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microorganisms Review The Genetic Basis of Toxin Biosynthesis in Dinoflagellates Arjun Verma 1,* , Abanti Barua 1,2, Rendy Ruvindy 1, Henna Savela 3, Penelope A. Ajani 1 and Shauna A. Murray 1 1 Climate Change Cluster, University of Technology Sydney, Sydney 2007, Australia 2 Department of Microbiology, Noakhali Science and Technology University, Chittagong 3814, Bangladesh 3 Finnish Environment Institute, Marine Research Centre, 00790 Helsinki, Finland * Correspondence: [email protected] Received: 22 June 2019; Accepted: 27 July 2019; Published: 29 July 2019 Abstract: In marine ecosystems, dinoflagellates can become highly abundant and even dominant at times, despite their comparatively slow growth rates. One factor that may play a role in their ecological success is the production of complex secondary metabolite compounds that can have anti-predator, allelopathic, or other toxic effects on marine organisms, and also cause seafood poisoning in humans. Our knowledge about the genes involved in toxin biosynthesis in dinoflagellates is currently limited due to the complex genomic features of these organisms. Most recently, the sequencing of dinoflagellate transcriptomes has provided us with valuable insights into the biosynthesis of polyketide and alkaloid-based toxin molecules in dinoflagellate species. This review synthesizes the recent progress that has been made in understanding the evolution, biosynthetic pathways, and gene regulation in dinoflagellates with the aid of transcriptomic and other molecular genetic tools, and provides a pathway for future studies of dinoflagellates in this exciting omics era. Keywords: dinoflagellates; toxins; transcriptomics; polyketides; alkaloids 1. Introduction Marine microbial eukaryotes are a diverse group of organisms comprising lineages that differ widely in their evolutionary histories, ecological niches, growth requirements, and nutritional strategies [1–5]. Among marine microbial eukaryotes (protists), dinoflagellates are of immense ecological and evolutionary significance [3,6–8]. Recent studies on protist species richness in the world’s oceans using genetic tools, such as metabarcoding, have shown that approximately half of 18S rDNA richness is made up of dinoflagellate sequences [9,10]. This widespread diversity is due to their ability to adapt to a wide variety of ecological niches, largely depending on their complex survival strategies (such as photoautotrophy, symbiosis, mixotrophy, and heterotrophy) [11,12]. They possess significant variability in morphology, pigment composition, and photosynthetic activity along with a broad spectrum of biological activities that serves various ecological niches. Their occupation of such diverse environments can be witnessed in their fossil records that date back several hundred million years [3,4,11]. Dinoflagellates are relatively inefficient at nutrient uptake, and exhibit slower growth rates compared to other protists such as chlorophytes, haptophytes, and diatoms [13,14]. Despite being poor competitors within their ecosystems, they can at times proliferate in large abundances, causing harmful algal blooms (HABs) [15,16]. Only about 2% of algal species have been reported as producing harmful blooms, of which 75% are dinoflagellates [14]. HABs are naturally occurring phenomena, however there is evidence that the frequency, geographic range, and intensity of these occurrences have increased over the past 30 years [17–20]. While the causes and consequences of HABs have been studied extensively, the production of toxic compounds by the culprit species and their interactions with co-occurring Microorganisms 2019, 7, 222; doi:10.3390/microorganisms7080222 www.mdpi.com/journal/microorganisms Microorganisms 2019, 7, x FOR PEER REVIEW 2 of 29 Microorganisms 2019, 7, 222 2 of 29 studied extensively, the production of toxic compounds by the culprit species and their interactions with co-occurring phytoplankton and potential predators remain to be fully understood [21,22]. Thesephytoplankton compounds and potentialdisplay a predators wide variety remain of to biolog be fullyical understood activity and [21,22 may]. 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Despite function theses studies, of these whether compounds they are is currentlyother as-yet-unidentified unknown [32] (Figure cellular 1). functions of these compounds is currently unknown [32] (Figure1). FigureFigure 1. FunctionalFunctional role role of of toxins producedproduced by dinoflagellates.dinoflagellates. Schematic Schematic representing representing various biologicalbiological roles roles played by toxins for their producing organisms. Photo credit: Diana Diana Kleine, Dieter Tracey, IanIan Hewson, Hewson, Jane Jane Hawkey, Hawkey, Jane Jane Thomas Thomas and Traceyand Tracey Saxby, Saxby, Integration Integration and Application and Application Network, Network,University University of Maryland of Maryland Center for Center Environmental for Environmental Science (ian.umces.edu Science (ian.umces.edu/imagelibrary/)./imagelibrary/). ToxinsToxins produced during HABs can have wide widespreadspread impacts on fisheries fisheries and aquaculture industriesindustries worldwide worldwide [17,33,34]. [17,33,34]. The The most most common common effects effects of of HABs HABs are poisoning events, resulting inin the the deaths deaths of of marine organisms, organisms, and and the the accumulation accumulation of of toxins toxins in in the the marine marine food food web, web, which which maymay lead to eventual human poisoning via the consumption of contaminated seafood [35,36]. [35,36]. It It is is estimatedestimated that that up up to to 60,000 60,000 human human intoxications intoxications o occurccur per per year year worldwide, worldwide, with with an an overall overall mortality mortality ofof approx. 1.5%1.5% [ 37[37,38].,38]. The The potential potential harm harm caused caused to commercially to commercially produced produced seafood seafood by these by marine these marinetoxins, andtoxins, the and associated the associated human human health riskshealth are risks a concern are a concern for seafood for seafood safety regulatorysafety regulatory bodies bodiesworldwide worldwide [39]. The [39]. greatest The greatest number number of HAB of related HAB related human human health impactshealth impacts have occurred have occurred due to duetoxic to compounds toxic compounds that are that classified are classified as; saxitoxin as; saxitoxin (STX) and (STX) its analoguesand its analogues causing paralyticcausing paralytic shellfish shellfishpoisoning poisoning (PSP); brevetoxins (PSP); brevetoxins (BTXs) and(BTXs) analogues and analogues causing causing neurotoxic neurotoxic shellfish shellfish poisoning poisoning (NSP); (NSP);ciguatoxins ciguatoxins (CTXs) (CTXs) and related and related compounds compounds resulting resulting in ciguatera in ciguatera fish poisoning fish poisoning (CFP); and (CFP); okadaic and okadaicacid (OA) acid and (OA) the dinophysis and the dinophysis toxins (DTXs) toxins causing (DTXs) diarrheic causing shellfish diarrheic poisoning shellfish (DSP) poisoning [35,38]. Besides (DSP) Microorganisms 2019, 7, 222 3 of 29 these well-known toxic compounds and their related illnesses, several new poisoning syndromes have recently appeared due to dinoflagellate toxins, such as azaspiracids (AZAs), yessotoxins (YTXs), and palytoxins (PLTXs) [38,40]. Approximately 20,000 marine natural products, with unique size, complexity, and biosynthetic pathways, have been discovered over the past 50 years, of which dinoflagellate toxins represent only a minor fraction, with many more that remain to be described [41]. Over the past 15 years, the first studies have begun to examine the genetic basis of bioactive compounds produced by algae, particularly the toxins synthesized by marine dinoflagellates. These studies have been challenging, largely due to the large size and the distinctive organization of dinoflagellate genomes compared to that of other eukaryotes [5,6]. 2. Dinoflagellate Genomics Dinoflagellate genomes are generally larger than the genomes of most other protists, ranging from 3–250 picograms of DNA per haploid genome, equating to around 1.2–112 109 base pairs [42]. × This genetic material is encoded in 24–220 nuclear