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The harmful algae, Cochlodinium polykrikoides and Aureococcus anophagefferens, elicit stronger transcriptomic and mortality response in larval bivalves (Argopecten irradians) than climate change stressors.

ABSTRACT: Global ocean change threatens marine life, yet a mechanistic understanding of how organisms are affected by specific stressors is poorly understood. Here, we identify and compare the unique and common transcriptomic responses of an organism experiencing widespread fisheries declines, Argopecten irradians (bay scallop) exposed to multiple stressors including high pCO2, elevated temperature, and two species of harmful algae, Cochlodinium (aka Margalefidinium) polykrikoides and Aureococcus anophagefferens using high-throughput sequencing (RNA-seq). After 48 hr of exposure, scallop transcriptomes revealed distinct expression profiles with larvae exposed to harmful algae (C. polykrikoides and A. anophagefferens) displaying broader responses in terms of significantly and differentially expressed (DE) transcripts (44,922 and 4,973; respectively) than larvae exposed to low pH or elevated temperature (559 and 467; respectively). Patterns of expression between larvae exposed to each harmful algal treatment were, however, strikingly different with larvae exposed to A. anophagefferens displaying large, significant declines in the expression of transcripts (n = 3,615; 87% of DE transcripts) whereas exposure to C. polykrikoides increased the abundance of transcripts, more than all other treatments combined (n = 43,668; 97% of DE transcripts). Larvae exposed to each stressor up-regulated a common set of 21 genes associated with protein synthesis, cellular metabolism, shell growth, and membrane transport. Larvae exposed to C. polykrikoides displayed large increases in antioxidant-associated transcripts, whereas acidification-exposed larvae increased abundance of transcripts associated with shell formation. After 10 days of exposure, each harmful algae caused declines in survival that were significantly greater than all other treatments. Collectively, this study reveals the common and unique transcriptional responses of bivalve larvae to stressors that promote population declines within coastal zones, providing insight into the means by which they promote mortality as well as traits possessed by bay scallops that enable potential resistance.

SUBMITTER: Griffith AW

PROVIDER: S-EPMC6476759 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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The harmful algae, Cochlodinium polykrikoides and Aureococcus anophagefferens, elicit stronger transcriptomic and mortality response in larval bivalves (Argopecten irradians) than climate change stressors.

Griffith Andrew W AW Harke Matthew J MJ DePasquale Elizabeth E Berry Dianna L DL Gobler Christopher J CJ

Ecology and evolution 20190405 8

Global ocean change threatens marine life, yet a mechanistic understanding of how organisms are affected by specific stressors is poorly understood. Here, we identify and compare the unique and common transcriptomic responses of an organism experiencing widespread fisheries declines, Argopecten irradians (bay scallop) exposed to multiple stressors including high pCO2, elevated temperature, and two species of harmful algae, Cochlodinium (aka Margalefidinium) ...[more]

PMID: 31031955

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Project description:While viruses with distinct phylogenetic origins and different nucleic acid types can infect and lyse eukaryotic phytoplankton, "giant" dsDNA viruses have been found to be associated with important ecological processes, including the collapse of algal blooms. However, the molecular aspects of giant virus-host interactions remain largely unknown. Aureococcus anophagefferens virus (AaV), a giant virus in the Mimiviridae clade, is known to play a critical role in regulating the fate of brown tide blooms caused by the pelagophyte Aureococcus anophagefferens. To understand the physiological response of A. anophagefferens CCMP1984 upon AaV infection, we studied the transcriptomic landscape of this host-virus pair over an entire infection cycle using a RNA-sequencing approach. A massive transcriptional response of the host was evident as early as 5 min post-infection, with modulation of specific processes likely related to both host defense mechanism(s) and viral takeover of the cell. Infected Aureococcus showed a relative suppression of host-cell transcripts associated with photosynthesis, cytoskeleton formation, fatty acid, and carbohydrate biosynthesis. In contrast, host cell processes related to protein synthesis, polyamine biosynthesis, cellular respiration, transcription, and RNA processing were overrepresented compared to the healthy cultures at different stages of the infection cycle. A large number of redox active host-selenoproteins were overexpressed, which suggested that viral replication and assembly progresses in a highly oxidative environment. The majority (99.2%) of annotated AaV genes were expressed at some point during the infection cycle and demonstrated a clear temporal-expression pattern and an increasing relative expression for the majority of the genes through the time course. We detected a putative early promoter motif for AaV, which was highly similar to the early promoter elements of two other Mimiviridae members, indicating some degree of evolutionary conservation of gene regulation within this clade. This large-scale transcriptome study provides insights into the Aureococcus cells infected by a giant virus and establishes a foundation to test hypotheses regarding metabolic and regulatory processes critical for AaV and other Mimiviridae members.

Project description:Harmful algal blooms (HABs) caused by the dinoflagellate Cochlodinium polykrikoides lead to severe environmental impacts in oceans worldwide followed by huge economic losses. Algicide agent copper sulfate (CuSO4) is regard as an economical and effective agent for HABs mitigation; its biochemical and physiological effects were revealed in C. polykrikoides. However, molecular mechanisms of CuSO4 effect on the C. polykrikoides, even other HAB species, have not been investigated. The present study investigated the transcriptional response of C. polykrikoides against CuSO4 treatments, with the aim of providing certain molecular mechanism of CuSO4 effect on the C. polykrikoides blooms.RNA-seq generated 173 million reads, which were further assembled to 191,212 contigs. 43.3 %, 33.9 %, and 15.6 % of contigs were annotated with NCBI NR, GO, and KEGG database, respectively. Transcriptomic analysis revealed 20.6 % differential expressed contigs, which grouped into 8 clusters according to K-means clustering analysis, responding to CuSO4; 848 contigs were up-regulated and 746 contigs were down-regulated more than 2-fold changes from 12 h to 48 h exposure. KEGG pathway analysis of eukaryotic homologous genes revealed the differentially expressed genes (DEGs) were involved in diverse pathway; amongst, the genes involved in the translation, spliceosome, and/or signal transduction genes were highly regulated. Most of photosystem related genes were down-regulated and most of mitochondria related genes were up-regulated. In addition, the genes involved in the copper ion binding or transporting and antioxidant systems were identified. Measurement of chlorophyll fluorescence showed that photosynthesis was significantly inhibited by CuSO4 exposure.This study reported the first transcriptome of the C. polykrikoides. The widely differential expressed photosystem genes suggested photosynthetic machinery were severely affected, and may further contribute to the cell death. Furthermore, gene translation and transcription processes may be disrupted, inhibiting cell growth and proliferation, and possibly accelerating cell death. However, antioxidant systems resistant to CuSO4 caused stress; mitochondrion may compensate for photosynthesis efficiency decreasing caused energy deficiency. In addition, various signal transduction pathways may be involved in the CuSO4 induced regulation network in the C. polykrikoides. These data provide the potential transcriptomic mechanism to explain the algicide CuSO4 effect on the harmful dinoflagellate C. polykrikoides.

Dataset Information

The harmful algae, Cochlodinium polykrikoides and Aureococcus anophagefferens, elicit stronger transcriptomic and mortality response in larval bivalves (Argopecten irradians) than climate change stressors.

Publications

The harmful algae, <i>Cochlodinium polykrikoides</i> and <i>Aureococcus anophagefferens</i>, elicit stronger transcriptomic and mortality response in larval bivalves (<i>Argopecten irradians</i>) than climate change stressors.

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