Multiple parallel origins of parasitic Marine Alveolates

Abstract

Microbial eukaryotes are important components of marine ecosystems, and the Marine Alveolates (MALVs) are consistently both abundant and diverse in global environmental sequencing surveys. MALVs are dinoflagellates that are thought to be parasites of other protists and animals, but the lack of data beyond ribosomal RNA gene sequences from all but a few described species means much of their biology and evolution remain unknown. Using single-cell transcriptomes from several MALVs and their free-living relatives, we show that MALVs evolved independently from two distinct, free-living ancestors and that their parasitism evolved in parallel. Phylogenomics shows one subgroup (MALV-II and -IV, or Syndiniales) is related to a novel lineage of free-living, eukaryovorous predators, the eleftherids, while the other (MALV-I, or Ichthyodinida) is related to the free-living predator Oxyrrhis and retains proteins targeted to a non-photosynthetic plastid. Reconstructing the evolution of photosynthesis, plastids, and parasitism in early-diverging dinoflagellates shows a number of parallels with the evolution of their apicomplexan sisters. In both groups, similar forms of parasitism evolved multiple times and photosynthesis was lost many times. By contrast, complete loss of the plastid organelle is infrequent and, when this does happen, leaves no residual genes.

The community of Marine Alveolate parasites in the Atlantic inflow to the Arctic Ocean is structured by season, depth and water mass

“…The enigmatic Marine Alveolates (commonly referred to as MALVs) is a polyphyletic assemblage of parasitic dinoflagellates which are considered to be the dominating group of parasites in marine microbial food webs (Anderson et al 2024;Bjorbaekmo et al 2019;Holt et al 2023). In environmental sequencing studies, MALVs are generally reported to have high abundance and richness in marine pelagic environments (e.g.…”

“…Guillou et al 2008;Koid et al 2012;Massana et al 2011;Vargas et al 2015), including polar waters (Clarke et al 2019;Cleary and Durbin 2016;López-García et al 2001;Lovejoy et al 2006). The existence of high genetic diversity within this group is mostly inferred from environmental sequencing, where a high number of unique rRNA SSU gene sequences are phylogenetically placed next to parasitic dinoflagellate species (Groisillier et al 2006;Guillou et al 2008;Holt et al 2023). Such parasitic dinoflagellates were first described in the 1920s (Chatton 1920) and later in the 1960s (e.g.…”

“…The MALV group was long thought to be a monophyletic sister group to the dinokaryotes (i.e., dinoflagellates with permanently condensed chromosomes, Orr et al 2012), and is often collectively referred to as "Syndiniales" (Holt et al 2023). Based on the rRNA SSU gene, the MALV group is split into two main groups, known in the literature as MALV I and II or Dino-Group (DG) I and II (Groisillier et al 2006;Guillou et al 2008).…”

“…Guillou et al (2008) also established the smaller clades DG-III -V. Since then, the MALV has been shown to be polyphyletic, with DG-II and DG-IV forming a sister clade to the dinokaryotes and DG-I placed basal to these clades in the dinoflagellate phylogeny (Strassert et al 2018). Recently, phylogenomics based on single-cell transcriptomics has shown that DG-I and DG-II/IV evolved independently from two distinct free-living ancestors (Holt et al 2023). The described genera in DG-I are Ichthyodinium, Euduboscquella and Duboscquella, the latter two genera have been isolated from ciliate and other dinoflagellate hosts.…”

“…Amoebophrya and Hematodinium, which are both characterised by the lack of any trace of a plastid are placed in DG-II/IV, along with Syndinium (Amoebophrya in DG-II and Hematodinium and Syndinium both in DG-IV). Holt et al (2023) suggest retaining the name "Syndiniales" for the group DG-II/IV, and using the order "Ichthyodinida" for DG-I. No described species has been assigned to DG-III and DG-V, and it…”