Novel Widespread Marine Oomycetes Parasitising Diatoms, Including the Toxic Genus Pseudo-nitzschia: Genetic, Morphological, and Ecological Characterisation

Abstract

Parasites are key drivers of phytoplankton bloom dynamics and related aquatic ecosystem processes. Yet, the dearth of morphological and molecular information hinders the assessment of their diversity and ecological role. Using single-cell techniques, we characterise morphologically and molecularly, intracellular parasitoids infecting four potentially toxin-producing Pseudo-nitzschia and one Melosira species on the North Atlantic coast. These sequences define two, morphologically indistinguishable clades within the phylum Oomycota, related to the genera of algal parasites Anisolpidium and Olpidiopsis and the diatom parasitoid species Miracula helgolandica. Our morphological data are insufficient to attribute either clade to the still unsequenced genus Ectrogella; hence it is proposed to name the clades OOM_1 and OOM_2. A screening of global databases of the barcode regions V4 and V9 of the 18S rDNA demonstrate the presence of these parasitoids beyond the North Atlantic coastal region. During a biweekly metabarcoding survey (Concarneau Bay, France), reads associated with one sequenced parasitoid coincided with the decline of Cerataulina pelagica bloom, whilst the other parasitoids co-occurred at low abundance with Pseudo-nitzschia. Our data highlight a complex and unexplored diversity of the oomycete parasitoids of diatoms and calls for the investigation of their phenology, evolution, and potential contribution in controlling their host spatial-temporal dynamics.

Phylogeny and cultivation of the holocarpic oomycete Diatomophthora perforans comb. nov., an endoparasitoid of marine diatoms

“…in D. perforans subsp, destruens in Coscinodiscus), additional wall thickening will not take place, as evidenced by the very slight thickening of D. perforans isolates on C. concinnus, while the same isolates would form it on P. intermedium. Therefore, this feature seems not to be constant, which is why a differentiation based on it (Garvetto et al (2018) is probably not reliable. Sparrow (1936) reported that D. perforans zoospores are anteriorly biflagellate and oppositely directed, which is similar to what has been documented in all of the isolates of the current study, and different from previous observations (Petersen 1905(Petersen , 1909Höhnk 1939;Aleem 1953).…”

“…Positive clones were sent for sequencing to the laboratory centre of the Senckenberg Biodiversity and Climate Research Centre (Frankfurt am Main, Germany) using M13 (M13-F, M13-R), T3, and T7 plasmid primers. The resulting sequences were prepared using Geneious (version 5.6), and the assembled sequences of the oomycetes infecting L. abbreviata, S. ulna, C. concinnus and P. intermedium were added to the dataset of Buaya and Thines (2020), to which also additional sequences from Garvetto et al 2018Garvetto et al , 2020 were added, aligned using muscle (Edgar 2004) as implemented in MEGA5 (Tamura et al 2011), with a gap opening penalty of 600 and a gap extension penalty of 6. Phylogenetic analyses were done using MEGA5 for Minimum Evolution analysis with 1000 bootstrap replicates, and on the TrEase webserver (http://thineslab.senckenberg.de/trease/), using RAxML (Stamatakis 2014) for Maximum Likelihood inference, also with 1000 bootstrap replicates.…”

“…Oomycete parasitoids of diatoms are ubiquitous in the aquatic environment (Karling 1942;Sparrow 1960). Despite their widespread occurrence (Garvetto et al 2018;Hassett et al 2019), little is known about the biology and ecology of these holocarpic organisms, especially in marine habitats (Sparrow 1936;Scholz et al 2015;Hassett et al 2019). However, these parasitoids are known to play a significant role in breaking down blooms of their host diatoms, and might also play a role in the marine food web (Skovgaard 2014;Scholz et al 2015).…”

“…However, these parasitoids are known to play a significant role in breaking down blooms of their host diatoms, and might also play a role in the marine food web (Skovgaard 2014;Scholz et al 2015). So far, only three marine oomycetes-infecting diatoms (Lagenisma coscinodisci, Diatomophthora drebesii and Miracula helgolandica) have been classified and studied for molecular phylogeny (Thines et al 2015;Buaya et al 2017), but additional lineages have been identified that have not been formally described (Badis et al 2019;Garvetto et al 2018Garvetto et al , 2020. The Coscinodiscophyceae parasitoid L. coscinodisci was found to belong to the basal Saprolegniomycetes (Thines et al 2015).…”

Analysis of interdomain taxonomic patterns in urban street mats

“…Most likely, these sequences were amplified from fungal spores which would indicate that gutters could act as a vector. A number of known plant and algae (including diatoms) parasites belong to the Oomycetes clade (Kuhn and Hofmann, 1999;Scholz et al, 2016;Garvette et al, 2018;Leonard et al, 2018). Among the Oomycetes, 14 OTUs assigned to the Phytophthora genus were identified in 18 samples.…”