the importance of this keystone species, there has yet to be a characterization of its transcriptomic response to disease exposure. In this study we provide the first transcriptomic analysis of 12 A. palmata genotypes and their symbiont Symbiodiniaceae exposed to disease in 2016 and 2017. Year was the primary driver of gene expression variance for A. palmata and the Symbiodiniaceae. We hypothesize that lower expression of ribosomal genes in the coral, and higher expression of transmembrane ion transport genes in the Symbiodiniaceae indicate that a compensation or dysbiosis may be occurring between host and symbiont. Disease response was the second driver of gene expression variance for A. palmata and included a core set of 422 genes that were significantly differentially expressed. Of these, 2 genes (a predicted cyclin-dependent kinase 11b and aspartate 1-decarboxylase) showed negative Log2 fold changes in corals showing transmission of disease, and positive Log2 fold changes in corals showing no transmission of disease, indicating that these may be important in disease resistance. Co-expression analysis identified two modules positively correlated to disease exposure, one enriched for lipid biosynthesis genes, and the other enriched in innate immune genes. The hub gene in the immune module was identified as D-amino acid oxidase, a gene implicated in phagocytosis and microbiome homeostasis. The role of D-amino acid oxidase in coral immunity has not been characterized but could be an important enzyme for responding to disease. Our results indicate that A. palmata mounts a core immune response to disease exposure despite differences in the disease type and virulence between 2016 and 2017. These identified genes may be important for future biomarker development in this Caribbean keystone species.

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“…Samples from these genotypes clustered with the year they were exposed to disease, indicating that genotype susceptibility was probably not the cause for the differences in disease prevalence (Fig 2, A). Our results indicate that other factors such as disease type, disease virulence, and the base health of the coral could be potential factors that led to the higher incidence of observed diseases in 2017 [10,26,47]. Additionally, we identified that the A. palmata genes driving the difference between 2016 and 2017 were putative coral ribosomal proteins (Fig 3A, Supp 1).…”

Section: Discussionmentioning

confidence: 78%

“…This has been especially notable for Acropora palmata and Acropora cervicornis , which have seen an 80% reduction throughout their geographic range [2] resulting in them being classed threatened (US Endangered Species Act; ESA), and critically endangered (IUCN). The primary driver of this decline is disease [2–4] and this is particularly worrying for these species as climate change and anthropogenic stressors are now being implicated in increasing disease prevalence, frequency, and severity [5–10]. These two species are being heavily focused on for restoration activities in the Caribbean, but are historically susceptible to disease, thus it is imperative we understand the disease dynamics within the remnant populations.…”

Section: Introductionmentioning

confidence: 99%

Innate immune gene expression inAcropora palmatais consistent despite variance in yearly disease events

Young

Serrano

Rosales

et al. 2020

Preprint

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Coral disease outbreaks are expected to increase in prevalence, frequency and severity due to climate change and other anthropogenic stressors. This is especially worrying for the Caribbean branching Acropora palmata which has already seen an 80% decrease in its coral cover, with this primarily due to disease. Despite the importance of this species, there has yet to be a characterization of its transcriptomic response to disease exposure. In this study we provide the first transcriptomic analysis of 12 A. palmata genotypes, and their symbiont Symbiodiniaceae, exposed to disease in 2016 and 2017. Year was the primary driver of sample variance for A. palmata and the Symbiodiniaceae. Lower expression of ribosomal genes in the coral, and higher expression of transmembrane ion transport genes in the Symbiodiniaceae indicate that the increased virulence in 2017 may have been due to a dysbiosis between the coral and Symbiodiniaceae. We also identified a conserved suite of innate immune genes responding to the disease challenge that was activated in both years. This included genes from the Toll-like receptor and lectin pathways, and antimicrobial peptides. Co-expression analysis identified a module positively correlated to disease exposure rich in innate immune genes, with D-amino acid oxidase, a gene implicated in phagocytosis and microbiome homeostasis, as the hub gene. The role of D-amino acid oxidase in coral immunity has not been characterized but holds potential as an important enzyme for responding to disease. Our results indicate that A. palmata mounts a similar immune response to disease exposure as other coral species previously studied, but with unique features that may be critical to the survival of this keystone Caribbean species.

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Increases and decreases in marine disease reports in an era of global change

Cited by 76 publications

References 46 publications

An initial comparative genomic autopsy of wasting disease in sea stars

An initial comparative genomic autopsy of wasting disease in sea stars

Innate immune gene expression in Acropora palmata is consistent despite variance in yearly disease events

Innate immune gene expression inAcropora palmatais consistent despite variance in yearly disease events

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