RNA-Seq as an Emerging Tool for Marine Dinoflagellate Transcriptome Analysis: Process and Challenges

Akbar, Muhamad Afiq; Ali, Ahmad; Usup, Gires; Bunawan, Hamidun

doi:10.3390/pr6010005

Cited by 11 publications

(10 citation statements)

References 92 publications

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“…Time-series experiments have been thoroughly used to understand transcriptional changes of apicomplexan parasites during infection (Bozdech et al, 2003 ; Wastling et al, 2009 ; Foth et al, 2011 ; Akbar et al, 2018 ). Potentially, a time-course comparison between the expression patterns in the overall gene expression could be of great value to explain common features and adaptations favorable for a parasitic lifestyle for Amoebophrya .…”

Section: Discussionmentioning

confidence: 99%

Comparative Time-Scale Gene Expression Analysis Highlights the Infection Processes of Two Amoebophrya Strains

et al. 2018

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Understanding factors that generate, maintain, and constrain host-parasite associations is of major interest to biologists. Although little studied, many extremely virulent micro-eukaryotic parasites infecting microalgae have been reported in the marine plankton. This is the case for Amoebophrya, a diverse and highly widespread group of Syndiniales infecting and potentially controlling dinoflagellate populations. Here, we analyzed the time-scale gene expression of a complete infection cycle of two Amoebophrya strains infecting the same host (the dinoflagellate Scrippsiella acuminata), but diverging by their host range (one infecting a single host, the other infecting more than one species). Over two-thirds of genes showed two-fold differences in expression between at least two sampled stages of the Amoebophrya life cycle. Genes related to carbohydrate metabolism as well as signaling pathways involving proteases and transporters were overexpressed during the free-living stage of the parasitoid. Once inside the host, all genes related to transcription and translation pathways were actively expressed, suggesting the rapid and extensive protein translation needed following host-cell invasion. Finally, genes related to cellular division and components of the flagellum organization were overexpressed during the sporont stage. In order to gain a deeper understanding of the biological basis of the host-parasitoid interaction, we screened proteins involved in host-cell recognition, invasion, and protection against host-defense identified in model apicomplexan parasites. Very few of the genes encoding critical components of the parasitic lifestyle of apicomplexans could be unambiguously identified as highly expressed in Amoebophrya. Genes related to the oxidative stress response were identified as highly expressed in both parasitoid strains. Among them, the correlated expression of superoxide dismutase/ascorbate peroxidase in the specialist parasite was consistent with previous studies on Perkinsus marinus defense. However, this defense process could not be identified in the generalist Amoebophrya strain, suggesting the establishment of different strategies for parasite protection related to host specificity.

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Section: Discussionmentioning

confidence: 99%

Comparative Time-Scale Gene Expression Analysis Highlights the Infection Processes of Two Amoebophrya Strains

et al. 2018

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“…The extraordinarily huge genome size of saxitoxin-producing dinoflagellates became a hindrance to genomics study, persuading researchers to turn to transcriptomics-based investigation as an alternative methodology that enables large-scale analysis of gene expression and transcriptome profiling [32,33]. Microarray and complementary DNA (cDNA) sequencing are the most common and preferred choices of transcriptomics approaches employed by researchers to investigate the saxitoxin biosynthesis in dinoflagellates.…”

Section: Recent Insight Into Saxitoxin Biosynthesis Through Transcripmentioning

confidence: 99%

Biosynthesis of Saxitoxin in Marine Dinoflagellates: An Omics Perspective

et al. 2020

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Saxitoxin is an alkaloid neurotoxin originally isolated from the clam Saxidomus giganteus in 1957. This group of neurotoxins is produced by several species of freshwater cyanobacteria and marine dinoflagellates. The saxitoxin biosynthesis pathway was described for the first time in the 1980s and, since then, it was studied in more than seven cyanobacterial genera, comprising 26 genes that form a cluster ranging from 25.7 kb to 35 kb in sequence length. Due to the complexity of the genomic landscape, saxitoxin biosynthesis in dinoflagellates remains unknown. In order to reveal and understand the dynamics of the activity in such impressive unicellular organisms with a complex genome, a strategy that can carefully engage them in a systems view is necessary. Advances in omics technology (the collective tools of biological sciences) facilitated high-throughput studies of the genome, transcriptome, proteome, and metabolome of dinoflagellates. The omics approach was utilized to address saxitoxin-producing dinoflagellates in response to environmental stresses to improve understanding of dinoflagellates gene–environment interactions. Therefore, in this review, the progress in understanding dinoflagellate saxitoxin biosynthesis using an omics approach is emphasized. Further potential applications of metabolomics and genomics to unravel novel insights into saxitoxin biosynthesis in dinoflagellates are also reviewed.

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“…The relationship between copy number of the sxtA4 domain and toxin content remains unclear and, so far, the available results suggest that the determination of toxin production is complex, and involves constitutive gene expression associated with processes regulating the level of toxin production ( Yang et al, 2010 ; Wiese et al, 2014 ; Zhang et al, 2017 ; Akbar et al, 2018 ). The use of several gene expression modes, including both transcriptional and post-transcriptional processes, are suspected in dinoflagellates ( Hackett et al, 2013 ; McLean, 2013 ; Roy and Morse, 2013 ).…”

Section: Introductionmentioning

confidence: 99%

From the sxtA4 Gene to Saxitoxin Production: What Controls the Variability Among Alexandrium minutum and Alexandrium pacificum Strains?

et al. 2021

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Paralytic shellfish poisoning (PSP) is a human foodborne syndrome caused by the consumption of shellfish that accumulate paralytic shellfish toxins (PSTs, saxitoxin group). In PST-producing dinoflagellates such as Alexandrium spp., toxin synthesis is encoded in the nuclear genome via a gene cluster (sxt). Toxin production is supposedly associated with the presence of a 4th domain in the sxtA gene (sxtA4), one of the core genes of the PST gene cluster. It is postulated that gene expression in dinoflagellates is partially constitutive, with both transcriptional and post-transcriptional processes potentially co-occurring. Therefore, gene structure and expression mode are two important features to explore in order to fully understand toxin production processes in dinoflagellates. In this study, we determined the intracellular toxin contents of twenty European Alexandrium minutum and Alexandrium pacificum strains that we compared with their genome size and sxtA4 gene copy numbers. We observed a significant correlation between the sxtA4 gene copy number and toxin content, as well as a moderate positive correlation between the sxtA4 gene copy number and genome size. The 18 toxic strains had several sxtA4 gene copies (9–187), whereas only one copy was found in the two observed non-toxin producing strains. Exploration of allelic frequencies and expression of sxtA4 mRNA in 11 A. minutum strains showed both a differential expression and specific allelic forms in the non-toxic strains compared with the toxic ones. Also, the toxic strains exhibited a polymorphic sxtA4 mRNA sequence between strains and between gene copies within strains. Finally, our study supported the hypothesis of a genetic determinism of toxin synthesis (i.e., the existence of several genetic isoforms of the sxtA4 gene and their copy numbers), and was also consistent with the hypothesis that constitutive gene expression and moderation by transcriptional and post-transcriptional regulation mechanisms are the cause of the observed variability in the production of toxins by A. minutum.

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RNA-Seq as an Emerging Tool for Marine Dinoflagellate Transcriptome Analysis: Process and Challenges

Cited by 11 publications

References 92 publications

Comparative Time-Scale Gene Expression Analysis Highlights the Infection Processes of Two Amoebophrya Strains

Comparative Time-Scale Gene Expression Analysis Highlights the Infection Processes of Two Amoebophrya Strains

Biosynthesis of Saxitoxin in Marine Dinoflagellates: An Omics Perspective

From the sxtA4 Gene to Saxitoxin Production: What Controls the Variability Among Alexandrium minutum and Alexandrium pacificum Strains?

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